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Ishiyama S. The neurobiology of ticklishness. Neurosci Res 2025; 217:104907. [PMID: 40383199 DOI: 10.1016/j.neures.2025.05.002] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/28/2025] [Accepted: 05/09/2025] [Indexed: 05/20/2025]
Abstract
Ticklishness is an idiosyncratic form of touch observed in multiple animal species, including humans. Although commonly regarded as trivial, it involves complex neurobiological mechanisms and diverse behavioral phenomena observed across species. Two distinct forms exist: knismesis, a mild tingling sensation elicited by gentle touch, and gargalesis, an intense sensation associated with involuntary laughter. Advocating the importance of clearly distinguishing these two types of ticklishness, this review synthesizes current knowledge on their neuronal underpinnings. Topics include somatosensory processing, self-tickling and sensory attenuation, emotional modulation, sociosexual dimensions, and evolutionary perspectives, among others. Special attention is given to the ambivalent nature of gargalesis, challenging conventional single-dimensional models of emotional valence. Ultimately, studying ticklishness provides a valuable opportunity to investigate playful emotional experiences from a naturalistic perspective, addressing fundamental yet underrepresented questions in contemporary neuroscience. Far from trivial, ticklishness thus provides valuable insights into the neural mechanisms underlying complex, context-dependent emotional and social experiences.
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Affiliation(s)
- Shimpei Ishiyama
- Central Institute of Mental Health, Department of Neuropeptide Research in Psychiatry Research Group for Neurobiology of Positive Emotions, J5, Mannheim 68159, Germany.
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2
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Ke J, Song H, Bai Z, Rosenberg MD, Leong YC. Dynamic brain connectivity predicts emotional arousal during naturalistic movie-watching. PLoS Comput Biol 2025; 21:e1012994. [PMID: 40215238 PMCID: PMC12058195 DOI: 10.1371/journal.pcbi.1012994] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/28/2024] [Revised: 05/07/2025] [Accepted: 03/25/2025] [Indexed: 05/09/2025] Open
Abstract
Human affective experience varies along the dimensions of valence (positivity or negativity) and arousal (high or low activation). It remains unclear how these dimensions are represented in the brain and whether the representations are shared across different individuals and diverse situational contexts. In this study, we first utilized two publicly available functional MRI datasets of participants watching movies to build predictive models of moment-to-moment emotional arousal and valence from dynamic functional brain connectivity. We tested the models by predicting emotional arousal and valence both within and across datasets. Our results revealed a generalizable arousal representation characterized by the interactions between multiple large-scale functional networks. The arousal representation generalized to two additional movie-watching datasets with different participants viewing different movies. In contrast, we did not find evidence of a generalizable valence representation. Taken together, our findings reveal a generalizable representation of emotional arousal embedded in patterns of dynamic functional connectivity, suggesting a common underlying neural signature of emotional arousal across individuals and situational contexts. We have made our model and analysis scripts publicly available to facilitate its use by other researchers in decoding moment-to-moment emotional arousal in novel datasets, providing a new tool to probe affective experience using fMRI.
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Affiliation(s)
- Jin Ke
- Department of Psychology, Neuroscience Institute, The University of Chicago, Chicago, Illinois, United States of America
- Department of Psychology, Yale University, New Haven, Connecticut, United States of America
| | - Hayoung Song
- Department of Psychology, Neuroscience Institute, The University of Chicago, Chicago, Illinois, United States of America
- Department of Neuroscience, Washington University School of Medicine, St Louis, Missouri, United States of America
| | - Zihan Bai
- Department of Psychology, Neuroscience Institute, The University of Chicago, Chicago, Illinois, United States of America
- Department of Psychiatry, Yale School of Medicine, New Haven, Connecticut, United States of America
| | - Monica D. Rosenberg
- Department of Psychology, Neuroscience Institute, The University of Chicago, Chicago, Illinois, United States of America
- Institute of Mind and Biology, Neuroscience Institute, The University of Chicago, Chicago, Illinois, United States of America
- Neuroscience Institute, The University of Chicago, Chicago, Illinois, United States of America
| | - Yuan Chang Leong
- Department of Psychology, Neuroscience Institute, The University of Chicago, Chicago, Illinois, United States of America
- Institute of Mind and Biology, Neuroscience Institute, The University of Chicago, Chicago, Illinois, United States of America
- Neuroscience Institute, The University of Chicago, Chicago, Illinois, United States of America
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3
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Tsutsui-Kimura I, Tian ZM, Amo R, Zhuo Y, Li Y, Campbell MG, Uchida N, Watabe-Uchida M. Dopamine in the tail of the striatum facilitates avoidance in threat-reward conflicts. Nat Neurosci 2025; 28:795-810. [PMID: 40065189 PMCID: PMC11976289 DOI: 10.1038/s41593-025-01902-9] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/29/2022] [Accepted: 01/24/2025] [Indexed: 03/23/2025]
Abstract
Responding appropriately to potential threats before they materialize is critical to avoiding disastrous outcomes. Here we examine how threat-coping behavior is regulated by the tail of the striatum (TS) and its dopamine input. Mice were presented with a potential threat (a moving object) while pursuing rewards. Initially, the mice failed to obtain rewards but gradually improved in later trials. We found that dopamine in TS promoted avoidance of the threat, even at the expense of reward acquisition. Furthermore, the activity of dopamine D1 receptor-expressing neurons promoted threat avoidance and prediction. In contrast, D2 neurons suppressed threat avoidance and facilitated overcoming the potential threat. Dopamine axon activation in TS not only potentiated the responses of dopamine D1 receptor-expressing neurons to novel sensory stimuli but also boosted them acutely. These results demonstrate that an opponent interaction of D1 and D2 neurons in the TS, modulated by dopamine, dynamically regulates avoidance and overcoming potential threats.
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Affiliation(s)
- Iku Tsutsui-Kimura
- Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, MA, USA
- Department of Pharmacology, Graduate School of Pharmaceutical Sciences, Hokkaido University, Sapporo, Japan
| | - Zhiyu Melissa Tian
- Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, MA, USA
| | - Ryunosuke Amo
- Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, MA, USA
| | - Yizhou Zhuo
- State Key Laboratory of Membrane Biology, Peking University School of Life Sciences, Beijing, China
- Peking-Tsinghua Center for Life Sciences, Beijing, China
- PKU-IDG/McGovern Institute for Brain Research, Beijing, China
| | - Yulong Li
- State Key Laboratory of Membrane Biology, Peking University School of Life Sciences, Beijing, China
- Peking-Tsinghua Center for Life Sciences, Beijing, China
- PKU-IDG/McGovern Institute for Brain Research, Beijing, China
| | - Malcolm G Campbell
- Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, MA, USA
| | - Naoshige Uchida
- Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, MA, USA
| | - Mitsuko Watabe-Uchida
- Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, MA, USA.
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Jang G, Kragel PA. Understanding human amygdala function with artificial neural networks. J Neurosci 2025; 45:e1436242025. [PMID: 40086868 PMCID: PMC12044042 DOI: 10.1523/jneurosci.1436-24.2025] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/29/2024] [Revised: 01/07/2025] [Accepted: 01/16/2025] [Indexed: 03/16/2025] Open
Abstract
The amygdala is a cluster of subcortical nuclei that receives diverse sensory inputs and projects to the cortex, midbrain, and other subcortical structures. Numerous accounts of amygdalar contributions to social and emotional behavior have been offered, yet an overarching description of amygdala function remains elusive. Here we adopt a computationally explicit framework that aims to develop a model of amygdala function based on the types of sensory inputs it receives, rather than individual constructs such as threat, arousal, or valence. Characterizing human fMRI signal acquired as male and female participants viewed a full-length film, we developed encoding models that predict both patterns of amygdala activity and self-reported valence evoked by naturalistic images. We use deep image synthesis to generate artificial stimuli that distinctly engage encoding models of amygdala subregions that systematically differ from one another in terms of their low-level visual properties. These findings characterize how the amygdala compresses high-dimensional sensory inputs into low-dimensional representations relevant for behavior.Significance Statement The amygdala is a cluster of subcortical nuclei critical for motivation, emotion, and social behavior. Characterizing the contribution of the amygdala to behavior has been challenging due to its structural complexity, broad connectivity, and functional heterogeneity. Here we use a combination of human neuroimaging and computational modeling to investigate how visual inputs relate to low-dimensional representations encoded in the amygdala. We find that the amygdala encodes an array of visual features, which systematically vary across specific nuclei and relate to the affective properties of the sensory environment.
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Monciatti AM, Lapini M, Gemignani J, Frediani G, Carpi F. Unpleasant odors compared to pleasant ones cause higher cortical activations detectable by fNIRS and observable mostly in females. APL Bioeng 2025; 9:016101. [PMID: 39801499 PMCID: PMC11719668 DOI: 10.1063/5.0231217] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/29/2024] [Accepted: 12/05/2024] [Indexed: 01/16/2025] Open
Abstract
Olfactory perception can be studied in deep brain regions at high spatial resolutions with functional magnetic resonance imaging (fMRI), but this is complex and expensive. Electroencephalography (EEG) and functional near-infrared spectroscopy (fNIRS) are limited to cortical responses and lower spatial resolutions but are easier and cheaper to use. Unlike EEG, available fNIRS studies on olfaction are few, limited in scope, and contradictory. Here, we investigated fNIRS efficacy in assessing the hedonic valence of pleasant and unpleasant odors, using ten channels on each hemisphere, covering the orbitofrontal cortex and adjacent areas involved in olfactory and cognitive tasks. Measurements on 22 subjects (11 males and 11 females) showed statistically significant higher increases in oxygenated hemoglobin concentration for the unpleasant odor, compared to the pleasant one (mean difference = 1.025 × 10-1 μM). No difference in activation was found between the hemispheres. Conversely, differences were observed between the sexes: for the first time, we show that higher activations for the unpleasant odor relative to the pleasant one are detectable by fNIRS in females (mean difference = 1.704 × 10-1 μM), but not in an equal-sized and equal-age group of males. Moreover, females had greater activations relative to males for the unpleasant odor (mean difference = 1.285 × 10-1 μM). Therefore, fNIRS can capture peculiarities of olfactory activations, highlighting differences between odors with opposite valence and between sexes. This evidence positions fNIRS next to EEG as suitable technologies for cortical investigations of olfactory perception, providing complementary information (late and early response components, respectively), with lower costs and easier operation (albeit at lower resolutions) compared to fMRI.
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Affiliation(s)
- Anna Maria Monciatti
- Biomedical Engineering Unit, Department of Industrial Engineering, University of Florence, 50121 Florence, Italy
| | - Maddalena Lapini
- Biomedical Engineering Unit, Department of Industrial Engineering, University of Florence, 50121 Florence, Italy
| | | | - Gabriele Frediani
- Biomedical Engineering Unit, Department of Industrial Engineering, University of Florence, 50121 Florence, Italy
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Adrar I, Hervé M, Mantel M, Bony A, Thévenet M, Boachon B, Dejou J, Caissard JC, Bensafi M, Baudino S, Mandairon N. Why do we like so much the smell of roses: The recipe for the perfect flower. iScience 2025; 28:111635. [PMID: 39925418 PMCID: PMC11804596 DOI: 10.1016/j.isci.2024.111635] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/04/2024] [Revised: 07/01/2024] [Accepted: 12/17/2024] [Indexed: 02/11/2025] Open
Abstract
The rose is the most cultivated ornamental plant in the world, and one of the reasons is that its fragrance is highly pleasant to humans. This raises the question of which volatile organic compounds (VOCs) emitted by flowers are involved in a rose odor-induced positive emotional response. Here, we invited participants to smell and rate the perceptual characteristics of roses whose VOCs were quantified. We revealed that (1) the more rose-specific the flower perception, the more pleasant the smell and (2) the rosy perception is driven by ionones and to a lesser extent by oxylipins while pleasantness by balanced proportion in the mixture of ionones, oxylipins, and 2-phenylethanol and derivatives. In the mixture, the proportion of some compounds, such as aliphatics and phenolic methyl esters, impact negatively the rose scent. Thus, the pleasure that roses bring to humans could be explained by the non-conscious perception of this unique mixture of compounds.
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Affiliation(s)
- Inès Adrar
- Lyon Neuroscience Research Center, Neurobiology and Plasticity of Olfactory Perception Team, University Lyon1, Inserm U1028 - CNRS UMR5292, Lyon, France
- Université Jean Monnet Saint-Etienne, CNRS, LBVpam UMR 5079, F-42023 Saint-etienne, France
| | - Maxime Hervé
- IGEPP, INRAE, Institut Agro, University Rennes, Rennes, France
| | - Marylou Mantel
- Laboratory for the Study of Cognitive Mechanisms, Institute of Psychology, University Lyon 2, Bron, France
| | - Aurélie Bony
- Université Jean Monnet Saint-Etienne, CNRS, LBVpam UMR 5079, F-42023 Saint-etienne, France
| | - Marc Thévenet
- Lyon Neuroscience Research Center, Neurobiology and Plasticity of Olfactory Perception Team, University Lyon1, Inserm U1028 - CNRS UMR5292, Lyon, France
| | - Benoît Boachon
- Université Jean Monnet Saint-Etienne, CNRS, LBVpam UMR 5079, F-42023 Saint-etienne, France
| | - Jules Dejou
- Lyon Neuroscience Research Center, Neurobiology and Plasticity of Olfactory Perception Team, University Lyon1, Inserm U1028 - CNRS UMR5292, Lyon, France
| | - Jean-Claude Caissard
- Université Jean Monnet Saint-Etienne, CNRS, LBVpam UMR 5079, F-42023 Saint-etienne, France
| | - Moustafa Bensafi
- Lyon Neuroscience Research Center, Neurobiology and Plasticity of Olfactory Perception Team, University Lyon1, Inserm U1028 - CNRS UMR5292, Lyon, France
| | - Sylvie Baudino
- Université Jean Monnet Saint-Etienne, CNRS, LBVpam UMR 5079, F-42023 Saint-etienne, France
| | - Nathalie Mandairon
- Lyon Neuroscience Research Center, Neurobiology and Plasticity of Olfactory Perception Team, University Lyon1, Inserm U1028 - CNRS UMR5292, Lyon, France
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Kokubun K, Nemoto K, Shiga Y, Makizato Y, Komaki A, Yamakawa Y. Incorporating "kawaii-ness" into your life may increase gray matter volume in the putamen and frontal gyrus. Acta Psychol (Amst) 2025; 252:104663. [PMID: 39701003 DOI: 10.1016/j.actpsy.2024.104663] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/27/2024] [Revised: 12/06/2024] [Accepted: 12/10/2024] [Indexed: 12/21/2024] Open
Abstract
Interest in kawaii-ness is growing day by day around the world. However, the relationship between the brain and kawaii-ness remains unclear. Previous studies have revealed how adults' brains respond to infants, but there is little research into the relationship between non-infant objects that have kawaii-ness and the brain, particularly its structure. Therefore, in this study, using data from 182 healthy men and women, including 90 participants from a toy manufacturer's fan community (TMFC), we analyzed the relationship between the adoption of kawaii-ness and the gray matter volume (GMV) of region of interest (ROI). The results showed that the adoption of kawaii-ness was significantly and positively related to the GMV of the putamen, insula, frontal gyrus (FG), and rectus in the TMFC sample in an analysis that controlled for demographic data. Of these, the significant relationships between putamen and FG and adoption survived multiple comparisons. This is the first study to clarify the relationship between adoption of kawaii-ness and brain structure.
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Affiliation(s)
- Keisuke Kokubun
- Open Innovation Institute, Kyoto University, Kyoto, Japan; Graduate School of Management, Kyoto University, Kyoto, Japan.
| | - Kiyotaka Nemoto
- Department of Psychiatry, Institute of Medicine, University of Tsukuba, Tsukuba, Japan
| | - Yuko Shiga
- Sanrio Entertainment, Co., Ltd., Tama, Tokyo, Japan
| | | | - Aya Komaki
- Sanrio Entertainment, Co., Ltd., Tama, Tokyo, Japan
| | - Yoshinori Yamakawa
- Open Innovation Institute, Kyoto University, Kyoto, Japan; Graduate School of Management, Kyoto University, Kyoto, Japan; Institute of Innovative Research, Tokyo Institute of Technology, Meguro, Tokyo, Japan; ImPACT Program of Council for Science, Technology and Innovation (Cabinet Office, Government of Japan), Chiyoda, Tokyo, Japan; Office for Academic and Industrial Innovation, Kobe University, Kobe, Japan; Brain Impact, Kyoto, Japan
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Mamadaliev D, Kariev G, Asadullaev U, Yakubov J, Khodjimetov DN, Chaurasia B. Transient olfactory hallucinations after insular glioma surgery: a case report. Ann Med Surg (Lond) 2025; 87:387-392. [PMID: 40109605 PMCID: PMC11918605 DOI: 10.1097/ms9.0000000000002849] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/31/2024] [Accepted: 11/27/2024] [Indexed: 03/22/2025] Open
Abstract
Introduction and importance There are various types of hallucinations reported in the literature (auditory, visual, tactile, gustatory, or olfactory), and most of them are related to psychiatric (schizophrenia) disorders. Olfactory hallucinations related to neurosurgical disorders are uncommon. The authors present a case of a patient with a left insular glioma who developed transient olfactory hallucinations after microsurgical resection of the tumor. Our Objective is to share a rare case of postoperative complication-olfactory hallucination following insular glioma surgery-which can potentially raise awareness among practicing neurosurgeons. Case presentation A 32-year-old male patient underwent left insular glioma resection at our institution in 2024. He developed transient olfactory hallucinations after microsurgical resection of the tumor, which resolved within a month postoperatively. Clinical discussion Insular gliomas often grow to a considerable size before becoming symptomatic in many patients. The insular region is regarded as one of the brain's most sophisticated areas, with lesions manifesting in a wide range of symptoms and syndromes including olfactory hallucinations. Conclusion Olfactory hallucinations following left insular glioma resection can potentially raise awareness among practicing neurosurgeons regarding this rare postoperative complication. These types of postoperative complications may resolve in a short period if no serious vascular injury has been encountered.
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Affiliation(s)
- Dilshod Mamadaliev
- Department of Skull Base Neurosurgery, Republican Specialized Scientific-Practical Medical Center of Neurosurgery of Uzbekistan, Tashkent, Uzbekistan
| | - Gayrat Kariev
- Department of Skull Base Neurosurgery, Republican Specialized Scientific-Practical Medical Center of Neurosurgery of Uzbekistan, Tashkent, Uzbekistan
- Department of Neurosurgery, Tashkent State Pediatric Medical Institute, Tashkent, Uzbekistan
| | - Ulugbek Asadullaev
- Department of Skull Base Neurosurgery, Republican Specialized Scientific-Practical Medical Center of Neurosurgery of Uzbekistan, Tashkent, Uzbekistan
| | - Jakhongir Yakubov
- Department of Skull Base Neurosurgery, Republican Specialized Scientific-Practical Medical Center of Neurosurgery of Uzbekistan, Tashkent, Uzbekistan
| | - D N Khodjimetov
- Department of Skull Base Neurosurgery, Republican Specialized Scientific-Practical Medical Center of Neurosurgery of Uzbekistan, Tashkent, Uzbekistan
| | - Bipin Chaurasia
- Department of Neurosurgery, Neurosurgery Clinic, Birgunj, Nepal
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9
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Xu D, Chen B, Yang M, Lin G, Zhang M, Wu Z, Zhou H, Shi X, Peng Q, Zeng Y, Lao J, Wang Q, Liang S, Li J, Yao K, Liu Q, Ou Y, Zhong X, Ning Y. Odor identification dysfunction in late-life depression with suicidal ideation. J Affect Disord 2024; 367:768-776. [PMID: 39233243 DOI: 10.1016/j.jad.2024.08.227] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/16/2024] [Revised: 08/26/2024] [Accepted: 08/31/2024] [Indexed: 09/06/2024]
Abstract
BACKGROUND Suicide is more prevalent among older adults compared to younger individuals. Late-life depression (LLD) poses the highest risk for suicide. However, early recognition of suicidal ideation is challenging. Dysfunction in odor identification (OI), a characteristic of LLD, may hold potential for early identification of suicidal ideation. This study aims to compare OI between LLD patients with suicidal ideation (LLD-S) and LLD patients without suicidal ideation (LLD-NS), and examine its relationship with cognitive function. METHODS A total of 262 LLD-NS patients, 63 LLD-S patients, and 316 healthy normal older adults (HOAs) underwent OI testing, standardized clinical interviews, and comprehensive neuropsychological assessments. RESULTS (1) LLD-S patients exhibited lower OI scores and poorer cognitive performance (including global cognition, information processing speed, memory, language, executive function, and visuospatial ability) compared to LLD-NS patients and HOAs. (2) There were interactive effects between suicidal ideation and OI dysfunction, leading to lower scores in information processing speed and visuospatial ability. (3) OI dysfunction mediated the differences in cognition between the LLD-NS and LLD-S groups. LIMITATIONS The present study was a cross-sectional design. CONCLUSIONS LLD-S patients had worse odor identification than LLD-NS patients and HOAs, suggesting that OI testing could be a valuable approach for identifying suicidal ideation in LLD and screening for suicide risk. The presence of both OI impairment and suicidal ideation was associated with poorer cognitive performance in LLD.
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Affiliation(s)
- Danyan Xu
- The First School of Clinical Medicine, Southern Medical University, Guangzhou, China; Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Ben Chen
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Mingfeng Yang
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Gaohong Lin
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Min Zhang
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Zhangying Wu
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Huarong Zhou
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Xiaolei Shi
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Qi Peng
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Yijie Zeng
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Jingyi Lao
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Qiang Wang
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Shuang Liang
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Jiafu Li
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Kexin Yao
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Qin Liu
- The First School of Clinical Medicine, Southern Medical University, Guangzhou, China; Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China
| | - Yanhong Ou
- Guangzhou Medical University, Guangzhou, China
| | - Xiaomei Zhong
- Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China.
| | - Yuping Ning
- The First School of Clinical Medicine, Southern Medical University, Guangzhou, China; Geriatric Neuroscience Center, The Affiliated Brain Hospital, Guangzhou Medical University, Guangzhou, China; Guangdong Engineering Technology Research Center for Translational Medicine of Mental Disorders, Guangzhou, China; Key Laboratory of Neurogenetics and Channelopathies of Guangdong Province and the Ministry of Education of China, Guangzhou Medical University, Guangzhou, China.
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10
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Hong S, Baek SH, Lai MKP, Arumugam TV, Jo DG. Aging-associated sensory decline and Alzheimer's disease. Mol Neurodegener 2024; 19:93. [PMID: 39633396 PMCID: PMC11616278 DOI: 10.1186/s13024-024-00776-y] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/02/2024] [Accepted: 11/08/2024] [Indexed: 12/07/2024] Open
Abstract
Multisensory decline is common as people age, and aging is the primary risk of Alzheimer's Disease (AD). Recent studies have begun to shed light on the possibility that age-related sensory decline could accelerate AD pathogenesis, or be a prodromal indicator of AD. Sensory impairments, specifically in taste and smell, often emerge before cognitive symptoms in AD, indicating their potential as early biomarkers. Olfactory dysfunction has been frequently associated with AD and may offer valuable insights into early detection. Hearing impairment is significantly associated with AD, but its causal impact on AD progression remains unclear. The review also discusses visual and tactile deficits in AD, including retinal thinning and changes in tactile perception, highlighting their links to disease progression. Focusing on molecular mechanisms, the review explores the roles of amyloid-β (Aβ) accumulation and tau protein pathology in sensory decline and their bidirectional relationship with AD. In summary, the evidence presented conclusively supports advocating for an integrated approach to understanding AD and sensory decline, to enhance early detection, implementing preventive strategies, and developing therapeutic interventions for AD. This approach underscores the significance of sensory health in addressing neurodegenerative diseases, particularly AD.
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Affiliation(s)
- Suji Hong
- The School of Pharmacy, Sungkyunkwan University, Suwon, 16419, Republic of Korea
| | - Seung-Hyun Baek
- The School of Pharmacy, Sungkyunkwan University, Suwon, 16419, Republic of Korea
| | - Mitchell K P Lai
- Department of Pharmacology, Yong Loo Lin School of Medicine, Singapore, 117600, Singapore
| | - Thiruma V Arumugam
- The School of Pharmacy, Sungkyunkwan University, Suwon, 16419, Republic of Korea.
- Centre for Cardiovascular Biology and Disease Research, La Trobe Institute for Molecular Science, Department of Microbiology, Anatomy, Physiology and Pharmacology, School of Agriculture, Biomedicine and Environment, La Trobe University, Melbourne, 3086, Australia.
| | - Dong-Gyu Jo
- The School of Pharmacy, Sungkyunkwan University, Suwon, 16419, Republic of Korea.
- Biomedical Institute for Convergence at SKKU (BICS), Suwon, 16419, Republic of Korea.
- Department of Health Sciences and Technology, SAIHST, Sungkyunkwan University, Seoul, 06355, Republic of Korea.
- Institute of Quantum Biophysics, Sungkyunkwan University, Suwon, 16419, Republic of Korea.
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11
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Bigras C, Duda V, Hébert S. Sensory and affective dimensions in loudness perception: Insights from young adults. Hear Res 2024; 454:109147. [PMID: 39550991 DOI: 10.1016/j.heares.2024.109147] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/12/2024] [Revised: 10/22/2024] [Accepted: 11/02/2024] [Indexed: 11/19/2024]
Abstract
Traditional psychoacoustic measures often lack accuracy in diagnosing hyperacusis and other sound tolerance disorders, possibly due to their reliance on artificial stimuli and unidimensional scales. The aim of this study was to assess loudness across sensory and affective dimensions using natural sounds, drawing on pain research wherein intensity and unpleasantness are assessed separately. We hypothesized that similar distinctions apply to loudness perception. A total of 102 young adults with normal to mild hearing loss rated 32 sound stimuli (pleasant, unpleasant, neutral, and artificial) at 10 intensities (40 to 100 dBA) on sensory and affective scales. They also completed the Hyperacusis Questionnaire, the Noise Sensitivity Scale, and the Hospital Anxiety and Depression Scale. Mixed linear models indicated both correlations and dissociations between scales that varied according to intensity and valence. Louder stimuli were rated as more unpleasant, but only at high intensities. On the sensory scale, sounds were perceived as louder with increasing intensity; however, at low to moderate intensities, pleasant and neutral sounds were rated as louder, whereas at higher intensities, artificial and unpleasant stimuli were rated as louder. On the affective scale, the perception of unpleasantness also increased with intensity, but less steeply. At high intensities, artificial stimuli were rated similarly to unpleasant stimuli. Noise sensitivity scores predicted louder and more unpleasant ratings, whereas depression scores were associated with softer and less pleasant perceptions. This study highlights the need for multidimensional approaches in audiology and suggests that the integration of sensory and affective scales with natural stimuli may improve the diagnosis and treatment of sound tolerance disorders.
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Affiliation(s)
- Charlotte Bigras
- École d'orthophonie et d'audiologie, Faculty of Medicine, Université de Montréal, Montréal, Canada; Centre Interdisciplinaire de Recherche sur le Cerveau et l'Apprentissage (CIRCA), Montréal, Canada; Center for Interdisciplinary Research in Rehabilitation of Metropolitan Montreal (CRIR), Montréal, Canada
| | - Victoria Duda
- École d'orthophonie et d'audiologie, Faculty of Medicine, Université de Montréal, Montréal, Canada; Center for Interdisciplinary Research in Rehabilitation of Metropolitan Montreal (CRIR), Montréal, Canada
| | - Sylvie Hébert
- École d'orthophonie et d'audiologie, Faculty of Medicine, Université de Montréal, Montréal, Canada; Centre Interdisciplinaire de Recherche sur le Cerveau et l'Apprentissage (CIRCA), Montréal, Canada; Center for Interdisciplinary Research in Rehabilitation of Metropolitan Montreal (CRIR), Montréal, Canada.
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12
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Cryns NG, Hardy EG, Roy ARK, Datta S, Sokolowski A, Sturm VE, Kramer JH, Boxer AL, Miller BL, Rosen HJ, Perry DC. Reward processing deficits arise early in familial frontotemporal dementia. Front Neurosci 2024; 18:1491972. [PMID: 39568670 PMCID: PMC11576384 DOI: 10.3389/fnins.2024.1491972] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/05/2024] [Accepted: 10/17/2024] [Indexed: 11/22/2024] Open
Abstract
Reward processing involves evaluation of stimuli to inform what an individual works to pursue or avoid. Patients with behavioral variant frontotemporal dementia (bvFTD) often display reward processing changes, including insensitivity to aversive stimuli. It is unknown how early in the disease course reward changes are detectable. We recruited mutation positive (symptomatic and asymptomatic) and negative members of families with known mutations in progranulin (GRN), microtubule-associated protein tau (MAPT) and chromosome 9 open reading frame 72 (C9orf72). The sample included 4 groups: asymptomatic non-carriers (n = 34), asymptomatic carriers [Clinical Dementia Rating (CDR) 0, n = 16], mildly symptomatic carriers (CDR 0.5, n = 10) and bvFTD (sporadic and genetic, n = 45). A series of tasks utilized pleasant, unpleasant, and neutral olfactants to probe reward consumption and effort to obtain reward. A group by valence interaction showed unpleasant scent ratings were more positive in groups with greater disease severity [χ2(6) = 87.983, p < 0.001]. Mildly symptomatic carriers showed a small difference in ratings of pleasant and unpleasant stimuli, similar to bvFTD. In an effort task, where participants chose to avoid or receive scents, mildly symptomatic carriers and bvFTD chose to smell unpleasant scents more frequently than asymptomatic groups, with mildly symptomatic carriers exceeding bvFTD in their frequency of choosing to smell unpleasant scents. In this same task, motivated effort, determined by rate of button press, determined success at obtaining or avoiding scents. Success rate, calculated based on the number of responses where participants' button presses exceeded an individual threshold set in a practice trial, differed across groups (p = 0.048), driven by mildly symptomatic carriers, who were consistently unsuccessful. There was a group difference in variability in button press rate across trials (p = 0.007), driven by mildly symptomatic carriers who showed less varied effort between scents. These findings suggest alterations to reward functioning can be detected early in bvFTD, even before meeting diagnostic criteria. These results may aid in identifying distinctive, initial reward changes in bvFTD that can facilitate early and accurate diagnosis and inspire efforts to identify anatomic underpinnings of early symptomatic changes.
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Affiliation(s)
| | | | | | | | | | | | | | | | | | | | - David C. Perry
- Department of Neurology, Memory and Aging Center, UCSF Weill Institute for Neurosciences, University of California San Francisco, San Francisco, CA, United States
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13
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Chen Y, Yang C, Gao B, Chen K, Jao Keehn RJ, Müller RA, Yuan LX, You Y. Altered Functional Connectivity of Unimodal Sensory and Multisensory Integration Networks Is Related to Symptom Severity in Autism Spectrum Disorder. BIOLOGICAL PSYCHIATRY. COGNITIVE NEUROSCIENCE AND NEUROIMAGING 2024:S2451-9022(24)00313-6. [PMID: 39491786 DOI: 10.1016/j.bpsc.2024.10.014] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 08/15/2024] [Revised: 10/11/2024] [Accepted: 10/22/2024] [Indexed: 11/05/2024]
Abstract
BACKGROUND Atypical sensory processing is a prevalent feature of autism spectrum disorder (ASD) and constitutes a core diagnostic criterion in DSM-5. However, the neurocognitive underpinnings of atypical unimodal and multimodal sensory processing and their relationships with autism symptoms remain unclear. METHODS In this study, we examined intrinsic functional connectivity (FC) patterns among 5 unimodal sensory and multisensory integration (MSI) networks in ASD using a large multisite dataset (N = 646) and investigated the relationships between altered FC, atypical sensory processing, social communicative deficits, and overall autism symptoms using correlation and mediation analyses. RESULTS Compared with typically developing control participants, participants in the ASD group demonstrated increased FC of the olfactory network, decreased FC within the MSI network, and decreased FC of the MSI-unimodal sensory networks. Furthermore, altered FC was positively associated with autism symptom severity, and such associations were completely mediated by atypical sensory processing and social communicative deficits. CONCLUSIONS ASD-specific olfactory overconnectivity and MSI-unimodal sensory underconnectivity lend support to the intense world theory and weak central coherence theory, suggesting olfactory hypersensitivity at the expense of MSI as a potential neural mechanism underlying atypical sensory processing in ASD. These atypical FC patterns suggest potential targets for psychological and neuromodulatory interventions.
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Affiliation(s)
- Yahui Chen
- Department of Psychology and Behavioral Sciences, Zhejiang University, Hangzhou, Zhejiang, China
| | - Chen Yang
- Center for Cognition and Brain Disorders, The Affiliated Hospital of Hangzhou Normal University, Hangzhou, Zhejiang, China; Institute of Psychological Sciences, Hangzhou Normal University, Hangzhou, Zhejiang, China; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments, Hangzhou, Zhejiang, China
| | - Bicheng Gao
- Department of Psychology and Behavioral Sciences, Zhejiang University, Hangzhou, Zhejiang, China
| | - Kehui Chen
- Institute of Psychological Sciences, Hangzhou Normal University, Hangzhou, Zhejiang, China
| | - R Joanne Jao Keehn
- Department of Psychology, San Diego State University, San Diego, California
| | - Ralph-Axel Müller
- Department of Psychology, San Diego State University, San Diego, California
| | - Li-Xia Yuan
- School of Physics, Zhejiang University, Hangzhou, Zhejiang, China.
| | - Yuqi You
- Department of Psychology and Behavioral Sciences, Zhejiang University, Hangzhou, Zhejiang, China.
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14
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Giraud M, Javadi AH, Lenatti C, Allen J, Tamè L, Nava E. The role of the somatosensory system in the feeling of emotions: a neurostimulation study. Soc Cogn Affect Neurosci 2024; 19:nsae062. [PMID: 39275796 PMCID: PMC11488518 DOI: 10.1093/scan/nsae062] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/20/2024] [Revised: 06/27/2024] [Accepted: 09/12/2024] [Indexed: 09/16/2024] Open
Abstract
Emotional experiences deeply impact our bodily states, such as when we feel 'anger', our fists close and our face burns. Recent studies have shown that emotions can be mapped onto specific body areas, suggesting a possible role of the primary somatosensory system (S1) in emotion processing. To date, however, the causal role of S1 in emotion generation remains unclear. To address this question, we applied transcranial alternating current stimulation (tACS) on the S1 at different frequencies (beta, theta, and sham) while participants saw emotional stimuli with different degrees of pleasantness and levels of arousal. Results showed that modulation of S1 influenced subjective emotional ratings as a function of the frequency applied. While theta and beta-tACS made participants rate the emotional images as more pleasant (higher valence), only theta-tACS lowered the subjective arousal ratings (more calming). Skin conductance responses recorded throughout the experiment confirmed a different arousal for pleasant versus unpleasant stimuli. Our study revealed that S1 has a causal role in the feeling of emotions, adding new insight into the embodied nature of emotions. Importantly, we provided causal evidence that beta and theta frequencies contribute differently to the modulation of two dimensions of emotions-arousal and valence-corroborating the view of a dissociation between these two dimensions of emotions.
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Affiliation(s)
- Michelle Giraud
- Department of Psychology, University of Milano-Bicocca, Milano 20126, Italy
- School of Psychology, University of Kent, Canterbury CT2 7NZ, United Kingdom
- Psychology Department and NeuroMi, Milan Centre of Neuroscience, University of Milano-Bicocca, Milan 20126, Italy
| | - Amir-Homayoun Javadi
- School of Psychology, University of Kent, Canterbury CT2 7NZ, United Kingdom
- School of Rehabilitation, Tehran University of Medical Sciences, Tehran 1416634793, Iran
| | - Carmen Lenatti
- School of Psychology, University of Kent, Canterbury CT2 7NZ, United Kingdom
| | - John Allen
- School of Psychology, University of Kent, Canterbury CT2 7NZ, United Kingdom
| | - Luigi Tamè
- School of Psychology, University of Kent, Canterbury CT2 7NZ, United Kingdom
| | - Elena Nava
- Department of Psychology, University of Milano-Bicocca, Milano 20126, Italy
- Psychology Department and NeuroMi, Milan Centre of Neuroscience, University of Milano-Bicocca, Milan 20126, Italy
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15
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Kehl MS, Mackay S, Ohla K, Schneider M, Borger V, Surges R, Spehr M, Mormann F. Single-neuron representations of odours in the human brain. Nature 2024; 634:626-634. [PMID: 39385026 PMCID: PMC11485236 DOI: 10.1038/s41586-024-08016-5] [Citation(s) in RCA: 1] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/27/2023] [Accepted: 09/04/2024] [Indexed: 10/11/2024]
Abstract
Olfaction is a fundamental sensory modality that guides animal and human behaviour1,2. However, the underlying neural processes of human olfaction are still poorly understood at the fundamental-that is, the single-neuron-level. Here we report recordings of single-neuron activity in the piriform cortex and medial temporal lobe in awake humans performing an odour rating and identification task. We identified odour-modulated neurons within the piriform cortex, amygdala, entorhinal cortex and hippocampus. In each of these regions, neuronal firing accurately encodes odour identity. Notably, repeated odour presentations reduce response firing rates, demonstrating central repetition suppression and habituation. Different medial temporal lobe regions have distinct roles in odour processing, with amygdala neurons encoding subjective odour valence, and hippocampal neurons predicting behavioural odour identification performance. Whereas piriform neurons preferably encode chemical odour identity, hippocampal activity reflects subjective odour perception. Critically, we identify that piriform cortex neurons reliably encode odour-related images, supporting a multimodal role of the human piriform cortex. We also observe marked cross-modal coding of both odours and images, especially in the amygdala and piriform cortex. Moreover, we identify neurons that respond to semantically coherent odour and image information, demonstrating conceptual coding schemes in olfaction. Our results bridge the long-standing gap between animal models and non-invasive human studies and advance our understanding of odour processing in the human brain by identifying neuronal odour-coding principles, regional functional differences and cross-modal integration.
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Affiliation(s)
- Marcel S Kehl
- Department of Epileptology, University Hospital Bonn, Bonn, Germany
- Department of Experimental Psychology, University of Oxford, Oxford, UK
| | - Sina Mackay
- Department of Epileptology, University Hospital Bonn, Bonn, Germany
| | - Kathrin Ohla
- Science & Research, dsm-firmenich, Satigny, Switzerland
| | | | - Valeri Borger
- Department of Neurosurgery, University Hospital Bonn, Bonn, Germany
| | - Rainer Surges
- Department of Epileptology, University Hospital Bonn, Bonn, Germany
| | - Marc Spehr
- Department of Chemosensation, Institute for Biology II, RWTH Aachen University, Aachen, Germany.
| | - Florian Mormann
- Department of Epileptology, University Hospital Bonn, Bonn, Germany.
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16
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Yao F, Chang X, Zhou B, Zhou W. Olfaction modulates cortical arousal independent of perceived odor intensity and pleasantness. Neuroimage 2024; 299:120843. [PMID: 39251115 DOI: 10.1016/j.neuroimage.2024.120843] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/02/2024] [Revised: 08/22/2024] [Accepted: 09/06/2024] [Indexed: 09/11/2024] Open
Abstract
Throughout history, various odors have been harnessed to invigorate or relax the mind. The mechanisms underlying odors' diverse arousal effects remain poorly understood. We conducted five experiments (184 participants) to investigate this issue, using pupillometry, electroencephalography, and the attentional blink paradigm, which exemplifies the limit in attentional capacity. Results demonstrated that exposure to citral, compared to vanillin, enlarged pupil size, reduced resting-state alpha oscillations and alpha network efficiency, augmented beta-gamma oscillations, and enhanced the coordination between parietal alpha and frontal beta-gamma activities. In parallel, it attenuated the attentional blink effect. These effects were observed despite citral and vanillin being comparable in perceived odor intensity, pleasantness, and nasal pungency, and were unlikely driven by semantic biases. Our findings reveal that odors differentially alter the small-worldness of brain network architecture, and thereby brain state and arousal. Furthermore, they establish arousal as a unique dimension in olfactory space, distinct from intensity and pleasantness.
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Affiliation(s)
- Fangshu Yao
- State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing 100049, China; School of Psychology, Shanghai University of Sport, Shanghai 200438, China
| | - Xiaoyue Chang
- State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing 100049, China
| | - Bin Zhou
- State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing 100049, China.
| | - Wen Zhou
- State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing 100049, China; Chinese Institute for Brain Research, Beijing 102206, China.
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17
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Ferry RA, Shah VV, Jin J, Jarcho JM, Hajcak G, Nelson BD. Neural response to monetary and social rewards in adolescent girls and their parents. Neuroimage 2024; 297:120705. [PMID: 38914211 DOI: 10.1016/j.neuroimage.2024.120705] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/01/2023] [Revised: 06/14/2024] [Accepted: 06/21/2024] [Indexed: 06/26/2024] Open
Abstract
Functional magnetic resonance imaging (fMRI) studies have indicated that the mesocorticolimbic dopamine system is heavily involved in all stages of reward processing. However, the majority of research has been conducted using monetary rewards and it is unclear to what extent other types of rewards, such as social rewards, evoke similar or different neural activation. There have also been few investigations into potential differences or similarities between reward processing in parents and offspring. The present study examined fMRI neural activation in response to monetary and social reward in a sample of 14-22-year-old adolescent girls (N = 145) and a biological parent (N = 124) and compared activation across adolescent-parent dyads (N = 82). Across all participants, both monetary and social reward elicited bilateral striatal activation, which did not differ between reward types or between adolescents and their parents. Neural activation in response to the different reward types were positively correlated in the striatum among adolescents and in the mPFC and OFC among parents. Overall, the present study suggests that both monetary and social reward elicit striatal activation regardless of age and provides evidence that neural mechanisms underlying reward processing may converge differentially among youth and adults.
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Affiliation(s)
- Rachel A Ferry
- Department of Psychology, Stony Brook University, 100 Nicolls Rd, Stony Brook, NY 11794-2500, USA.
| | - Virja V Shah
- Department of Psychology, Stony Brook University, 100 Nicolls Rd, Stony Brook, NY 11794-2500, USA
| | - Jingwen Jin
- Department of Psychology, University of Hong Kong, The Jockey Club Tower, Centennial Campus, Pokfulam Road, Hong Kong
| | - Johanna M Jarcho
- Department of Psychology and Neuroscience, Temple University, 1701N 13th St, Philadelphia, PA 19122, USA
| | - Greg Hajcak
- School of Education and Counseling Psychology, Santa Clara University, 455 El Camino Real, Santa Clara, CA 95053, USA
| | - Brady D Nelson
- Department of Psychology, Stony Brook University, 100 Nicolls Rd, Stony Brook, NY 11794-2500, USA
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18
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Zhao LS, Raithel CU, Tisdall MD, Detre JA, Gottfried JA. Leveraging Multi-Echo EPI to Enhance BOLD Sensitivity in Task-based Olfactory fMRI. BIORXIV : THE PREPRINT SERVER FOR BIOLOGY 2024:2024.01.15.575530. [PMID: 38293143 PMCID: PMC10827088 DOI: 10.1101/2024.01.15.575530] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 02/01/2024]
Abstract
Functional magnetic resonance imaging (fMRI) using blood-oxygenation-level-dependent (BOLD) contrast relies on gradient echo echo-planar imaging (GE-EPI) to quantify dynamic susceptibility changes associated with the hemodynamic response to neural activity. However, acquiring BOLD fMRI in human olfactory regions is particularly challenging due to their proximity to the sinuses where large susceptibility gradients induce magnetic field distortions. BOLD fMRI of the human olfactory system is further complicated by respiratory artifacts that are highly correlated with event onsets in olfactory tasks. Multi-echo EPI (ME-EPI) acquires gradient echo data at multiple echo times (TEs) during a single acquisition and can leverage signal evolution over the multiple echo times to enhance BOLD sensitivity and reduce artifactual signal contributions. In the current study, we developed a ME-EPI acquisition protocol for olfactory task-based fMRI and demonstrated significant improvement in BOLD signal sensitivity over conventional single-echo EPI (1E-EPI). The observed improvement arose from both an increase in BOLD signal changes through a T 2 * -weighted echo combination and a reduction in non-BOLD artifacts through the application of the Multi-Echo Independent Components Analysis (ME-ICA) denoising method. This study represents one of the first direct comparisons between 1E-EPI and ME-EPI in high-susceptibility regions and provides compelling evidence in favor of using ME-EPI for future task-based fMRI studies.
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19
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Jang G, Kragel PA. Understanding human amygdala function with artificial neural networks. BIORXIV : THE PREPRINT SERVER FOR BIOLOGY 2024:2024.07.29.605621. [PMID: 39131372 PMCID: PMC11312467 DOI: 10.1101/2024.07.29.605621] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Subscribe] [Scholar Register] [Indexed: 08/13/2024]
Abstract
The amygdala is a cluster of subcortical nuclei that receives diverse sensory inputs and projects to the cortex, midbrain and other subcortical structures. Numerous accounts of amygdalar contributions to social and emotional behavior have been offered, yet an overarching description of amygdala function remains elusive. Here we adopt a computationally explicit framework that aims to develop a model of amygdala function based on the types of sensory inputs it receives, rather than individual constructs such as threat, arousal, or valence. Characterizing human fMRI signal acquired as participants viewed a full-length film, we developed encoding models that predict both patterns of amygdala activity and self-reported valence evoked by naturalistic images. We use deep image synthesis to generate artificial stimuli that distinctly engage encoding models of amygdala subregions that systematically differ from one another in terms of their low-level visual properties. These findings characterize how the amygdala compresses high-dimensional sensory inputs into low-dimensional representations relevant for behavior.
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20
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Heidari F, Shiran MB, Kaheni H, Karami A, Zare-Sadeghi A. An fMRI-based investigation of the effects of odors on the functional connectivity network underlying the working memory. Exp Brain Res 2024; 242:1561-1571. [PMID: 38753044 DOI: 10.1007/s00221-024-06848-1] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/17/2024] [Accepted: 05/07/2024] [Indexed: 06/27/2024]
Abstract
In the human brain, the regions responsible for emotion processing, motivation, and memory are heavily influenced by olfaction, whose neural pathway is directly exposed to the outer world. In this study, we used fMRI to examine how different olfactory conditions might affect the functional connectivity circuit underlying working memory in the brain. To this end, 30 adults (aged 20-35), 13 males and 17 females, with high educational levels were chosen. Participants were screened for potential olfactory issues before undergoing the Sniffin' sticks test, which was part of the inclusion criteria. Before imaging, each participant was given the required level of training and was then asked to complete four olfactory tests involving pleasant and unpleasant odors, air, and null stimulation. The results of Seed-based analysis suggested a function connection between the inferior parietal region and the left frontal pole region upon olfactory stimulation with vanilla scent in contrast to null stimulation in this comparison, ROI-based analysis revealed an inverse synchronous among the entorhinal cortex, orbitofrontal cortex, and dorsolateral prefrontal cortex (dlPFC). Both dlPFC and hippocampus were involved in olfactory discrimination between two different stimulants. Our findings indicate the presence of inverse correlations between several regions associated with olfaction and working memory, with pleasant scents leaving a stronger impact on the working memory-related areas, particularly the inferior parietal region.
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Affiliation(s)
- Faezeh Heidari
- Clinical Neuroscience and Neuroimaging, Department of Neurology, Institute of Clinical Medicine, University of Eastern Finland, Kuopio, Finland
| | - Mohammad Bagher Shiran
- Finetech in Medicine Research Center, School of Medicine, Iran University of Medical Sciences (IUMS), Tehran, Iran
- Department of Medical Physics, School of Medicine, Iran University of Medical Science (IUMS), Tehran, Iran
| | - Haniyeh Kaheni
- Finetech in Medicine Research Center, School of Medicine, Iran University of Medical Sciences (IUMS), Tehran, Iran
- Department of Medical Physics, School of Medicine, Iran University of Medical Science (IUMS), Tehran, Iran
| | - Asra Karami
- Finetech in Medicine Research Center, School of Medicine, Iran University of Medical Sciences (IUMS), Tehran, Iran
- Department of Medical Physics, School of Medicine, Iran University of Medical Science (IUMS), Tehran, Iran
| | - Arash Zare-Sadeghi
- Finetech in Medicine Research Center, School of Medicine, Iran University of Medical Sciences (IUMS), Tehran, Iran.
- Department of Medical Physics, School of Medicine, Iran University of Medical Science (IUMS), Tehran, Iran.
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21
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Gabriel DB, Havugimana F, Liley AE, Aguilar I, Yeasin M, Simon NW. Lateral Orbitofrontal Cortex Encodes Presence of Risk and Subjective Risk Preference During Decision-Making. BIORXIV : THE PREPRINT SERVER FOR BIOLOGY 2024:2024.04.08.588332. [PMID: 38645204 PMCID: PMC11030364 DOI: 10.1101/2024.04.08.588332] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 04/23/2024]
Abstract
Adaptive decision-making requires consideration of objective risks and rewards associated with each option, as well as subjective preference for risky/safe alternatives. Inaccurate risk/reward estimations can engender excessive risk-taking, a central trait in many psychiatric disorders. The lateral orbitofrontal cortex (lOFC) has been linked to many disorders associated with excessively risky behavior and is ideally situated to mediate risky decision-making. Here, we used single-unit electrophysiology to measure neuronal activity from lOFC of freely moving rats performing in a punishment-based risky decision-making task. Subjects chose between a small, safe reward and a large reward associated with either 0% or 50% risk of concurrent punishment. lOFC activity repeatedly encoded current risk in the environment throughout the decision-making sequence, signaling risk before, during, and after a choice. In addition, lOFC encoded reward magnitude, although this information was only evident during action selection. A Random Forest classifier successfully used neural data accurately to predict the risk of punishment in any given trial, and the ability to predict choice via lOFC activity differentiated between and risk-preferring and risk-averse rats. Finally, risk preferring subjects demonstrated reduced lOFC encoding of risk and increased encoding of reward magnitude. These findings suggest lOFC may serve as a central decision-making hub in which external, environmental information converges with internal, subjective information to guide decision-making in the face of punishment risk.
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Affiliation(s)
- Daniel B.K. Gabriel
- Department of Psychiatry, Indiana University School of Medicine, Indianapolis, IN 46202
| | - Felix Havugimana
- Department of Computer Engineering, University of Memphis, Memphis, TN, 38152
| | - Anna E. Liley
- Institut du Cerveau/Paris Brain Institute, Paris, France, 75013
| | - Ivan Aguilar
- Department of Psychology, University of Memphis, Memphis, TN, 38152
| | - Mohammed Yeasin
- Department of Computer Engineering, University of Memphis, Memphis, TN, 38152
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22
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Zou L, Qi Y, Shen L, Huang Y, Huang J, Xia Z, Fan M, Fan W, Chai GB, Shi QZ, Zhang Q, Yan C. The neural representations of valence transformation in indole processing. Cereb Cortex 2024; 34:bhae167. [PMID: 38652554 DOI: 10.1093/cercor/bhae167] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/16/2024] [Revised: 03/18/2024] [Accepted: 03/20/2024] [Indexed: 04/25/2024] Open
Abstract
Indole is often associated with a sweet and floral odor typical of jasmine flowers at low concentrations and an unpleasant, animal-like odor at high concentrations. However, the mechanism whereby the brain processes this opposite valence of indole is not fully understood yet. In this study, we aimed to investigate the neural mechanisms underlying indole valence encoding in conversion and nonconversion groups using the smelling task to arouse pleasantness. For this purpose, 12 conversion individuals and 15 nonconversion individuals participated in an event-related functional magnetic resonance imaging paradigm with low (low-indole) and high (high-indole) indole concentrations in which valence was manipulated independent of intensity. The results of this experiment showed that neural activity in the right amygdala, orbitofrontal cortex and insula was associated with valence independent of intensity. Furthermore, activation in the right orbitofrontal cortex in response to low-indole was positively associated with subjective pleasantness ratings. Conversely, activation in the right insula and amygdala in response to low-indole was positively correlated with anticipatory hedonic traits. Interestingly, while amygdala activation in response to high-indole also showed a positive correlation with these hedonic traits, such correlation was observed solely with right insula activation in response to high-indole. Additionally, activation in the right amygdala in response to low-indole was positively correlated with consummatory pleasure and hedonic traits. Regarding olfactory function, only activation in the right orbitofrontal cortex in response to high-indole was positively correlated with olfactory identification, whereas activation in the insula in response to low-indole was negatively correlated with the level of self-reported olfactory dysfunction. Based on these findings, valence transformation of indole processing in the right orbitofrontal cortex, insula, and amygdala may be associated with individual hedonic traits and perceptual differences.
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Affiliation(s)
- Laiquan Zou
- Chemical Senses and Mental Health Lab, Department of Psychology, School of Public Health, Southern Medical University, South Shatai Road 1023, Guangzhou 510515, China
| | - Yue Qi
- Chemical Senses and Mental Health Lab, Department of Psychology, School of Public Health, Southern Medical University, South Shatai Road 1023, Guangzhou 510515, China
| | - Lei Shen
- Key Laboratory of Brain Functional Genomics (MOE & STCSM), Shanghai Changning-ECNU Mental Health Center, School of Psychology and Cognitive Science, East China Normal University, North Zhongshan Road 3663, Shanghai 200062, China
- Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, North Zhongshan Road 3663, Shanghai 20062, China
| | - Yanyang Huang
- Chemical Senses and Mental Health Lab, Department of Psychology, School of Public Health, Southern Medical University, South Shatai Road 1023, Guangzhou 510515, China
| | - Jiayu Huang
- Chemical Senses and Mental Health Lab, Department of Psychology, School of Public Health, Southern Medical University, South Shatai Road 1023, Guangzhou 510515, China
| | - Zheng Xia
- Key Laboratory of Brain Functional Genomics (MOE & STCSM), Shanghai Changning-ECNU Mental Health Center, School of Psychology and Cognitive Science, East China Normal University, North Zhongshan Road 3663, Shanghai 200062, China
- Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, North Zhongshan Road 3663, Shanghai 20062, China
| | - Mingxia Fan
- Key Laboratory of Brain Functional Genomics (MOE & STCSM), Shanghai Changning-ECNU Mental Health Center, School of Psychology and Cognitive Science, East China Normal University, North Zhongshan Road 3663, Shanghai 200062, China
| | - Wu Fan
- Zhengzhou Tobacco Research Institute of CNTC, Fengyang Road 2, Zhengzhou 450001, China
| | - Guo-Bi Chai
- Zhengzhou Tobacco Research Institute of CNTC, Fengyang Road 2, Zhengzhou 450001, China
| | - Qing-Zhao Shi
- Zhengzhou Tobacco Research Institute of CNTC, Fengyang Road 2, Zhengzhou 450001, China
| | - Qidong Zhang
- Zhengzhou Tobacco Research Institute of CNTC, Fengyang Road 2, Zhengzhou 450001, China
| | - Chao Yan
- Key Laboratory of Brain Functional Genomics (MOE & STCSM), Shanghai Changning-ECNU Mental Health Center, School of Psychology and Cognitive Science, East China Normal University, North Zhongshan Road 3663, Shanghai 200062, China
- Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, North Zhongshan Road 3663, Shanghai 20062, China
- Key Laboratory of Philosophy and Social Science of Anhui Province on Adolescent Mental Health and Crisis Intelligence Intervention, South Jiuhua Road 189, Hefei 241002, China
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Kokubun K, Nemoto K, Yamakawa Y. Continuous inhalation of essential oil increases gray matter volume. Brain Res Bull 2024; 208:110896. [PMID: 38331299 DOI: 10.1016/j.brainresbull.2024.110896] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/31/2023] [Revised: 12/22/2023] [Accepted: 02/05/2024] [Indexed: 02/10/2024]
Abstract
Research into the health benefits of scents is on the rise. However, little is known about the effects of continuous inhalation, such as wearing scents on clothing, on brain structure. Therefore, in this study, an intervention study was conducted on a total of 50 healthy female people, 28 in the intervention group and 22 in the control group, asking them to wear a designated rose scent on their clothes for a month. The effect of continuous inhalation of essential oil on the gray matter of the brain was measured by calculating changes in brain images of participants taken before and after the intervention using Magnetic Resonance Imaging (MRI). The results showed that the intervention increased the gray matter volume (GMV) of the whole brain and posterior cingulate cortex (PCC) subregion. On the other hand, the GMV of the amygdala and orbitofrontal cortex (OFC) did not change. This study is the first to show that continuous scent inhalation changes brain structure.
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Affiliation(s)
- Keisuke Kokubun
- Open Innovation Institute, Kyoto University, Kyoto, Japan; Graduate School of Management, Kyoto University, Kyoto, Japan.
| | - Kiyotaka Nemoto
- Department of Psychiatry, Institute of Medicine, University of Tsukuba, Tsukuba, Japan
| | - Yoshinori Yamakawa
- Open Innovation Institute, Kyoto University, Kyoto, Japan; Graduate School of Management, Kyoto University, Kyoto, Japan; Institute of Innovative Research, Tokyo Institute of Technology, Meguro, Tokyo, Japan; ImPACT Program of Council for Science, Technology and Innovation (Cabinet Office, Government of Japan), Chiyoda, Tokyo, Japan; Office for Academic and Industrial Innovation, Kobe University, Kobe, Japan; Brain Impact, Kyoto, Japan
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24
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Schwen Blackett D, Borod JC, Speer SR, Pan X, Harnish SM. The effects of emotional stimuli on Word retrieval in people with aphasia. Neuropsychologia 2024; 192:108734. [PMID: 37952713 PMCID: PMC10833091 DOI: 10.1016/j.neuropsychologia.2023.108734] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/24/2023] [Revised: 10/07/2023] [Accepted: 11/08/2023] [Indexed: 11/14/2023]
Abstract
PURPOSE Prior studies have shown that people with aphasia (PWA) have demonstrated superior language performance for emotional compared to nonemotional stimuli on a range of tasks, including auditory comprehension, verbal pragmatics, repetition, reading, and writing. However, studies on word retrieval, specifically, have suggested a possible interference effect of emotion on naming. The purpose of this study was to examine the effect of the emotional valence of stimuli on word retrieval in a series of naming tasks in PWA. METHOD Thirteen PWA and 13 neurotypical controls participated in four single-word naming tasks, including 1) object picture naming, 2) action picture naming, 3) category-member generation, and 4) verb generation. Each task included three valence sets of positively-, negatively-, and neutrally-rated pictures or words, which were obtained from the standardized International Affective Picture System (Lang et al., 2008) and the Affective Norms for Emotional Words (Bradley and Lang, 1999) databases. Accuracy and reaction time (RT) were measured and compared across groups, tasks, and valence sets. RESULTS Emotional stimuli, especially negative stimuli, resulted in worse naming performance, as measured by accuracy and RT, compared to nonemotional stimuli in PWA and neurotypical controls. This effect was relatively robust across the four naming tasks. In most cases, negative stimuli resulted in lower accuracy and slower RT than positive stimuli. CONCLUSIONS These findings suggest that stimulus valence may interfere with word retrieval for PWA and neurotypical adults and that this effect is robust across different types of naming tasks that vary by word class (nouns versus verbs) and stimulus type (pictures versus words). Negative stimuli resulted in worse naming performance than positive stimuli. These results suggest that emotionality of stimuli is an important variable to consider in word retrieval research.
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Affiliation(s)
- Deena Schwen Blackett
- Department of Speech and Hearing Science, College of Arts & Sciences, The Ohio State University, 110 Pressey Hall, 1070 Carmack Road, Columbus, OH, 43210, USA.
| | - Joan C Borod
- Department of Psychology, Queens College of the City University of New York, 65-30 Kissena Blvd, Flushing, NY, 11367, USA.
| | - Shari R Speer
- Department of Linguistics, College of Arts & Sciences, The Ohio State University, Oxley Hall, 1712 Neil Ave, Columbus, OH, 43210, USA.
| | - Xueliang Pan
- Center for Biostatistics, Department of Biomedical Informatics, The Ohio State University, 310-H Lincoln Tower, 1800 Cannon Drive, Columbus, OH, 43210, USA.
| | - Stacy M Harnish
- Department of Speech and Hearing Science, College of Arts & Sciences, The Ohio State University, 110 Pressey Hall, 1070 Carmack Road, Columbus, OH, 43210, USA.
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25
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Alahäivälä ALI, Thaploo D, Wein S, Seidel P, Riebel M, Hummel T, Schwarzbach JV. Inhalation-modulated detection of olfactory BOLD responses in the human brain. FRONTIERS IN NEUROIMAGING 2023; 2:1260893. [PMID: 38107774 PMCID: PMC10725246 DOI: 10.3389/fnimg.2023.1260893] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 07/18/2023] [Accepted: 11/02/2023] [Indexed: 12/19/2023]
Abstract
Introduction In contrast to other sensory domains, detection of primary olfactory processes using functional magnetic resonance imaging has proven to be notably challenging with conventional block designs. This difficulty arises from significant habituation and hemodynamic responses in olfactory areas that do not appear to align with extended boxcar functions convolved with a generic hemodynamic response model. Consequently, some researchers have advocated for a transition to event-related designs, despite their known lower detection power compared to block designs. Methods Here, we conducted a block design experiment with 16s of continuous odorant stimulation alternating with 16s of continuous odorless air stimulation in 33 healthy participants. We compared four statistical analyses that relied either on standard block designs (SBD1-2) or on block designs that were modulated by the participants' individual breathing patterns (MBD1-2). Results We found that such modulated block designs were comparatively more powerful than standard block designs, despite having a substantially lower design efficiency. Using whole-brain effect size maps, we observed that the right insular and medial aspects of the left piriform cortex exhibited a preference for a breathing-modulated analysis approach. Discussion Research in olfaction that necessitates designs with longer-lasting blocks, such as those employed in the investigation of state-dependent processing, will benefit from the breathing-modulated analyses outlined in this study.
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Affiliation(s)
- Aino-Lotta I. Alahäivälä
- Biomedical Imaging Group, Department of Psychiatry and Psychotherapy, University of Regensburg, Regensburg, Germany
| | - Divesh Thaploo
- Interdisciplinary Center Smell and Taste, Department of Otorhinolaryngology, Technische Universität Dresden, Dresden, Germany
| | - Simon Wein
- Biomedical Imaging Group, Department of Psychiatry and Psychotherapy, University of Regensburg, Regensburg, Germany
| | - Philipp Seidel
- Biomedical Imaging Group, Department of Psychiatry and Psychotherapy, University of Regensburg, Regensburg, Germany
| | - Marco Riebel
- Biomedical Imaging Group, Department of Psychiatry and Psychotherapy, University of Regensburg, Regensburg, Germany
| | - Thomas Hummel
- Interdisciplinary Center Smell and Taste, Department of Otorhinolaryngology, Technische Universität Dresden, Dresden, Germany
| | - Jens Volkmar Schwarzbach
- Biomedical Imaging Group, Department of Psychiatry and Psychotherapy, University of Regensburg, Regensburg, Germany
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Sagar V, Shanahan LK, Zelano CM, Gottfried JA, Kahnt T. High-precision mapping reveals the structure of odor coding in the human brain. Nat Neurosci 2023; 26:1595-1602. [PMID: 37620443 PMCID: PMC10726579 DOI: 10.1038/s41593-023-01414-4] [Citation(s) in RCA: 11] [Impact Index Per Article: 5.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/26/2022] [Accepted: 07/18/2023] [Indexed: 08/26/2023]
Abstract
Odor perception is inherently subjective. Previous work has shown that odorous molecules evoke distributed activity patterns in olfactory cortices, but how these patterns map on to subjective odor percepts remains unclear. In the present study, we collected neuroimaging responses to 160 odors from 3 individual subjects (18 h per subject) to probe the neural coding scheme underlying idiosyncratic odor perception. We found that activity in the orbitofrontal cortex (OFC) represents the fine-grained perceptual identity of odors over and above coarsely defined percepts, whereas this difference is less pronounced in the piriform cortex (PirC) and amygdala. Furthermore, the implementation of perceptual encoding models enabled us to predict olfactory functional magnetic resonance imaging responses to new odors, revealing that the dimensionality of the encoded perceptual spaces increases from the PirC to the OFC. Whereas encoding of lower-order dimensions generalizes across subjects, encoding of higher-order dimensions is idiosyncratic. These results provide new insights into cortical mechanisms of odor coding and suggest that subjective olfactory percepts reside in the OFC.
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Affiliation(s)
- Vivek Sagar
- Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA
| | | | - Christina M Zelano
- Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA
| | - Jay A Gottfried
- Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA
- Department of Psychology, University of Pennsylvania, Philadelphia, PA, USA
| | - Thorsten Kahnt
- National Institute on Drug Abuse Intramural Research Program, Baltimore, MD, USA.
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27
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Wang L, Li J, Pan Y, Huang P, Li D, Voon V. Subacute alpha frequency (10Hz) subthalamic stimulation for emotional processing in Parkinson's disease. Brain Stimul 2023; 16:1223-1231. [PMID: 37567462 DOI: 10.1016/j.brs.2023.08.005] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/18/2023] [Revised: 05/21/2023] [Accepted: 08/07/2023] [Indexed: 08/13/2023] Open
Abstract
BACKGROUND Psychiatric comorbidities are common in Parkinson's disease (PD) and may change with high-frequency stimulation targeting the subthalamic nucleus. Numerous accounts indicate subthalamic alpha-frequency oscillation is implicated in emotional processing. While intermittent alpha-frequency (10Hz) stimulation induces positive emotional effects, with more ventromedial contacts inducing larger effects, little is known about the subacute effect of ventral 10Hz subthalamic stimulation on emotional processing. OBJECTIVE/HYPOTHESIS To evaluate the subacute effect of 10Hz stimulation at bilateral ventral subthalamic nucleus on emotional processing in PD patients using an affective task, compared to that of clinical-frequency stimulation and off-stimulation. METHODS Twenty PD patients with bilateral subthalamic deep brain stimulation for more than six months were tested with the affective task under three stimulation conditions (10Hz, 130Hz, and off-stimulation) in a double-blinded randomized design. RESULTS While 130Hz stimulation reduced arousal ratings in all patients, 10Hz stimulation increased arousal selectively in patients with higher depression scores. Furthermore, 10Hz stimulation induced a positive shift in valence rating to negative emotional stimuli in patients with lower apathy scores, and 130Hz stimulation led to more positive valence to emotional stimuli in the patients with higher apathy scores. Notably, we found correlational relationships between stimulation site and affective rating: arousal ratings increase with stimulation from anterior to posterior site, and positive valence ratings increase with stimulation from dorsal to ventral site of the ventral subthalamic nucleus. CONCLUSIONS Our findings highlight the distinctive role of 10Hz stimulation on subjective emotional experience and unveil the spatial organization of the stimulation effect.
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Affiliation(s)
- Linbin Wang
- Institute of Science and Technology for Brain-Inspired Intelligence (ISTBI), Fudan University, Shanghai, China; Department of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Jun Li
- School of Information Science and Technology, ShanghaiTech University, Shanghai, China
| | - Yixin Pan
- Department of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Peng Huang
- Department of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Dianyou Li
- Department of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
| | - Valerie Voon
- Institute of Science and Technology for Brain-Inspired Intelligence (ISTBI), Fudan University, Shanghai, China; Department of Psychiatry, University of Cambridge, Cambridge, United Kingdom.
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Lillqvist M, Claeson AS, Zakrzewska M, Andersson L. Comparable responses to a wide range of olfactory stimulation in women and men. Sci Rep 2023; 13:9059. [PMID: 37270617 DOI: 10.1038/s41598-023-35936-5] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/20/2023] [Accepted: 05/25/2023] [Indexed: 06/05/2023] Open
Abstract
The evidence for differences between women and men in terms of olfactory abilities is contradictory. We analyzed women and men's performance and reactions to a wider range of odour exposure outcomes than usually studied, to assess possible differences and similarities between sexes. Measures of sensitivity and sensory decision rule were established in 37 women and 39 men. Perceptual, cognitive, symptom-related and autonomic nervous system (skin conductance level and heart-rate variability) reactions were also assessed during extended ambient odour exposure, as well as participants' self-rated chemical intolerance. Bayesian analyses consistently revealed greater support for sex-related similarities than differences, suggesting that women and men perform and react comparably not only in terms of basic olfactory measures, but also to environmental odour exposure mimicking everyday situations.
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Affiliation(s)
- Moa Lillqvist
- Department of Psychology, Umeå University, Umeå, Sweden.
| | | | - Marta Zakrzewska
- Department of Clinical Neuroscience, Karolinska Institute, Solna, Sweden
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Peng L, Peng Y, Luo H, Deng Y. How high-intensity sensory consumption fills up resource scarcity: The boundary condition of self-acceptance. PLoS One 2023; 18:e0285853. [PMID: 37235592 PMCID: PMC10218729 DOI: 10.1371/journal.pone.0285853] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/18/2022] [Accepted: 05/02/2023] [Indexed: 05/28/2023] Open
Abstract
OBJECTIVE Everyone in life will experience resource scarcity, which causes self-discrepancy. It is widely known that individuals participate in reactive consumption to solve the problems of self-discrepancy and resources scarcity. This kind of consumption may be symbolically related to the essence of the resource scarcity or may occur in an unrelated domain. This study proposes a theory for "filling up" one's resource scarcity through high-intensity sensory consumption (HISC). METHODS We used different methods, including one-way analysis of variance (ANOVA), linear regression, mediating effect, and moderating effect, to test the four hypotheses. Four experiments in the study were conducted from May 2022 and August 2022 and involved undergraduates from a university and volunteers recruited online. All participants are adults and verbally agree to participate voluntarily. Study 1a (N = 96 (male 47, female 49), participants from a business school in China) measured resource scarcity in the laboratory experiments and verified the effect of resource scarcity on consumer HISC preference by using linear regression (H1). Study 1b (N = 191 (male 98, female 93), students and teachers from a university in China) measured resource scarcity in the laboratory experiments and manipulated positively and negatively valenced experiences. Using the PROCESS SPSS Mode l, we verified that negatively valenced stimuli also lead to higher levels of arousal, which in turn restores the self-discrepancy caused by resource scarcity (H2). Study 2 (an online experiment, N = 182 (male 91, female 91), participants from China) manipulated the resource scarcity in a color sensory stimulant context, replicating the preliminary effect and examined the mediating effect of the self-worth by using the PROCESS SPSS Mode 4 (H3). Study 3 (an online experiment, N = 251 (male 125, female 126), participants from China) manipulated resource scarcity and self-acceptance in the tactile sensory experience, and tested the moderating effect of self-acceptance by using the PROCESS SPSS Mode 8 (H4). RESULTS Four studies suggest that not only do individuals facing resources scarcity prefer HISC but also that this consumption is mediated and moderated by self-worth and self-acceptance, respectively. This preference for HISC is negated when individuals have high self-acceptance traits. The findings are tested in the auditory domain (as evidenced by a propensity for louder volume), the visual domain (as evidenced by a propensity for more intense colors), and the tactile domain (as evidenced by a propensity for more intense need for touch). The findings also demonstrate that individual preferences for HISC is shown to operate regardless of the valence (positive valence vs. negative valence) of the sensory consumption. CONCLUSIONS Across four experiments, we find that individuals who are subjected to resource scarcity show a preference for high-intensity sensory consumption in the auditory, visual, and tactile domains. We also find that both negatively and positively valenced sensory stimuli have the same impact on resource-scarce individuals' preference for HISC. Furthermore, we demonstrate that the sense of self-worth significantly mediates the effect of resource scarcity on HISC. Finally, we reveal that self-acceptance moderates the effect of resource scarcity on HISC preference.
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Affiliation(s)
- Liangjun Peng
- School of Economics and Management, Chongqing Jiaotong University, Chongqing, China
| | - Yuxin Peng
- College of Life Sciences, Henan Normal University, Xinxiang, Henan, China
| | - Haiyan Luo
- School of Education, Universiti Teknologi Malaysia, Johor Bahru, Malaysia
| | - Yeying Deng
- Faculty of Economics and Management, Universiti Kebangsaan Malaysia, Bangi Selangor, Malaysia
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Cieri F, Cera N, Ritter A, Cordes D, Caldwell JZK. Olfaction and Anxiety Are Differently Associated in Men and Women in Cognitive Physiological and Pathological Aging. J Clin Med 2023; 12:2338. [PMID: 36983338 PMCID: PMC10054317 DOI: 10.3390/jcm12062338] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/21/2023] [Revised: 03/07/2023] [Accepted: 03/11/2023] [Indexed: 03/19/2023] Open
Abstract
BACKGROUND Olfaction impairment in aging is associated with increased anxiety. We explored this association in cognitively healthy controls (HCs), Mild Cognitive Impairment (MCI) and Parkinson's disease (PD) patients. Both olfaction and anxiety have sex differences, therefore we also investigated these variances. OBJECTIVES Investigate the association of olfaction with anxiety in three distinct clinical categories of aging, exploring the potential role of sex. METHODS 117 subjects (29 HCs, 43 MCI, and 45 PD patients) were assessed for olfaction and anxiety. We used regression models to determine whether B-SIT predicted anxiety and whether sex impacted that relationship. RESULTS Lower olfaction was related to greater anxiety traits in all groups (HCs: p = 0.015; MCI: p = 0.001 and PD: p = 0.038), significantly differed by sex. In fact, in HCs, for every unit increase in B-SIT, anxiety traits decreased by 7.63 in men (p = 0.009) and 1.5 in women (p = 0.225). In MCI patients for every unit increase in B-SIT, anxiety traits decreased by 1.19 in men (p = 0.048) and 3.03 in women (p = 0.0036). Finally, in PD patients for every unit increase in B-SIT, anxiety traits decreased by 1.73 in men (p = 0.004) and 0.41 in women (p = 0.3632). DISCUSSION Olfaction and anxiety are correlated in all three distinct diagnostic categories, but differently in men and women.
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Affiliation(s)
- Filippo Cieri
- Department of Neurology, Cleveland Clinic Lou Ruvo Center for Brain Health, Las Vegas, NV 89106, USA
| | - Nicoletta Cera
- Laboratory of Neuropsychophysiology, Faculty of Psychology and Education Sciences, University of Porto, 4200-135 Porto, Portugal
- CIBIT—Coimbra Institute for Biomedical Imaging and Translational Research, University of Coimbra, 3000-548 Coimbra, Portugal
| | - Aaron Ritter
- Department of Neurology, Cleveland Clinic Lou Ruvo Center for Brain Health, Las Vegas, NV 89106, USA
| | - Dietmar Cordes
- Department of Neurology, Cleveland Clinic Lou Ruvo Center for Brain Health, Las Vegas, NV 89106, USA
- Department of Brain Health, University of Nevada, Las Vegas, NV 89154, USA
- Department of Psychology and Neuroscience, University of Colorado, Boulder, CO 80309, USA
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Tu L, Wang Z, Lv X, Xie T, Fan Z, Zhang M, Wang H, Yu X. Characteristics of Odor Identification and Hedonics and Their Association with Piriform Cortex-Based Resting-State Functional Connectivity in Amnestic Mild Cognitive Impairment. J Alzheimers Dis 2023; 94:247-258. [PMID: 37212099 DOI: 10.3233/jad-221163] [Citation(s) in RCA: 2] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 05/23/2023]
Abstract
BACKGROUND Olfactory identification dysfunction (OID) might be an early sign of amnestic mild cognitive impairment (aMCI). However, odor hedonics, the ability to perceive odor pleasantness, is neglected. Also, the neural substrate of OID remains unclear. OBJECTIVE To explore the characteristics of odor identification and hedonics in aMCI and examine the potential neural correlates of OID by analyzing olfactory functional connectivity (FC) patterns in MCI. METHODS Forty-five controls and 83 aMCI patients were examined. The Chinese smell identification test was used to assess olfaction. Global cognition, memory, and social cognition were assessed. Resting-state functional networks associated with olfactory cortex seeds were compared between the cognitively normal (CN) and aMCI groups, as well as between aMCI subgroups by the degree of OID. RESULTS Compared to controls, aMCI patients had a significant deficit in olfactory identification, mainly reflected in the identification of pleasant and neutral odors. aMCI patients also rated pleasant and neutral odors much lower than controls. A positive correlation between olfaction and social cognition was found in aMCI. The seed-based FC analysis found that aMCI patients had higher FC between the right orbitofrontal cortex and right frontal lobe/middle frontal gyrus than controls. Subgroup analysis showed that, compared to aMCI without OID, aMCI with severe OID had abnormal FC in the bilateral piriform region. CONCLUSION Our results suggest that OID in aMCI primarily refers to the identification of pleasant and neutral odors. The FC alterations in bilateral orbitofrontal cortex and piriform cortices might contribute to the impairment in odor identification.
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Affiliation(s)
- Lihui Tu
- Dementia Care and Research Center, Clinical Research Division, Peking University Institute of Mental Health, Sixth Hospital, Haidian District, Beijing, China
- Beijing Dementia Key Lab, National Clinical Research Center for Mental Disorders, Key Laboratory of Mental Health, Ministry of Health, Peking University, Beijing, China
- The National Clinical Research Center for Mental Disorders & Beijing Key Laboratory of Mental Disorders, Beijing Anding Hospital, Capital Medical University, Beijing, China
| | - Zhijiang Wang
- Dementia Care and Research Center, Clinical Research Division, Peking University Institute of Mental Health, Sixth Hospital, Haidian District, Beijing, China
- Beijing Dementia Key Lab, National Clinical Research Center for Mental Disorders, Key Laboratory of Mental Health, Ministry of Health, Peking University, Beijing, China
| | - Xiaozhen Lv
- Dementia Care and Research Center, Clinical Research Division, Peking University Institute of Mental Health, Sixth Hospital, Haidian District, Beijing, China
- Beijing Dementia Key Lab, National Clinical Research Center for Mental Disorders, Key Laboratory of Mental Health, Ministry of Health, Peking University, Beijing, China
| | - Teng Xie
- Dementia Care and Research Center, Clinical Research Division, Peking University Institute of Mental Health, Sixth Hospital, Haidian District, Beijing, China
- Beijing Dementia Key Lab, National Clinical Research Center for Mental Disorders, Key Laboratory of Mental Health, Ministry of Health, Peking University, Beijing, China
| | - Zili Fan
- Dementia Care and Research Center, Clinical Research Division, Peking University Institute of Mental Health, Sixth Hospital, Haidian District, Beijing, China
- Beijing Dementia Key Lab, National Clinical Research Center for Mental Disorders, Key Laboratory of Mental Health, Ministry of Health, Peking University, Beijing, China
- The National Clinical Research Center for Mental Disorders & Beijing Key Laboratory of Mental Disorders, Beijing Anding Hospital, Capital Medical University, Beijing, China
| | - Ming Zhang
- Dementia Care and Research Center, Clinical Research Division, Peking University Institute of Mental Health, Sixth Hospital, Haidian District, Beijing, China
- Beijing Dementia Key Lab, National Clinical Research Center for Mental Disorders, Key Laboratory of Mental Health, Ministry of Health, Peking University, Beijing, China
- Department of Psychiatry, the Third Affiliated Hospital of Sun Yat-Sen University, Guangzhou, China
| | - Huali Wang
- Dementia Care and Research Center, Clinical Research Division, Peking University Institute of Mental Health, Sixth Hospital, Haidian District, Beijing, China
- Beijing Dementia Key Lab, National Clinical Research Center for Mental Disorders, Key Laboratory of Mental Health, Ministry of Health, Peking University, Beijing, China
| | - Xin Yu
- Dementia Care and Research Center, Clinical Research Division, Peking University Institute of Mental Health, Sixth Hospital, Haidian District, Beijing, China
- Beijing Dementia Key Lab, National Clinical Research Center for Mental Disorders, Key Laboratory of Mental Health, Ministry of Health, Peking University, Beijing, China
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Kazour F, Atanasova B, Mourad M, El Hachem C, Desmidt T, Richa S, El-Hage W. Mania associated olfactory dysfunction: A comparison between bipolar subjects in mania and remission. J Psychiatr Res 2022; 156:330-338. [PMID: 36323136 DOI: 10.1016/j.jpsychires.2022.10.038] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/03/2022] [Revised: 10/07/2022] [Accepted: 10/17/2022] [Indexed: 11/06/2022]
Abstract
OBJECTIVES The aim of this study was to assess the olfactory functions of patients with bipolar disorder in manic phase and to compare them to those of bipolar subjects in remission and healthy controls. METHODS We recruited 96 participants divided in 3 groups: bipolar mania (MB), euthymic bipolar in remission (EB) and healthy controls (HC). All participants underwent an assessment of their olfactory functions using the Sniffin' sticks threshold and identification tests. Odors' pleasantness, intensity, familiarity and emotion were assessed. All participants were screened for the presence of psychiatric disorder through the MINI questionnaire. Clinical evaluation explored dimensions of mania, depression, anxiety respectively through YMRS, MADRS and STAI scales. Anhedonia was explored through the Chapman physical and social anhedonia questionnaire. RESULTS Patients in mania had deficits in identifying positive smells compared to bipolar subjects in remission and to healthy controls (MB < EB < HC; p < 0.001). Hedonic (MB < EB = HC; p < 0.001) and emotional (MB < EB = HC; p < 0.001) ratings of positive smells were lower in patients in manic phase compared to remitted subjects or controls. Mania was associated to higher emotion rating of negative smells compared to remitted subjects and controls (MB > EB = HC; p < 0.001). There was no difference between the 3 groups in the ratings of intensity and familiarity of smells, as well as in the olfactory threshold testing. The 3 groups showed no difference in the identification of negative smells. CONCLUSIONS Patients in manic episodes showed deficits in identifying positive odors. They evaluated these smells as less pleasant and less emotional compared to remitted bipolar subjects and healthy controls. These olfactory dysfunctions may constitute potential indicators of manic state. The persistence of olfactory dysfunction in remission phase (deficit in the olfactory identification of positive odors compared to healthy controls) may constitute a potential trait indicator of bipolarity.
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Affiliation(s)
- Francois Kazour
- UMR 1253, iBrain, Université de Tours, INSERM, Tours, France; Clinique Psychiatrique Universitaire, CHU de Tours, Tours, France; Department of Psychiatry, Faculty of Medicine, Saint Joseph University, Beirut, Lebanon.
| | | | - Marc Mourad
- Department of Psychiatry, Faculty of Medicine, Saint Joseph University, Beirut, Lebanon
| | - Charline El Hachem
- Department of Psychiatry, Faculty of Medicine, Saint Joseph University, Beirut, Lebanon
| | - Thomas Desmidt
- UMR 1253, iBrain, Université de Tours, INSERM, Tours, France; Clinique Psychiatrique Universitaire, CHU de Tours, Tours, France
| | - Sami Richa
- Department of Psychiatry, Faculty of Medicine, Saint Joseph University, Beirut, Lebanon
| | - Wissam El-Hage
- UMR 1253, iBrain, Université de Tours, INSERM, Tours, France; Clinique Psychiatrique Universitaire, CHU de Tours, Tours, France
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Sabiniewicz A, Zimmermann P, Ozturk GA, Warr J, Hummel T. Effects of odors on sleep quality in 139 healthy participants. Sci Rep 2022; 12:17165. [PMID: 36229501 PMCID: PMC9562345 DOI: 10.1038/s41598-022-21371-5] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/05/2022] [Accepted: 09/27/2022] [Indexed: 01/04/2023] Open
Abstract
The present study aimed to systematically examine whether laurinal, orange odor, and a specifically designed "perfume" influence sleep quality. During sleep, healthy participants (n = 139) were presented with odor or no odor through nose clips for fourteen consecutive nights (phase one). We collected physiological parameters together with subjective reports. Later on, longer lasting effects of this manipulation were examined for the following fourteen nights (phase two) without exposition to odors. Additionally, olfactory, cognitive and non-cognitive measures were conducted before phase one, between both phases and after phase two. One-way analyses of variance for repeated measures with nights and condition (1 vs 2) as the within-subject factor and odor condition (0, 1, 2 or 3) together with odor pleasantness rating as between-subject factor, was employed to analyse data. Overall, the present results demonstrated that the odor condition in comparison to control had no consistent effect on sleep in healthy participants which can be possibly explained by exposure to odors via nose clips. However, the analyses indicated that the individual pleasantness of odors enhanced the positive assessment of sleep quality. Altogether, the present results indicate that the subjective perception of an odor's hedonic value appears to be crucial for sleep quality, not the odors themselves.
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Affiliation(s)
- Agnieszka Sabiniewicz
- Interdisciplinary Center "Smell & Taste", Department of Otorhinolaryngology, TU Dresden, Dresden, Germany.
| | - Pia Zimmermann
- Interdisciplinary Center "Smell & Taste", Department of Otorhinolaryngology, TU Dresden, Dresden, Germany
| | - Guliz Akin Ozturk
- Interdisciplinary Center "Smell & Taste", Department of Otorhinolaryngology, TU Dresden, Dresden, Germany
- Dokuz Eylul University, Izmir, Turkey
| | | | - Thomas Hummel
- Interdisciplinary Center "Smell & Taste", Department of Otorhinolaryngology, TU Dresden, Dresden, Germany
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34
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Pu D, Shan Y, Wang J, Sun B, Xu Y, Zhang W, Zhang Y. Recent trends in aroma release and perception during food oral processing: A review. Crit Rev Food Sci Nutr 2022; 64:3441-3457. [PMID: 36218375 DOI: 10.1080/10408398.2022.2132209] [Citation(s) in RCA: 26] [Impact Index Per Article: 8.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/07/2023]
Abstract
The dynamic and complex peculiarities of the oral environment present several challenges for controlling the aroma release during food consumption. They also pose higher requirements for designing food with better sensory quality. This requires a comprehensive understanding of the basic rules of aroma transmission and aroma perception during food oral processing and its behind mechanism. This review summarized the latest developments in aroma release from food to retronasal cavity, aroma release and delivery influencing factors, aroma perception mechanisms. The individual variance is the most important factor affecting aroma release and perception. Therefore, the intelligent chewing simulator is the key to establish a standard analytical method. The key odorants perceived from the retronasal cavity should be given more attention during food oral processing. Identification of the olfactory receptor activated by specific odorants and its binding mechanisms are still the bottleneck. Electrophysiology and image technology are the new noninvasive technologies in elucidating the brain signals among multisensory, which can fill the gap between aroma perception and other senses. Moreover, it is necessary to develop a new approach to integrate the relationship among aroma binding parameters, aroma concentration, aroma attributes and cross-modal reactions to make the aroma prediction model more accurate.
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Affiliation(s)
- Dandan Pu
- Beijing Key Laboratory of Flavor Chemistry, Beijing Technology and Business University (BTBU), Beijing, China
| | - Yimeng Shan
- Beijing Key Laboratory of Flavor Chemistry, Beijing Technology and Business University (BTBU), Beijing, China
| | - Juan Wang
- Beijing Key Laboratory of Flavor Chemistry, Beijing Technology and Business University (BTBU), Beijing, China
| | - Baoguo Sun
- Beijing Key Laboratory of Flavor Chemistry, Beijing Technology and Business University (BTBU), Beijing, China
| | - Youqiang Xu
- Beijing Key Laboratory of Flavor Chemistry, Beijing Technology and Business University (BTBU), Beijing, China
| | - Wangang Zhang
- College of Food Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu, China
| | - Yuyu Zhang
- Beijing Key Laboratory of Flavor Chemistry, Beijing Technology and Business University (BTBU), Beijing, China
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35
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Karim AKMR, Proulx MJ, de Sousa AA, Likova LT. Do we enjoy what we sense and perceive? A dissociation between aesthetic appreciation and basic perception of environmental objects or events. COGNITIVE, AFFECTIVE & BEHAVIORAL NEUROSCIENCE 2022; 22:904-951. [PMID: 35589909 PMCID: PMC10159614 DOI: 10.3758/s13415-022-01004-0] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Accepted: 03/27/2022] [Indexed: 05/06/2023]
Abstract
This integrative review rearticulates the notion of human aesthetics by critically appraising the conventional definitions, offerring a new, more comprehensive definition, and identifying the fundamental components associated with it. It intends to advance holistic understanding of the notion by differentiating aesthetic perception from basic perceptual recognition, and by characterizing these concepts from the perspective of information processing in both visual and nonvisual modalities. To this end, we analyze the dissociative nature of information processing in the brain, introducing a novel local-global integrative model that differentiates aesthetic processing from basic perceptual processing. This model builds on the current state of the art in visual aesthetics as well as newer propositions about nonvisual aesthetics. This model comprises two analytic channels: aesthetics-only channel and perception-to-aesthetics channel. The aesthetics-only channel primarily involves restricted local processing for quality or richness (e.g., attractiveness, beauty/prettiness, elegance, sublimeness, catchiness, hedonic value) analysis, whereas the perception-to-aesthetics channel involves global/extended local processing for basic feature analysis, followed by restricted local processing for quality or richness analysis. We contend that aesthetic processing operates independently of basic perceptual processing, but not independently of cognitive processing. We further conjecture that there might be a common faculty, labeled as aesthetic cognition faculty, in the human brain for all sensory aesthetics albeit other parts of the brain can also be activated because of basic sensory processing prior to aesthetic processing, particularly during the operation of the second channel. This generalized model can account not only for simple and pure aesthetic experiences but for partial and complex aesthetic experiences as well.
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Affiliation(s)
- A K M Rezaul Karim
- Department of Psychology, University of Dhaka, Dhaka, 1000, Bangladesh.
- Envision Research Institute, 610 N. Main St., Wichita, KS, USA.
- The Smith-Kettlewell Eye Research Institute, 2318 Fillmore St., San Francisco, CA, USA.
| | | | | | - Lora T Likova
- The Smith-Kettlewell Eye Research Institute, 2318 Fillmore St., San Francisco, CA, USA
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36
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Mastinu M, Melis M, Yousaf NY, Barbarossa IT, Tepper BJ. Emotional responses to taste and smell stimuli: Self-reports, physiological measures, and a potential role for individual and genetic factors. J Food Sci 2022; 88:65-90. [PMID: 36169921 DOI: 10.1111/1750-3841.16300] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/17/2022] [Revised: 06/24/2022] [Accepted: 07/26/2022] [Indexed: 11/30/2022]
Abstract
Taste and olfaction elicit conscious feelings by direct connection with the neural circuits of emotions that affects physiological responses in the body (e.g., heart rate and skin conductance). While sensory attributes are strong determinants of food liking, other factors such as emotional reactions to foods may be better predictors of consumer choices even for products that are equally-liked. Thus, important insights can be gained for understanding the full spectrum of emotional reactions to foods that inform the activities of product developers and marketers, eating psychologist and nutritionists, and policy makers. Today, self-reported questionnaires and physiological measures are the most common tools applied to study variations in emotional perception. The present review discusses these methodological approaches, underlining their different strengths and weaknesses. We also discuss a small, emerging literature suggesting that individual differences and genetic variations in taste and smell perception, like the genetic ability to perceive the bitter compound PROP, may also play a role in emotional reactions to aromas and foods.
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Affiliation(s)
- Mariano Mastinu
- Department of Biomedical Sciences, University of Cagliari, Monserrato, Italy.,Center for Sensory Sciences & Innovation & Department of Food Science, Rutgers University, New Brunswick, New Jersey, USA
| | - Melania Melis
- Department of Biomedical Sciences, University of Cagliari, Monserrato, Italy
| | - Neeta Y Yousaf
- Center for Sensory Sciences & Innovation & Department of Food Science, Rutgers University, New Brunswick, New Jersey, USA
| | | | - Beverly J Tepper
- Center for Sensory Sciences & Innovation & Department of Food Science, Rutgers University, New Brunswick, New Jersey, USA
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37
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Villar-Martinez MD, Goadsby PJ. Pathophysiology and Therapy of Associated Features of Migraine. Cells 2022; 11:cells11172767. [PMID: 36078174 PMCID: PMC9455236 DOI: 10.3390/cells11172767] [Citation(s) in RCA: 23] [Impact Index Per Article: 7.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/09/2022] [Revised: 08/30/2022] [Accepted: 08/31/2022] [Indexed: 11/16/2022] Open
Abstract
Migraine is a complex and debilitating disorder that is broadly recognised by its characteristic headache. However, given the wide array of clinical presentations in migraineurs, the headache might not represent the main troublesome symptom and it can even go unnoticed. Understanding migraines exclusively as a pain process is simplistic and certainly hinders management. We describe the mechanisms behind some of the most disabling associated symptoms of migraine, including the relationship between the central and peripheral processes that take part in nausea, osmophobia, phonophobia, vertigo and allodynia. The rationale for the efficacy of the current therapeutic arsenal is also depicted in this article. The associated symptoms to migraine, apart from the painful component, are frequent, under-recognised and can be more deleterious than the headache itself. The clinical anamnesis of a headache patient should enquire about the associated symptoms, and treatment should be considered and individualised. Acknowledging the associated symptoms as a fundamental part of migraine has permitted a deeper and more coherent comprehension of the pathophysiology of migraine.
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Affiliation(s)
- Maria Dolores Villar-Martinez
- Headache Group, Wolfson CARD, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London WC2R 2LS, UK
- NIHR King’s Clinical Research Facility, SLaM Biomedical Research Centre, King’s College Hospital, London SE5 9RS, UK
| | - Peter J. Goadsby
- Headache Group, Wolfson CARD, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London WC2R 2LS, UK
- NIHR King’s Clinical Research Facility, SLaM Biomedical Research Centre, King’s College Hospital, London SE5 9RS, UK
- Department of Neurology, University of California, Los Angeles, CA 90095, USA
- Correspondence:
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38
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Kulason S, Ratnanather JT, Miller MI, Kamath V, Hua J, Yang K, Ma M, Ishizuka K, Sawa A. A comparative neuroimaging perspective of olfaction and higher-order olfactory processing: on health and disease. Semin Cell Dev Biol 2022; 129:22-30. [PMID: 34462249 PMCID: PMC9900497 DOI: 10.1016/j.semcdb.2021.08.009] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/11/2021] [Accepted: 08/18/2021] [Indexed: 02/08/2023]
Abstract
Olfactory dysfunction is often the earliest indicator of disease in a range of neurological and psychiatric disorders. One tempting working hypothesis is that pathological changes in the peripheral olfactory system where the body is exposed to many adverse environmental stressors may have a causal role for the brain alteration. Whether and how the peripheral pathology spreads to more central brain regions may be effectively studied in rodent models, and there is successful precedence in experimental models for Parkinson's disease. It is of interest to study whether a similar mechanism may underlie the pathology of psychiatric illnesses, such as schizophrenia. However, direct comparison between rodent models and humans includes challenges under light of comparative neuroanatomy and experimental methodologies used in these two distinct species. We believe that neuroimaging modality that has been the main methodology of human brain studies may be a useful viewpoint to address and fill the knowledge gap between rodents and humans in this scientific question. Accordingly, in the present review article, we focus on brain imaging studies associated with olfaction in healthy humans and patients with neurological and psychiatric disorders, and if available those in rodents. We organize this review article at three levels: 1) olfactory bulb (OB) and peripheral structures of the olfactory system, 2) primary olfactory cortical and subcortical regions, and 3) associated higher-order cortical regions. This research area is still underdeveloped, and we acknowledge that further validation with independent cohorts may be needed for many studies presented here, in particular those with human subjects. Nevertheless, whether and how peripheral olfactory disturbance impacts brain function is becoming even a hotter topic in the ongoing COVID-19 pandemic, given the risk of long-term changes of mental status associated with olfactory infection of SARS-CoV-2. Together, in this review article, we introduce this underdeveloped but important research area focusing on its implications in neurological and psychiatric disorders, with several pioneered publications.
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Affiliation(s)
- Sue Kulason
- Center for Imaging Science, Johns Hopkins University, Baltimore, MD, USA; Institute for Computational Medicine, Johns Hopkins University, Baltimore, MD, USA; Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
| | - J Tilak Ratnanather
- Center for Imaging Science, Johns Hopkins University, Baltimore, MD, USA; Institute for Computational Medicine, Johns Hopkins University, Baltimore, MD, USA; Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
| | - Michael I Miller
- Center for Imaging Science, Johns Hopkins University, Baltimore, MD, USA; Institute for Computational Medicine, Johns Hopkins University, Baltimore, MD, USA; Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
| | - Vidyulata Kamath
- Department of Psychiatry, Johns Hopkins School of Medicine, Baltimore, MD, USA
| | - Jun Hua
- Department of Radiology and Radiological Science, Johns Hopkins University School of Medicine, Baltimore, MD, USA; F.M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD, USA
| | - Kun Yang
- Department of Psychiatry, Johns Hopkins School of Medicine, Baltimore, MD, USA; Johns Hopkins Schizophrenia Center, Baltimore, MD, USA
| | - Minghong Ma
- Department of Neuroscience, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, USA
| | - Koko Ishizuka
- Department of Psychiatry, Johns Hopkins School of Medicine, Baltimore, MD, USA; Johns Hopkins Schizophrenia Center, Baltimore, MD, USA
| | - Akira Sawa
- Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA; Department of Psychiatry, Johns Hopkins School of Medicine, Baltimore, MD, USA; Johns Hopkins Schizophrenia Center, Baltimore, MD, USA; Department of Neuroscience, Johns Hopkins School of Medicine, Baltimore, MD, USA; Department of Mental Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.
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39
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Chouinard‐Leclaire C, Manescu S, Collignon O, Lepore F, Frasnelli J. Altered morphological traits along central olfactory centers in congenitally blind subjects. Eur J Neurosci 2022; 56:4486-4500. [DOI: 10.1111/ejn.15758] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/20/2022] [Revised: 06/28/2022] [Accepted: 06/30/2022] [Indexed: 11/27/2022]
Affiliation(s)
| | - Simona Manescu
- Centre de Recherche en Neuropsychologie et Cognition (CERNEC) Université de Montréal Montréal Québec Canada
| | - Olivier Collignon
- Institutes for research in Psychology (IPSY) and Neurosciences (IoNS) University of Louvain Belgium
| | - Franco Lepore
- Centre de Recherche en Neuropsychologie et Cognition (CERNEC) Université de Montréal Montréal Québec Canada
| | - Johannes Frasnelli
- Centre de Recherche en Neuropsychologie et Cognition (CERNEC) Université de Montréal Montréal Québec Canada
- Department of Anatomy Université du Québec à Trois‐Rivières Canada
- Centre d’études avancées en médecine du sommeil (CÉAMS), Centre de Recherche de l’Hôpital du Sacré‐Cœur de Montréal, Centre intégré universitaire de santé et de services sociaux du Nord‐de‐l’Île‐de‐Montréal (CIUSSS du Nord‐de‐l’Île‐de‐Montréal) Canada
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40
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Abstract
This paper develops the claim that epistemic feelings are affective experiences. To establish some diagnostic criteria, characteristic features of affective experiences are outlined: valence and arousal. Then, in order to pave the way for showing that epistemic feelings have said features, an initial challenge coming from introspection is addressed. Next, the paper turns to empirical findings showing that we can observe physiological and behavioural proxies for valence and arousal in epistemic tasks that typically rely on epistemic feelings. Finally, it is argued that the affective properties do not only correlate with epistemic feelings but that we, in fact, capitalise on these affective properties to perform the epistemic tasks. In other words: the affective properties in question constitute epistemic feelings.
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Affiliation(s)
- Slawa Loev
- Faculty of Philosophy, Philosophy of Science and the Study of Religion, Ludwig Maximilian University of Munich, Germany
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41
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Ginieis R, Abeywickrema S, Oey I, Peng M. Testing Links of Food-Related Olfactory Perception to Peripheral Ghrelin and Leptin Concentrations. Front Nutr 2022; 9:888608. [PMID: 35634372 PMCID: PMC9130723 DOI: 10.3389/fnut.2022.888608] [Citation(s) in RCA: 10] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/03/2022] [Accepted: 04/19/2022] [Indexed: 01/04/2023] Open
Abstract
The peptide hormones ghrelin and leptin play major roles in the regulation of appetite and food intake. However, the precise effects of these hormones on sensory processing remain a subject of debate, particularly with food related stimuli and its small body of evidence. Here, we test for relationships between ghrelin and leptin levels against olfactory performance with multiple food-related odours. Specifically, a total of 94 Caucasian males were tested for their supra-threshold sensitivity (i.e., d′), intensity, and valence perception to three odour compounds (i.e., vanilla, potato, and dairy odours). These sensory data were then analysed against peripheral ghrelin and leptin levels, both assessed in plasma samples. Participants’ body adiposity measures were also obtained. Results lent strong support to one of our original hypotheses, with ghrelin levels being positively correlated to the supra-threshold sensitivity of the dairy odour, (r = 0.241, p = 0.020), and intensity ratings to most of the food odours tested [dairy (r = 0.216, p = 0.037) and vanilla (r = 0.241, p = 0.020)]. By contrast, peripheral leptin levels were not significantly linked to any of the olfactory measures (p > 0.05). These relationships remained similar after controlling for variabilities of adiposity measures. The present study brings novel insights by identifying positive links between supra-threshold olfactory perception and ghrelin. This new knowledge is highly relevant for future research linking olfactory shifts to hormonal dysregulation and obesity.
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Affiliation(s)
- Rachel Ginieis
- Sensory Neuroscience Laboratory, Department of Food Science, University of Otago, Dunedin, New Zealand
| | - Sashie Abeywickrema
- Sensory Neuroscience Laboratory, Department of Food Science, University of Otago, Dunedin, New Zealand
| | - Indrawati Oey
- Sensory Neuroscience Laboratory, Department of Food Science, University of Otago, Dunedin, New Zealand
- Riddet Institute, Palmerston North, New Zealand
| | - Mei Peng
- Sensory Neuroscience Laboratory, Department of Food Science, University of Otago, Dunedin, New Zealand
- Riddet Institute, Palmerston North, New Zealand
- *Correspondence: Mei Peng,
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42
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Helfenstein C, Strupf M, Stefke A, Fraunberger B, Renner B, Suchantke I, Rothermel M, Messlinger K, DeCol R, Namer B. Cyclic changes of sensory parameters in migraine patients. Cephalalgia 2022; 42:1148-1159. [PMID: 35514204 DOI: 10.1177/03331024221097932] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/16/2022]
Abstract
BACKGROUND Migraine shows a cyclic pattern with an inter-ictal-, a pre-ictal, an ictal- and a post-ictal phase. We aimed to examine changes in psychophysical parameters during the migraine cycle. METHODS The perception of nociceptive and non-nociceptive stimuli and an electrically induced axon-reflex-erythema were assessed in 20 healthy controls and 14 migraine patients on five consecutive days according to different phases of the migraine cycle. Pain was rated three times during a 10-second electrical stimulus. The size of the axon-reflex-erythema was determined using laser-Doppler-imaging. Intensity and hedonic estimates of odours presented by Sniffin' Sticks were rated. RESULTS In healthy controls, no significant changes over the test days were observed. In migraine patients pain thresholds at the head decreased with an ictal minimum. Less habituation after five seconds of stimulation at the head was found pre-ictally, whereas reduced habituation to 10-second electrical stimulation was present in all phases. The axon-reflex-erythema size showed an inter-ictal-specific minimum at the head. odours were perceived ictally as more unpleasant and intense. CONCLUSIONS Somatosensory functions, pain thresholds and habituation as predominantly central parameters, axon-reflex-erythema as a peripheral function of trigeminal neurons and odour perception as a predominantly extra-thalamic sensation change specifically over the migraine cycle indicating complex variations of neuronal signal processing.
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Affiliation(s)
- Carolin Helfenstein
- Department of Physiology and Experimental Pathophysiology, University of Erlangen/Nürnberg, Germany
| | - Marion Strupf
- Department of Physiology and Experimental Pathophysiology, University of Erlangen/Nürnberg, Germany
| | - Andrea Stefke
- Department of Physiology and Experimental Pathophysiology, University of Erlangen/Nürnberg, Germany
| | - Britta Fraunberger
- Pain Centre, Medical Faculty Erlangen, University of Erlangen/Nürnberg, Germany
| | - Bertold Renner
- Institute of Experimental and Clinical Pharmacology and Toxicology, University of Erlangen/Nürnberg, Germany.,Institute of Clinical Pharmacology, Medical Faculty Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
| | - Insa Suchantke
- Department of Mechanical Learning and Data Analysis, University of Erlangen/Nürnberg, Germany
| | - Markus Rothermel
- Institute for Physiology and Cell Biology, University of Veterinary Medicine Hannover, Foundation, Hanover, Germany
| | - Karl Messlinger
- Department of Physiology and Experimental Pathophysiology, University of Erlangen/Nürnberg, Germany
| | - Roberto DeCol
- Department of Physiology and Experimental Pathophysiology, University of Erlangen/Nürnberg, Germany
| | - Barbara Namer
- Department of Physiology and Experimental Pathophysiology, University of Erlangen/Nürnberg, Germany.,IZKF Research group Neuroscience, University Hospital of RWTH Aachen, Germany.,Institute for Physiology, University hospital of the RWTH Aachen, Aachen, Germany
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43
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Patel ZM, Holbrook EH, Turner JH, Adappa ND, Albers MW, Altundag A, Appenzeller S, Costanzo RM, Croy I, Davis GE, Dehgani-Mobaraki P, Doty RL, Duffy VB, Goldstein BJ, Gudis DA, Haehner A, Higgins TS, Hopkins C, Huart C, Hummel T, Jitaroon K, Kern RC, Khanwalkar AR, Kobayashi M, Kondo K, Lane AP, Lechner M, Leopold DA, Levy JM, Marmura MJ, Mclelland L, Miwa T, Moberg PJ, Mueller CA, Nigwekar SU, O'Brien EK, Paunescu TG, Pellegrino R, Philpott C, Pinto JM, Reiter ER, Roalf DR, Rowan NR, Schlosser RJ, Schwob J, Seiden AM, Smith TL, Soler ZM, Sowerby L, Tan BK, Thamboo A, Wrobel B, Yan CH. International consensus statement on allergy and rhinology: Olfaction. Int Forum Allergy Rhinol 2022; 12:327-680. [PMID: 35373533 DOI: 10.1002/alr.22929] [Citation(s) in RCA: 64] [Impact Index Per Article: 21.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/18/2021] [Revised: 01/01/2021] [Accepted: 11/19/2021] [Indexed: 12/11/2022]
Abstract
BACKGROUND The literature regarding clinical olfaction, olfactory loss, and olfactory dysfunction has expanded rapidly over the past two decades, with an exponential rise in the past year. There is substantial variability in the quality of this literature and a need to consolidate and critically review the evidence. It is with that aim that we have gathered experts from around the world to produce this International Consensus on Allergy and Rhinology: Olfaction (ICAR:O). METHODS Using previously described methodology, specific topics were developed relating to olfaction. Each topic was assigned a literature review, evidence-based review, or evidence-based review with recommendations format as dictated by available evidence and scope within the ICAR:O document. Following iterative reviews of each topic, the ICAR:O document was integrated and reviewed by all authors for final consensus. RESULTS The ICAR:O document reviews nearly 100 separate topics within the realm of olfaction, including diagnosis, epidemiology, disease burden, diagnosis, testing, etiology, treatment, and associated pathologies. CONCLUSION This critical review of the existing clinical olfaction literature provides much needed insight and clarity into the evaluation, diagnosis, and treatment of patients with olfactory dysfunction, while also clearly delineating gaps in our knowledge and evidence base that we should investigate further.
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Affiliation(s)
- Zara M Patel
- Otolaryngology, Stanford University School of Medicine, Stanford, California, USA
| | - Eric H Holbrook
- Otolaryngology, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts, USA
| | - Justin H Turner
- Otolaryngology, Vanderbilt School of Medicine, Nashville, Tennessee, USA
| | - Nithin D Adappa
- Otolaryngology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
| | - Mark W Albers
- Neurology, Harvard Medical School, Boston, Massachusetts, USA
| | - Aytug Altundag
- Otolaryngology, Biruni University School of Medicine, İstanbul, Turkey
| | - Simone Appenzeller
- Rheumatology, School of Medical Sciences, University of Campinas, São Paulo, Brazil
| | - Richard M Costanzo
- Physiology and Biophysics and Otolaryngology, Virginia Commonwealth University School of Medicine, Richmond, Virginia, USA
| | - Ilona Croy
- Psychology and Psychosomatic Medicine, TU Dresden, Dresden, Germany
| | - Greg E Davis
- Otolaryngology, Proliance Surgeons, Seattle and Puyallup, Washington, USA
| | - Puya Dehgani-Mobaraki
- Associazione Naso Sano, Umbria Regional Registry of Volunteer Activities, Corciano, Italy
| | - Richard L Doty
- Smell and Taste Center, Otolaryngology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
| | - Valerie B Duffy
- Allied Health Sciences, University of Connecticut, Storrs, Connecticut, USA
| | | | - David A Gudis
- Otolaryngology, Columbia University Irving Medical Center, New York, USA
| | - Antje Haehner
- Smell and Taste, Otolaryngology, TU Dresden, Dresden, Germany
| | - Thomas S Higgins
- Otolaryngology, University of Louisville School of Medicine, Louisville, Kentucky, USA
| | - Claire Hopkins
- Otolaryngology, Guy's and St. Thomas' Hospitals, London Bridge Hospital, London, UK
| | - Caroline Huart
- Otorhinolaryngology, Cliniques universitaires Saint-Luc, Institute of Neuroscience, Université catholgique de Louvain, Brussels, Belgium
| | - Thomas Hummel
- Smell and Taste, Otolaryngology, TU Dresden, Dresden, Germany
| | | | - Robert C Kern
- Otolaryngology, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA
| | - Ashoke R Khanwalkar
- Otolaryngology, Stanford University School of Medicine, Stanford, California, USA
| | - Masayoshi Kobayashi
- Otorhinolaryngology-Head and Neck Surgery, Mie University Graduate School of Medicine, Mie, Japan
| | - Kenji Kondo
- Otolaryngology, Graduate School of Medicine, University of Tokyo, Tokyo, Japan
| | - Andrew P Lane
- Otolaryngology, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA
| | - Matt Lechner
- Otolaryngology, Barts Health and University College London, London, UK
| | - Donald A Leopold
- Otolaryngology, University of Vermont Medical Center, Burlington, Vermont, USA
| | - Joshua M Levy
- Otolaryngology, Emory University School of Medicine, Atlanta, Georgia, USA
| | - Michael J Marmura
- Neurology Thomas Jefferson University School of Medicine, Philadelphia, Pennsylvania, USA
| | - Lisha Mclelland
- Otolaryngology, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK
| | - Takaki Miwa
- Otolaryngology, Kanazawa Medical University, Ishikawa, Japan
| | - Paul J Moberg
- Psychiatry, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, USA
| | | | - Sagar U Nigwekar
- Division of Nephrology, Massachusetts General Hospital, Boston, Massachusetts, USA
| | - Erin K O'Brien
- Otolaryngology, Mayo Clinic Rochester, Rochester, Minnesota, USA
| | - Teodor G Paunescu
- Division of Nephrology, Massachusetts General Hospital, Boston, Massachusetts, USA
| | | | - Carl Philpott
- Otolaryngology, University of East Anglia, Norwich, UK
| | - Jayant M Pinto
- Otolaryngology, University of Chicago, Chicago, Illinois, USA
| | - Evan R Reiter
- Otolaryngology, Virginia Commonwealth University School of Medicine, Richmond, Virginia, USA
| | - David R Roalf
- Psychiatry, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, USA
| | - Nicholas R Rowan
- Otolaryngology, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA
| | - Rodney J Schlosser
- Otolaryngology, Medical University of South Carolina, Mt Pleasant, South Carolina, USA
| | - James Schwob
- Biomedical Sciences, Tufts University School of Medicine, Boston, Massachusetts, USA
| | - Allen M Seiden
- Otolaryngology, University of Cincinnati School of Medicine, Cincinnati, Ohio, USA
| | - Timothy L Smith
- Otolaryngology, Oregon Health and Sciences University, Portland, Oregon, USA
| | - Zachary M Soler
- Otolaryngology, Medical University of South Carolina, Mt Pleasant, South Carolina, USA
| | - Leigh Sowerby
- Otolaryngology, University of Western Ontario, London, Ontario, Canada
| | - Bruce K Tan
- Otolaryngology, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA
| | - Andrew Thamboo
- Otolaryngology, University of British Columbia, Vancouver, British Columbia, Canada
| | - Bozena Wrobel
- Otolaryngology, Keck School of Medicine, USC, Los Angeles, California, USA
| | - Carol H Yan
- Otolaryngology, School of Medicine, UCSD, La Jolla, California, USA
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44
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Lee KM, Lee S, Satpute AB. Sinful pleasures and pious woes? Using fMRI to examine evaluative and hedonic emotion knowledge. Soc Cogn Affect Neurosci 2022; 17:986-994. [PMID: 35348768 PMCID: PMC9629474 DOI: 10.1093/scan/nsac024] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/24/2021] [Revised: 02/24/2022] [Accepted: 03/22/2022] [Indexed: 01/12/2023] Open
Abstract
Traditionally, lust and pride have been considered pleasurable, yet sinful in the West. Conversely, guilt is often considered aversive, yet valuable. These emotions illustrate how evaluations about specific emotions and beliefs about their hedonic properties may often diverge. Evaluations about specific emotions may shape important aspects of emotional life (e.g. in emotion regulation, emotion experience and acquisition of emotion concepts). Yet these evaluations are often understudied in affective neuroscience. Prior work in emotion regulation, affective experience, evaluation/attitudes and decision-making point to anterior prefrontal areas as candidates for supporting evaluative emotion knowledge. Thus, we examined the brain areas associated with evaluative and hedonic emotion knowledge, with a focus on the anterior prefrontal cortex. Participants (N = 25) made evaluative and hedonic ratings about emotion knowledge during functional magnetic resonance imaging (fMRI). We found that greater activity in the medial prefrontal cortex (mPFC), ventromedial PFC (vmPFC) and precuneus was associated with an evaluative (vs hedonic) focus on emotion knowledge. Our results suggest that the mPFC and vmPFC, in particular, may play a role in evaluating discrete emotions.
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Affiliation(s)
- Kent M Lee
- Correspondence should be addressed to Kent M. Lee, Department of Psychology, Northeastern University, 125 Nightingale Hall, Boston, MA, USA. E-mail:
| | - SuhJin Lee
- Department of Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA
| | - Ajay B Satpute
- Department of Psychology, Northeastern University, Boston, MA 02115, USA
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Domínguez-Borràs J, Vuilleumier P. Amygdala function in emotion, cognition, and behavior. HANDBOOK OF CLINICAL NEUROLOGY 2022; 187:359-380. [PMID: 35964983 DOI: 10.1016/b978-0-12-823493-8.00015-8] [Citation(s) in RCA: 19] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/15/2023]
Abstract
The amygdala is a core structure in the anterior medial temporal lobe, with an important role in several brain functions involving memory, emotion, perception, social cognition, and even awareness. As a key brain structure for saliency detection, it triggers and controls widespread modulatory signals onto multiple areas of the brain, with a great impact on numerous aspects of adaptive behavior. Here we discuss the neural mechanisms underlying these functions, as established by animal and human research, including insights provided in both healthy and pathological conditions.
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Affiliation(s)
- Judith Domínguez-Borràs
- Department of Clinical Psychology and Psychobiology & Institute of Neurosciences, University of Barcelona, Barcelona, Spain
| | - Patrik Vuilleumier
- Department of Neuroscience and Center for Affective Sciences, University of Geneva, Geneva, Switzerland.
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Noto T, Zhou G, Yang Q, Lane G, Zelano C. Human Primary Olfactory Amygdala Subregions Form Distinct Functional Networks, Suggesting Distinct Olfactory Functions. Front Syst Neurosci 2021; 15:752320. [PMID: 34955769 PMCID: PMC8695617 DOI: 10.3389/fnsys.2021.752320] [Citation(s) in RCA: 16] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/02/2021] [Accepted: 11/08/2021] [Indexed: 12/02/2022] Open
Abstract
Three subregions of the amygdala receive monosynaptic projections from the olfactory bulb, making them part of the primary olfactory cortex. These primary olfactory areas are located at the anterior-medial aspect of the amygdala and include the medial amygdala (MeA), cortical amygdala (CoA), and the periamygdaloid complex (PAC). The vast majority of research on the amygdala has focused on the larger basolateral and basomedial subregions, which are known to be involved in implicit learning, threat responses, and emotion. Fewer studies have focused on the MeA, CoA, and PAC, with most conducted in rodents. Therefore, our understanding of the functions of these amygdala subregions is limited, particularly in humans. Here, we first conducted a review of existing literature on the MeA, CoA, and PAC. We then used resting-state fMRI and unbiased k-means clustering techniques to show that the anatomical boundaries of human MeA, CoA, and PAC accurately parcellate based on their whole-brain resting connectivity patterns alone, suggesting that their functional networks are distinct, relative both to each other and to the amygdala subregions that do not receive input from the olfactory bulb. Finally, considering that distinct functional networks are suggestive of distinct functions, we examined the whole-brain resting network of each subregion and speculated on potential roles that each region may play in olfactory processing. Based on these analyses, we speculate that the MeA could potentially be involved in the generation of rapid motor responses to olfactory stimuli (including fight/flight), particularly in approach/avoid contexts. The CoA could potentially be involved in olfactory-related reward processing, including learning and memory of approach/avoid responses. The PAC could potentially be involved in the multisensory integration of olfactory information with other sensory systems. These speculations can be used to form the basis of future studies aimed at clarifying the olfactory functions of these under-studied primary olfactory areas.
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Affiliation(s)
- Torben Noto
- Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, United States
| | - Guangyu Zhou
- Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, United States
| | - Qiaohan Yang
- Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, United States
| | - Gregory Lane
- Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, United States
| | - Christina Zelano
- Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, United States
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Kandemir S, Pamuk AE, Habipoğlu Y, Özel G, Bayar Muluk N, Kılıç R. Olfactory acuity based on Brief Smell Identification Test (BSIT Ⓡ) in migraine patients with and without aura: A cross-sectional, controlled study. Auris Nasus Larynx 2021; 49:613-617. [PMID: 34930631 DOI: 10.1016/j.anl.2021.11.014] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/11/2021] [Revised: 11/25/2021] [Accepted: 11/29/2021] [Indexed: 01/07/2023]
Abstract
OBJECTIVE The aim of this study was to evaluate olfactory acuity in migraine patients with and without aura (MwA and MwoA) MATERIAL AND METHODS: The study included 30 MwA patients, 30 MwoA patients, and 30 age- and gender-matched controls. Demographic features and odor-related symptoms (osmophobia, odor offensiveness, and odor-triggered attack status) were noted. Olfactory acuity was measured using the Brief Smell Identification Test (BSIT®), a 12-item derivative of the University of Pennsylvania Smell Identification Test (UPSIT®). BSIT® scores were compared between the migraine patients and controls. RESULTS The mean BSIT® score did not differ significantly between the MwA patients (8.7 ± 0.9) and MwoA (9.17 ± 0.9) patients (P = 0.094); however, the mean score in the control group was higher (10.4 ± 0.6) than in the MwA and MwoA patients (P < 0.001). The mean BSIT® score did not differ significantly between patients with and without odor-triggered migraine attacks (9 ± 0.9 and 8.8 ± 0.8, respectively) (P = 0.4). Osmophobia and odor-triggered attacks were more common in the MwA patients than in the MwoA patients (odor-triggered attacks: 66% vs. 40% [P = 0.04]; osmophobia: 76.6% vs. 60% [P = 0.16]) CONCLUSION: Olfactory acuity is lower during attack-free periods in migraine patients, as compared to controls. Migraine aura status does not affect olfactory acuity. Odor-triggered attacks, osmophobia, and offensive odors between attacks were more common in the MwA patients than in the MwoA patients.
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Affiliation(s)
- Süheyla Kandemir
- Kırıkkale Yüksek İhtisas Hospital, Department of Otorhinolaryngology, Kırıkkale 71400, Turkey
| | - A Erim Pamuk
- Kırıkkale Yüksek İhtisas Hospital, Department of Otorhinolaryngology, Kırıkkale 71400, Turkey.
| | - Yasin Habipoğlu
- Kırıkkale Yüksek İhtisas Hospital, Department of Neurology, Kırıkkale, Turkey
| | - Gökçe Özel
- Kırşehir Ahi Evran University , Faculty of Medicine, Department of Otorhinolaryngology, Kırşehir, Turkey
| | - Nuray Bayar Muluk
- Kırıkkale University, Faculty of Medicine, Department of Otorhinolaryngology, Kırıkkale, Turkey
| | - Rahmi Kılıç
- Ankara Training and Research Hospital, Department of Otorhinolaryngology, Ankara, Turkey
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Puleo S, Braghieri A, Pacelli C, Bendini A, Toschi TG, Torri L, Piochi M, Di Monaco R. Food Neophobia, Odor and Taste Sensitivity, and Overall Flavor Perception in Food. Foods 2021; 10:foods10123122. [PMID: 34945673 PMCID: PMC8702209 DOI: 10.3390/foods10123122] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/29/2021] [Revised: 12/07/2021] [Accepted: 12/14/2021] [Indexed: 01/25/2023] Open
Abstract
Smell, which allows us to gather information about the hedonic value of an odor, is affected by many factors. This study aimed to assess the relationship among individual factors, odor sensitivity, and enjoyment, and to evaluate how overall flavor perception and liking in actual food samples are affected by odor sensitivity. A total of 749 subjects, from four different Italian regions, participated in the study. The olfactory capabilities test on four odors (anise, banana, mint, and pine), as well as PROP (6-n-prpyl-2-thiouracil) status and food neophobia were assessed. The subjects were clustered into three groups of odor sensitivity, based on the perceived intensity of anise. The liking and intensity of the overall flavor were evaluated for four chocolate puddings with increasing sweetness (C1, C2, C3, and C4). The individual variables significantly affected the perceived intensity and liking of the odors. Even if all of the odor sensitivity groups perceived the more intensely flavored samples as the C1 and C4 chocolate puddings, the high-sensitivity group scored the global flavor of all of the samples as more intense than the low-sensitivity group. The low-sensitive subjects evaluated the liking of the sweeter samples with higher scores than the moderate-sensitive subjects, whereas the high-sensitive subjects gave intermediate scores. In conclusion, odor sensitivity plays a pivotal role in the perception and liking of real food products; this has to be taken into account in the formulation of new products, suitable for particular categories with reduced olfactory abilities.
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Affiliation(s)
- Sharon Puleo
- Department of Agricultural Sciences, Food Science and Technology Division, University of Naples Federico II, 80055 Portici, Italy; (S.P.); (R.D.M.)
| | - Ada Braghieri
- School of Agricultural, Forestry, Food and Environmental Sciences, University of Basilicata, 85100 Potenza, Italy;
- Correspondence: ; Tel.: +39-0971-205101
| | - Corrado Pacelli
- School of Agricultural, Forestry, Food and Environmental Sciences, University of Basilicata, 85100 Potenza, Italy;
| | - Alessandra Bendini
- Department of Agricultural and Food Sciences (DiSTAL), University of Bologna, Piazza Goidanich 60, 47521 Cesena, Italy; (A.B.); (T.G.T.)
| | - Tullia Gallina Toschi
- Department of Agricultural and Food Sciences (DiSTAL), University of Bologna, Piazza Goidanich 60, 47521 Cesena, Italy; (A.B.); (T.G.T.)
| | - Luisa Torri
- Sensory and Consumer Science, University of Gastronomic Sciences, 12042 Pollenzo, Italy; (L.T.); (M.P.)
| | - Maria Piochi
- Sensory and Consumer Science, University of Gastronomic Sciences, 12042 Pollenzo, Italy; (L.T.); (M.P.)
| | - Rossella Di Monaco
- Department of Agricultural Sciences, Food Science and Technology Division, University of Naples Federico II, 80055 Portici, Italy; (S.P.); (R.D.M.)
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49
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Leitão J, Burckhardt M, Vuilleumier P. Amygdala in Action: Functional Connectivity during Approach and Avoidance Behaviors. J Cogn Neurosci 2021; 34:729-747. [PMID: 34860249 DOI: 10.1162/jocn_a_01800] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/04/2022]
Abstract
Motivation is an important feature of emotion. By driving approach to positive events and promoting avoidance of negative stimuli, motivation drives adaptive actions and goal pursuit. The amygdala has been associated with a variety of affective processes, particularly the appraisal of stimulus valence that is assumed to play a crucial role in the generation of approach and avoidance behaviors. Here, we measured amygdala functional connectivity patterns while participants played a video game manipulating goal conduciveness through the presence of good, neutral, or bad monsters. As expected, good versus bad monsters elicited opposing motivated behaviors, whereby good monsters induced more approach and bad monsters triggered more avoidance. These opposing directional behaviors were paralleled by increased connectivity between the amygdala and medial brain areas, such as the OFC and posterior cingulate, for good relative to bad, and between amygdala and caudate for bad relative to good monsters. Moreover, in both conditions, individual connectivity strength between the amygdala and medial prefrontal regions was positively correlated with brain scores from a latent component representing efficient goal pursuit, which was identified by a partial least square analysis determining the multivariate association between amygdala connectivity and behavioral motivation indices during gameplay. At the brain level, this latent component highlighted a widespread pattern of amygdala connectivity, including a dorsal frontoparietal network and motor areas. These results suggest that amygdala-medial prefrontal interactions captured the overall subjective relevance of ongoing events, which could consecutively drive the engagement of attentional, executive, and motor circuits necessary for implementing successful goal-pursuit, irrespective of approach or avoidance directions.
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50
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How JJ, Navlakha S, Chalasani SH. Neural network features distinguish chemosensory stimuli in Caenorhabditis elegans. PLoS Comput Biol 2021; 17:e1009591. [PMID: 34752447 PMCID: PMC8604368 DOI: 10.1371/journal.pcbi.1009591] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/03/2020] [Revised: 11/19/2021] [Accepted: 10/26/2021] [Indexed: 11/19/2022] Open
Abstract
Nervous systems extract and process information from the environment to alter animal behavior and physiology. Despite progress in understanding how different stimuli are represented by changes in neuronal activity, less is known about how they affect broader neural network properties. We developed a framework for using graph-theoretic features of neural network activity to predict ecologically relevant stimulus properties, in particular stimulus identity. We used the transparent nematode, Caenorhabditis elegans, with its small nervous system to define neural network features associated with various chemosensory stimuli. We first immobilized animals using a microfluidic device and exposed their noses to chemical stimuli while monitoring changes in neural activity of more than 50 neurons in the head region. We found that graph-theoretic features, which capture patterns of interactions between neurons, are modulated by stimulus identity. Further, we show that a simple machine learning classifier trained using graph-theoretic features alone, or in combination with neural activity features, can accurately predict salt stimulus. Moreover, by focusing on putative causal interactions between neurons, the graph-theoretic features were almost twice as predictive as the neural activity features. These results reveal that stimulus identity modulates the broad, network-level organization of the nervous system, and that graph theory can be used to characterize these changes. Animals use their nervous systems to detect and respond to changes in their external environment. A central challenge in computational neuroscience is to determine how specific properties of these stimuli affect interactions between neurons. While most studies have focused on the neurons in the sensory periphery, recent advances allow us to probe how the rest of the nervous system responds to sensory stimulation. We recorded activity of neurons within the C. elegans head region while the animal was exposed to various chemosensory stimuli. We then used computational methods to identify various stimuli by analyzing neural activity. Specifically, we used a combination of population-level activity statistics (e.g., average, standard deviation, frequency-based measures) and graph-theoretic features of functional network structure (e.g., transitivity, which is the existence of strongly connected triplets of neurons) to accurately predict salt stimulus. Our method is general and can be used across species, particularly in instances where the identities of individual neurons are unknown. These results also suggest that neural activity downstream of the sensory periphery contains a signature of changes in the environment.
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Affiliation(s)
- Javier J. How
- Neurosciences Graduate Program, University of California, San Diego, La Jolla, California, United States of America
| | - Saket Navlakha
- Neurosciences Graduate Program, University of California, San Diego, La Jolla, California, United States of America
- Simons Center for Quantitative Biology, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, United States of America
- * E-mail: (SN); (SHC)
| | - Sreekanth H. Chalasani
- Neurosciences Graduate Program, University of California, San Diego, La Jolla, California, United States of America
- Molecular Neurobiology Laboratory, The Salk Institute for Biological Studies, San Diego, La Jolla, California, United States of America
- * E-mail: (SN); (SHC)
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