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Madadi Asl M, Valizadeh A. Entrainment by transcranial alternating current stimulation: Insights from models of cortical oscillations and dynamical systems theory. Phys Life Rev 2025; 53:147-176. [PMID: 40106964 DOI: 10.1016/j.plrev.2025.03.008] [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: 03/12/2025] [Accepted: 03/12/2025] [Indexed: 03/22/2025]
Abstract
Signature of neuronal oscillations can be found in nearly every brain function. However, abnormal oscillatory activity is linked with several brain disorders. Transcranial alternating current stimulation (tACS) is a non-invasive brain stimulation technique that can potentially modulate neuronal oscillations and influence behavior both in health and disease. Yet, a complete understanding of how interacting networks of neurons are affected by tACS remains elusive. Entrainment effects by which tACS synchronizes neuronal oscillations is one of the main hypothesized mechanisms, as evidenced in animals and humans. Computational models of cortical oscillations may shed light on the entrainment effects of tACS, but current modeling studies lack specific guidelines to inform experimental investigations. This study addresses the existing gap in understanding the mechanisms of tACS effects on rhythmogenesis within the brain by providing a comprehensive overview of both theoretical and experimental perspectives. We explore the intricate interactions between oscillators and periodic stimulation through the lens of dynamical systems theory. Subsequently, we present a synthesis of experimental findings that demonstrate the effects of tACS on both individual neurons and collective oscillatory patterns in animal models and humans. Our review extends to computational investigations that elucidate the interplay between tACS and neuronal dynamics across diverse cortical network models. To illustrate these concepts, we conclude with a simple oscillatory neuron model, showcasing how fundamental theories of oscillatory behavior derived from dynamical systems, such as phase response of neurons to external perturbation, can account for the entrainment effects observed with tACS. Studies reviewed here render the necessity of integrated experimental and computational approaches for effective neuromodulation by tACS in health and disease.
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Affiliation(s)
- Mojtaba Madadi Asl
- School of Biological Sciences, Institute for Research in Fundamental Sciences (IPM), Tehran, Iran; Pasargad Institute for Advanced Innovative Solutions (PIAIS), Tehran, Iran.
| | - Alireza Valizadeh
- Pasargad Institute for Advanced Innovative Solutions (PIAIS), Tehran, Iran; Department of Physics, Institute for Advanced Studies in Basic Sciences (IASBS), Zanjan, Iran; The Zapata-Briceño Institute of Neuroscience, Madrid, Spain
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2
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Wang BY, Wang B, Cao B, Gu LL, Chen J, He H, Zhao Z, Chen F, Wang Z. Associative Learning-Induced Synaptic Potentiation at the Two Major Hippocampal CA1 Inputs for Cued Memory Acquisition. Neurosci Bull 2025; 41:649-664. [PMID: 39604622 PMCID: PMC11979062 DOI: 10.1007/s12264-024-01327-7] [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: 05/31/2024] [Accepted: 09/03/2024] [Indexed: 11/29/2024] Open
Abstract
Learning-associated functional plasticity at hippocampal synapses remains largely unexplored. Here, in a single session of reward-based trace conditioning, we examine learning-induced synaptic plasticity in the dorsal CA1 hippocampus (dCA1). Local field-potential recording combined with selective optogenetic inhibition first revealed an increase of dCA1 synaptic responses to the conditioned stimulus (CS) induced during conditioning at both Schaffer collaterals to the stratum radiatum (Rad) and temporoammonic input to the lacunosum moleculare (LMol). At these dCA1 inputs, synaptic potentiation of CS-responding excitatory synapses was further demonstrated by locally blocking NMDA receptors during conditioning and whole-cell recording sensory-evoked synaptic responses in dCA1 neurons from naive animals. An overall similar time course of the induction of synaptic potentiation was found in the Rad and LMol by multiple-site recording; this emerged later and saturated earlier than conditioned behavioral responses. Our experiments demonstrate a cued memory-associated dCA1 synaptic plasticity induced at both Schaffer collaterals and temporoammonic pathways.
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Affiliation(s)
- Bing-Ying Wang
- Institute and Key Laboratory of Brain Functional Genomics of Chinese Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
| | - Bo Wang
- Institute and Key Laboratory of Brain Functional Genomics of Chinese Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
| | - Bo Cao
- Institute and Key Laboratory of Brain Functional Genomics of Chinese Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
| | - Ling-Ling Gu
- Institute and Key Laboratory of Brain Functional Genomics of Chinese Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
| | - Jiayu Chen
- Institute and Key Laboratory of Brain Functional Genomics of Chinese Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
| | - Hua He
- Department of Neurosurgery, Third Affiliated Hospital of Navy Military Medical University, Shanghai, 200438, China
| | - Zheng Zhao
- Institute and Key Laboratory of Brain Functional Genomics of Chinese Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China.
| | - Fujun Chen
- Bio-X Institutes, Key Laboratory for the Genetics of Developmental and Neuropsychiatric Disorders, Ministry of Education, Shanghai Jiao Tong University, Shanghai, 200030, China.
| | - Zhiru Wang
- Institute and Key Laboratory of Brain Functional Genomics of Chinese Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China.
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Negelspach D, Kennedy KER, Huskey A, Cha J, Alkozei A, Killgore WDS. Mapping the Neural Basis of Wake Onset Regularity and Its Effects on Sleep Quality and Positive Affect. Clocks Sleep 2025; 7:15. [PMID: 40136852 PMCID: PMC11941042 DOI: 10.3390/clockssleep7010015] [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: 10/24/2024] [Revised: 02/14/2025] [Accepted: 03/08/2025] [Indexed: 03/27/2025] Open
Abstract
The regularity of sleep-wake cycles is a defining characteristic of normative sleep patterns that are typically associated with proper circadian rhythmicity. The previous literature indicates that consistent patterns of sleep and wake are associated with improved sleep quality and cognitive functioning. Conversely, sleep irregularity has been associated with reduced well-being and inefficiency in resting-state neural networks. This study investigated the relationship between specific sleep regularity measures and outcomes, including emotional affect, sleep quality, and resting-state functional connectivity. We found that variability in wake onset predicted poorer sleep quality and reduced positive affect. Furthermore, sleep regularity measures were associated with altered functional connectivity between the posterior cingulate cortex and regions involved in emotional processing. We propose that alterations in default mode network (DMN) connectivity linked to sleep irregularity reflect disruptions in emotional processing and sleep quality.
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Berres S, Erdfelder E, Kuhlmann BG. Does sleep benefit source memory? Investigating 12-h retention intervals with a multinomial modeling approach. Mem Cognit 2025; 53:467-493. [PMID: 38831160 PMCID: PMC11868154 DOI: 10.3758/s13421-024-01579-8] [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] [Accepted: 04/22/2024] [Indexed: 06/05/2024]
Abstract
For retention intervals of up to 12 h, the active systems consolidation hypothesis predicts that sleep compared to wakefulness strengthens the context binding of memories previously established during encoding. Sleep should thus improve source memory. By comparing retention intervals filled with natural night sleep versus daytime wakefulness, we tested this prediction in two online source-monitoring experiments using intentionally learned pictures as items and incidentally learned screen positions and frame colors as source dimensions. In Experiment 1, we examined source memory by varying the spatial position of pictures on the computer screen. Multinomial modeling analyses revealed a significant sleep benefit in source memory. In Experiment 2, we manipulated both the spatial position and the frame color of pictures orthogonally to investigate source memory for two different source dimensions at the same time, also allowing exploration of bound memory for both source dimensions. The sleep benefit on spatial source memory replicated. In contrast, no source memory sleep benefit was observed for either frame color or bound memory of both source dimensions, probably as a consequence of a floor effect in incidental encoding of color associations. In sum, the results of both experiments show that sleep within a 12-h retention interval improves source memory for spatial positions, supporting the prediction of the active systems consolidation hypothesis. However, additional research is required to clarify the impact of sleep on source memory for other context features and bound memories of multiple source dimensions.
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Affiliation(s)
- Sabrina Berres
- Department of Psychology, School of Social Sciences, University of Mannheim, L13, 15-17, Room 425, 68161, Mannheim, Germany.
| | - Edgar Erdfelder
- Department of Psychology, School of Social Sciences, University of Mannheim, L13, 15-17, Room 425, 68161, Mannheim, Germany.
| | - Beatrice G Kuhlmann
- Department of Psychology, School of Social Sciences, University of Mannheim, L13, 15-17, Room 425, 68161, Mannheim, Germany.
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Liu B, Shi P, Jin T, Feng X. Associations between meeting 24h movement behavior guidelines and cognition, gray matter volume, and academic performance in children and adolescents: a systematic review. Arch Public Health 2025; 83:10. [PMID: 39794834 PMCID: PMC11720839 DOI: 10.1186/s13690-024-01493-0] [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: 04/12/2024] [Accepted: 12/26/2024] [Indexed: 01/13/2025] Open
Abstract
BACKGROUND 24-h movement behaviors have a close relationship with children and adolescents' cognition, gray matter volume, and academic performance. This systematic review aims to precisely explore the associations between meeting different combinations of guidelines and the aforementioned indicators, in order to better serve public health policy. METHODS Computer retrieval was conducted on CNKI, Web of Science, PubMed, SPORT Discus and Cochrane library databases. The screening and data extraction processes were conducted by two researchers. This study used the Joanna Briggs Institute checklist for methodological quality assessment and the Grading of Recommendations Assessment, Development, and Evaluation system for the evaluation of the level of evidence. Descriptive statistical analysis is performed using frequency and percentage on the extracted data and key findings, primarily to assess the consistency of the positive benefits associated with meeting different guidelines and outcome variables. RESULTS A total of 10 studies were included (with 16 correlation analyses conducted), involving 51,566 children and adolescents aged between 4.2 and 15.9 years old. The included studies generally agreed upon the following associations: adherence to the screen time (ST) guidelines is positively linked to fluid intelligence; adherence to the sleep duration (SD) guidelines is positively linked to literacy; adherence to both ST and SD guidelines is associated with increased fluid intelligence and gray matter volume; and overall adherence to all guidelines is positively correlated with fluid intelligence. The included studies reported low certainty of evidence. Additionally, the included studies have provided clear evidence, but some studies did not strictly control confounding factors, and it is also unclear whether there is a larger effect size, hence the level of evidence is relatively low. CONCLUSION There are varying degrees of associations between different combinations of guidelines and cognition, gray matter volume, and academic performance, but further research is needed to confirm these findings, especially the relatively limited role of meeting physical activity guidelines.
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Affiliation(s)
- Bo Liu
- School of Athletic Performance, Shanghai University of Sport, Shanghai, 200438, China
| | - Peng Shi
- School of Physical Education, Shanghai University of Sport, Shanghai, 200438, China.
| | - Teng Jin
- School of Physical Education, Shandong University of Technology, Zibo, 255000, China
| | - Xiaosu Feng
- School of Physical Education, Liaoning Normal University, Dalian, 116029, China
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Zhang CL, Sontag L, Gómez-Ocádiz R, Schmidt-Hieber C. Learning-dependent gating of hippocampal inputs by frontal interneurons. Proc Natl Acad Sci U S A 2024; 121:e2403325121. [PMID: 39467130 PMCID: PMC11551329 DOI: 10.1073/pnas.2403325121] [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: 02/16/2024] [Accepted: 09/03/2024] [Indexed: 10/30/2024] Open
Abstract
The hippocampus is a brain region that is essential for the initial encoding of episodic memories. However, the consolidation of these memories is thought to occur in the neocortex, under guidance of the hippocampus, over the course of days and weeks. Communication between the hippocampus and the neocortex during hippocampal sharp wave-ripple oscillations is believed to be critical for this memory consolidation process. Yet, the synaptic and circuit basis of this communication between brain areas is largely unclear. To address this problem, we perform in vivo whole-cell patch-clamp recordings in the frontal neocortex and local field potential recordings in CA1 of head-fixed mice exposed to a virtual-reality environment. In mice trained in a goal-directed spatial task, we observe a depolarization in frontal principal neurons during hippocampal ripple oscillations. Both this ripple-associated depolarization and goal-directed task performance can be disrupted by chemogenetic inactivation of somatostatin-positive (SOM+) interneurons. In untrained mice, a ripple-associated depolarization is not observed, but it emerges when frontal parvalbumin-positive (PV+) interneurons are inactivated. These results support a model where SOM+ interneurons inhibit PV+ interneurons during hippocampal activity, thereby acting as a disinhibitory gate for hippocampal inputs to neocortical principal neurons during learning.
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Affiliation(s)
- Chun-Lei Zhang
- Institut Pasteur, Université Paris Cité, Neural Circuits for Space and Memory, Department of Neuroscience, ParisF-75015, France
| | - Lucile Sontag
- Institut Pasteur, Université Paris Cité, Neural Circuits for Space and Memory, Department of Neuroscience, ParisF-75015, France
| | - Ruy Gómez-Ocádiz
- Institut Pasteur, Université Paris Cité, Neural Circuits for Space and Memory, Department of Neuroscience, ParisF-75015, France
| | - Christoph Schmidt-Hieber
- Institut Pasteur, Université Paris Cité, Neural Circuits for Space and Memory, Department of Neuroscience, ParisF-75015, France
- Institute for Physiology I, Jena University Hospital, Jena07743, Germany
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Hahn MA, Lendner JD, Anwander M, Slama KSJ, Knight RT, Lin JJ, Helfrich RF. A tradeoff between efficiency and robustness in the hippocampal-neocortical memory network during human and rodent sleep. Prog Neurobiol 2024; 242:102672. [PMID: 39369838 DOI: 10.1016/j.pneurobio.2024.102672] [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: 05/13/2024] [Revised: 08/30/2024] [Accepted: 10/03/2024] [Indexed: 10/08/2024]
Abstract
Sleep constitutes a brain state of disengagement from the external world that supports memory consolidation and restores cognitive resources. The precise mechanisms how sleep and its varied stages support information processing remain largely unknown. Synaptic scaling models imply that daytime learning accumulates neural information, which is then consolidated and downregulated during sleep. Currently, there is a lack of in-vivo data from humans and rodents that elucidate if, and how, sleep renormalizes information processing capacities. From an information-theoretical perspective, a consolidation process should entail a reduction in neural pattern variability over the course of a night. Here, in a cross-species intracranial study, we identify a tradeoff in the neural population code during sleep where information coding efficiency is higher in the neocortex than in hippocampal archicortex in humans than in rodents as well as during wakefulness compared to sleep. Critically, non-REM sleep selectively reduces information coding efficiency through pattern repetition in the neocortex in both species, indicating a transition to a more robust information coding regime. Conversely, the coding regime in the hippocampus remained consistent from wakefulness to non-REM sleep. These findings suggest that new information could be imprinted to the long-term mnemonic storage in the neocortex through pattern repetition during sleep. Lastly, our results show that task engagement increased coding efficiency, while medically-induced unconsciousness disrupted the population code. In sum, these findings suggest that neural pattern variability could constitute a fundamental principle underlying cognitive engagement and memory formation, while pattern repetition reflects robust coding, possibly underlying the consolidation process.
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Affiliation(s)
- Michael A Hahn
- Hertie-Institute for Clinical Brain Research, University Medical Center Tübingen, Otfried-Müller Str. 27, Tübingen 72076, Germany.
| | - Janna D Lendner
- Hertie-Institute for Clinical Brain Research, University Medical Center Tübingen, Otfried-Müller Str. 27, Tübingen 72076, Germany; Department of Anesthesiology and Intensive Care Medicine, University Medical Center Tübingen, Hoppe-Seyler-Str 3, Tübingen 72076, Germany
| | - Matthias Anwander
- Hertie-Institute for Clinical Brain Research, University Medical Center Tübingen, Otfried-Müller Str. 27, Tübingen 72076, Germany
| | - Katarina S J Slama
- Department of Psychology and the Helen Wills Neuroscience Institute, UC Berkeley, 130 Barker Hall, Berkeley, CA 94720, USA
| | - Robert T Knight
- Department of Psychology and the Helen Wills Neuroscience Institute, UC Berkeley, 130 Barker Hall, Berkeley, CA 94720, USA
| | - Jack J Lin
- Department of Neurology, UC Davis, 3160 Folsom Blvd, Sacramento, CA 95816, USA; Center for Mind and Brain, UC Davis, 267 Cousteau Pl, Davis, CA 95618, USA
| | - Randolph F Helfrich
- Hertie-Institute for Clinical Brain Research, University Medical Center Tübingen, Otfried-Müller Str. 27, Tübingen 72076, Germany.
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Kucewicz MT, Cimbalnik J, Garcia-Salinas JS, Brazdil M, Worrell GA. High frequency oscillations in human memory and cognition: a neurophysiological substrate of engrams? Brain 2024; 147:2966-2982. [PMID: 38743818 PMCID: PMC11370809 DOI: 10.1093/brain/awae159] [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: 02/07/2024] [Revised: 04/16/2024] [Accepted: 04/21/2024] [Indexed: 05/16/2024] Open
Abstract
Despite advances in understanding the cellular and molecular processes underlying memory and cognition, and recent successful modulation of cognitive performance in brain disorders, the neurophysiological mechanisms remain underexplored. High frequency oscillations beyond the classic electroencephalogram spectrum have emerged as a potential neural correlate of fundamental cognitive processes. High frequency oscillations are detected in the human mesial temporal lobe and neocortical intracranial recordings spanning gamma/epsilon (60-150 Hz), ripple (80-250 Hz) and higher frequency ranges. Separate from other non-oscillatory activities, these brief electrophysiological oscillations of distinct duration, frequency and amplitude are thought to be generated by coordinated spiking of neuronal ensembles within volumes as small as a single cortical column. Although the exact origins, mechanisms and physiological roles in health and disease remain elusive, they have been associated with human memory consolidation and cognitive processing. Recent studies suggest their involvement in encoding and recall of episodic memory with a possible role in the formation and reactivation of memory traces. High frequency oscillations are detected during encoding, throughout maintenance, and right before recall of remembered items, meeting a basic definition for an engram activity. The temporal coordination of high frequency oscillations reactivated across cortical and subcortical neural networks is ideally suited for integrating multimodal memory representations, which can be replayed and consolidated during states of wakefulness and sleep. High frequency oscillations have been shown to reflect coordinated bursts of neuronal assembly firing and offer a promising substrate for tracking and modulation of the hypothetical electrophysiological engram.
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Affiliation(s)
- Michal T Kucewicz
- BioTechMed Center, Brain & Mind Electrophysiology laboratory, Department of Multimedia Systems, Faculty of Electronics, Telecommunications and Informatics, Gdansk University of Technology, Gdansk 80-233, Poland
- Bioelectronics, Neurophysiology and Engineering Laboratory, Mayo Clinic, Departments of Neurology and Biomedical Engineering & Physiology, Mayo Clinic, Rochester, MN 55902, USA
| | - Jan Cimbalnik
- BioTechMed Center, Brain & Mind Electrophysiology laboratory, Department of Multimedia Systems, Faculty of Electronics, Telecommunications and Informatics, Gdansk University of Technology, Gdansk 80-233, Poland
- Department of Biomedical Engineering, St. Anne’s University Hospital in Brno & International Clinical Research Center, Brno 602 00, Czech Republic
- Brno Epilepsy Center, 1th Department of Neurology, St. Anne's University Hospital and Medical Faculty of Masaryk University, member of the ERN-EpiCARE, Brno 602 00, Czech Republic
| | - Jesus S Garcia-Salinas
- BioTechMed Center, Brain & Mind Electrophysiology laboratory, Department of Multimedia Systems, Faculty of Electronics, Telecommunications and Informatics, Gdansk University of Technology, Gdansk 80-233, Poland
| | - Milan Brazdil
- BioTechMed Center, Brain & Mind Electrophysiology laboratory, Department of Multimedia Systems, Faculty of Electronics, Telecommunications and Informatics, Gdansk University of Technology, Gdansk 80-233, Poland
- Brno Epilepsy Center, 1th Department of Neurology, St. Anne's University Hospital and Medical Faculty of Masaryk University, member of the ERN-EpiCARE, Brno 602 00, Czech Republic
- Behavioural and Social Neuroscience Research Group, CEITEC—Central European Institute of Technology, Masaryk University, Brno 625 00, Czech Republic
| | - Gregory A Worrell
- BioTechMed Center, Brain & Mind Electrophysiology laboratory, Department of Multimedia Systems, Faculty of Electronics, Telecommunications and Informatics, Gdansk University of Technology, Gdansk 80-233, Poland
- Bioelectronics, Neurophysiology and Engineering Laboratory, Mayo Clinic, Departments of Neurology and Biomedical Engineering & Physiology, Mayo Clinic, Rochester, MN 55902, USA
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Yook S, Choi SJ, Lee H, Joo EY, Kim H. Long-term night-shift work is associated with accelerates brain aging and worsens N3 sleep in female nurses. Sleep Med 2024; 121:69-76. [PMID: 38936046 PMCID: PMC11330713 DOI: 10.1016/j.sleep.2024.06.013] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/10/2024] [Revised: 06/12/2024] [Accepted: 06/13/2024] [Indexed: 06/29/2024]
Abstract
BACKGROUND Shift work disrupts circadian rhythms and alters sleep patterns, resulting in various health problems. To quantitatively assess the impact of shift work on brain health, we evaluated the brain age index (BAI) derived from sleep electroencephalography (EEG) results in night-shift workers and compared it with that in daytime workers. METHODS We studied 45 female night shift nurses (mean age: 28.2 ± 3.3 years) and 44 female daytime workers (30.5 ± 4.7 years). Sleep EEG data were analyzed to calculate BAI. The BAI of night shift workers who were asleep during the daytime with those of daytime workers who were asleep at night were statistically compared to explore associations between BAI, duration of shift work, and sleep quality. RESULTS Night-shift workers exhibited significantly higher BAI (2.14 ± 6.04 vs. 0 ± 5.35), suggesting accelerated brain aging and altered sleep architecture, including reduced delta and sigma wave frequency activity during non-rapid eye movement sleep than daytime workers. Furthermore, poor deep sleep quality, indicated by a higher percentage of N1, lower percentage of N3, and higher arousal index, was associated with increased BAI among shift workers. Additionally, a longer duration of night-shift work was correlated with increased BAI, particularly in older shift workers. CONCLUSION Night-shift work, especially over extended periods, may be associated with accelerated brain aging, as indicated by higher BAI and alterations in sleep architecture. Interventions are necessary to mitigate the health impacts of shift work. Further research on the long-term effects and potential strategies for sleep improvement and mitigating brain aging in shift workers is warranted.
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Affiliation(s)
- Soonhyun Yook
- USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine of USC, University of Southern California, Los Angeles, CA, 90033, USA
| | - Su Jung Choi
- Graduate School of Clinical Nursing Science, Sungkyunkwan University, Seoul, 03063, South Korea
| | - Hanul Lee
- Department of Neurology, Samsung Medical Center, Seoul, 06351, South Korea
| | - Eun Yeon Joo
- Department of Neurology, Neuroscience Center, Samsung Medical Center, Samsung Biomedical Research Institute, School of Medicine, Sungkyunkwan University, Seoul, 06351, South Korea.
| | - Hosung Kim
- USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine of USC, University of Southern California, Los Angeles, CA, 90033, USA
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10
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Mushtaq M, Marshall L, ul Haq R, Martinetz T. Possible mechanisms to improve sleep spindles via closed loop stimulation during slow wave sleep: A computational study. PLoS One 2024; 19:e0306218. [PMID: 38924001 PMCID: PMC11207127 DOI: 10.1371/journal.pone.0306218] [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: 11/15/2023] [Accepted: 06/12/2024] [Indexed: 06/28/2024] Open
Abstract
Sleep spindles are one of the prominent EEG oscillatory rhythms of non-rapid eye movement sleep. In the memory consolidation, these oscillations have an important role in the processes of long-term potentiation and synaptic plasticity. Moreover, the activity (spindle density and/or sigma power) of spindles has a linear association with learning performance in different paradigms. According to the experimental observations, the sleep spindle activity can be improved by closed loop acoustic stimulations (CLAS) which eventually improve memory performance. To examine the effects of CLAS on spindles, we propose a biophysical thalamocortical model for slow oscillations (SOs) and sleep spindles. In addition, closed loop stimulation protocols are applied on a thalamic network. Our model results show that the power of spindles is increased when stimulation cues are applied at the commencing of an SO Down-to-Up-state transition, but that activity gradually decreases when cues are applied with an increased time delay from this SO phase. Conversely, stimulation is not effective when cues are applied during the transition of an Up-to-Down-state. Furthermore, our model suggests that a strong inhibitory input from the reticular (RE) layer to the thalamocortical (TC) layer in the thalamic network shifts leads to an emergence of spindle activity at the Up-to-Down-state transition (rather than at Down-to-Up-state transition), and the spindle frequency is also reduced (8-11 Hz) by thalamic inhibition.
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Affiliation(s)
| | - Lisa Marshall
- Institute of Experimental and Clinical Pharmacology, University of Lübeck, Lübeck, Germany
- Center of Brain, Behavior and Metabolism, Lübeck, Germany
- University Clinic Hospital Schleswig Holstein, Lübeck, Germany
| | - Rizwan ul Haq
- Department of Pharmacy, Abbottabad University of Science and Technology, Abbottabad, Pakistan
| | - Thomas Martinetz
- Institute for Neuro- and Bioinformatics, Lübeck, Germany
- Center of Brain, Behavior and Metabolism, Lübeck, Germany
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11
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Samona EA, Chowdury A, Kopchick J, Thomas P, Rajan U, Khatib D, Zajac-Benitez C, Amirsadri A, Haddad L, Stanley JA, Diwadkar VA. The importance of covert memory consolidation in schizophrenia: Dysfunctional network profiles of the hippocampus and the dorsolateral prefrontal cortex. Psychiatry Res Neuroimaging 2024; 340:111805. [PMID: 38447230 PMCID: PMC11188056 DOI: 10.1016/j.pscychresns.2024.111805] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/31/2023] [Revised: 01/24/2024] [Accepted: 02/20/2024] [Indexed: 03/08/2024]
Abstract
Altered brain network profiles in schizophrenia (SCZ) during memory consolidation are typically observed during task-active periods such as encoding or retrieval. However active processes are also sub served by covert periods of memory consolidation. These periods are active in that they allow memories to be recapitulated even in the absence of overt sensorimotor processing. It is plausible that regions central to memory formation like the dlPFC and the hippocampus, exert network signatures during covert periods. Are these signatures altered in patients? The question is clinically relevant because real world learning and memory is facilitated by covert processing, and may be impaired in schizophrenia. Here, we compared network signatures of the dlPFC and the hippocampus during covert periods of a learning and memory task. Because behavioral proficiency increased non-linearly, functional connectivity of the dlPFC and hippocampus [psychophysiological interaction (PPI)] was estimated for each of the Early (linear increases in performance) and Late (asymptotic performance) covert periods. During Early periods, we observed hypo-modulation by the hippocampus but hyper-modulation by dlPFC. Conversely, during Late periods, we observed hypo-modulation by both the dlPFC and the hippocampus. We stitch these results into a conceptual model of network deficits during covert periods of memory consolidation.
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Affiliation(s)
- Elias A Samona
- Department of Psychiatry & Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, United States
| | - Asadur Chowdury
- Department of Psychiatry & Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, United States
| | - John Kopchick
- Department of Psychiatry & Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, United States
| | - Patricia Thomas
- Department of Psychiatry & Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, United States
| | - Usha Rajan
- Department of Psychiatry & Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, United States
| | - Dalal Khatib
- Department of Psychiatry & Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, United States
| | - Caroline Zajac-Benitez
- Department of Psychiatry & Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, United States
| | - Alireza Amirsadri
- Department of Psychiatry & Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, United States
| | - Luay Haddad
- Department of Psychiatry & Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, United States
| | - Jeffrey A Stanley
- Department of Psychiatry & Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, United States
| | - Vaibhav A Diwadkar
- Department of Psychiatry & Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, United States.
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12
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Seenivasan P, Basak R, Narayanan R. Cross-strata co-occurrence of ripples with theta-frequency oscillations in the hippocampus of foraging rats. J Physiol 2024; 602:2315-2341. [PMID: 38654581 PMCID: PMC7615956 DOI: 10.1113/jp284629] [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: 03/02/2023] [Accepted: 04/04/2024] [Indexed: 04/26/2024] Open
Abstract
Brain rhythms have been postulated to play central roles in animal cognition. A prominently reported dichotomy of hippocampal rhythms links theta-frequency oscillations (4-12 Hz) and ripples (120-250 Hz) exclusively to preparatory and consummatory behaviours, respectively. However, because of the differential power expression of these two signals across hippocampal strata, such exclusivity requires validation through analyses of simultaneous multi-strata recordings. We assessed co-occurrence of theta-frequency oscillations with ripples in multi-channel recordings of extracellular potentials across hippocampal strata from foraging rats. We detected all ripple events from an identified stratum pyramidale (SP) channel. We then defined theta epochs based on theta oscillations detected from the stratum lacunosum-moleculare (SLM) or the stratum radiatum (SR). We found ∼20% of ripple events (in SP) to co-occur with theta epochs identified from SR/SLM channels, defined here as theta ripples. Strikingly, when theta epochs were instead identified from the SP channel, such co-occurrences were significantly reduced because of a progressive reduction in theta power along the SLM-SR-SP axis. Behaviourally, we found most theta ripples to occur during immobile periods, with comparable theta power during exploratory and immobile theta epochs. Furthermore, the progressive reduction in theta power along the SLM-SR-SP axis was common to exploratory and immobile periods. Finally, we found a strong theta-phase preference of theta ripples within the fourth quadrant [3π/2 - 2π] of the associated theta oscillation. The prevalence of theta ripples expands the potential roles of ripple-frequency oscillations to span the continuum of encoding, retrieval and consolidation, achieved through interactions with theta oscillations. KEY POINTS: The brain manifests oscillations in recorded electrical potentials, with different frequencies of oscillation associated with distinct behavioural states. A prominently reported dichotomy assigns theta-frequency oscillations (4-12 Hz) and ripples (120-250 Hz) recorded in the hippocampus to be exclusively associated with preparatory and consummatory behaviours, respectively. Our multi-strata recordings from the rodent hippocampus coupled with cross-strata analyses provide direct quantitative evidence for the occurrence of ripple events nested within theta oscillations. These results highlight the need for an analysis pipeline that explicitly accounts for the specific strata where individual oscillatory power is high, in analysing simultaneously recorded data from multiple strata. Our observations open avenues for investigations involving cross-strata interactions between theta oscillations and ripples across different behavioural states.
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Affiliation(s)
- Pavithraa Seenivasan
- Cellular Neurophysiology Laboratory, Molecular Biophysics Unit, Indian Institute of Science, Bangalore, India
| | - Reshma Basak
- Cellular Neurophysiology Laboratory, Molecular Biophysics Unit, Indian Institute of Science, Bangalore, India
| | - Rishikesh Narayanan
- Cellular Neurophysiology Laboratory, Molecular Biophysics Unit, Indian Institute of Science, Bangalore, India
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13
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Méndez JC, Perry BAL, Premereur E, Pelekanos V, Ramadan T, Mitchell AS. Variable cardiac responses in rhesus macaque monkeys after discrete mediodorsal thalamus manipulations. Sci Rep 2023; 13:16913. [PMID: 37805650 PMCID: PMC10560229 DOI: 10.1038/s41598-023-42752-4] [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: 11/19/2022] [Accepted: 09/14/2023] [Indexed: 10/09/2023] Open
Abstract
The control of some physiological parameters, such as the heart rate, is known to have a role in cognitive and emotional processes. Cardiac changes are also linked to mental health issues and neurodegeneration. Thus, it is not surprising that many of the brain structures typically associated with cognition and emotion also comprise a circuit-the central automatic network-responsible for the modulation of cardiovascular output. The mediodorsal thalamus (MD) is involved in higher cognitive processes and is also known to be connected to some of the key neural structures that regulate cardiovascular function. However, it is unclear whether the MD has any role in this circuitry. Here, we show that discrete manipulations (microstimulation during anaesthetized functional neuroimaging or localized cytotoxin infusions) to either the magnocellular or the parvocellular MD subdivisions led to observable and variable changes in the heart rate of female and male rhesus macaque monkeys. Considering the central positions that these two MD subdivisions have in frontal cortico-thalamocortical circuits, our findings suggest that MD contributions to autonomic regulation may interact with its identified role in higher cognitive processes, representing an important physiological link between cognition and emotion.
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Affiliation(s)
- Juan Carlos Méndez
- Department of Clinical and Biomedical Sciences, University of Exeter, College House, St Luke's Campus, Heavitree Road, Exeter, EX1 2LU, UK
| | - Brook A L Perry
- Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK
| | - Elsie Premereur
- Laboratory for Neuro- and Psychophysiology, KU Leuven, Leuven, Belgium
| | | | - Tamara Ramadan
- Department of Biological Sciences, University of Oxford, Oxford, UK
| | - Anna S Mitchell
- Department of Psychology, Speech and Hearing, University of Canterbury, Christchurch, 8041, New Zealand.
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14
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Wamsley EJ, Arora M, Gibson H, Powell P, Collins M. Memory Consolidation during Ultra-short Offline States. J Cogn Neurosci 2023; 35:1617-1634. [PMID: 37584585 DOI: 10.1162/jocn_a_02035] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 08/17/2023]
Abstract
Traditionally, neuroscience and psychology have studied the human brain during periods of "online" attention to the environment, while participants actively engage in processing sensory stimuli. However, emerging evidence shows that the waking brain also intermittently enters an "offline" state, during which sensory processing is inhibited and our attention shifts inward. In fact, humans may spend up to half of their waking hours offline [Wamsley, E. J., & Summer, T. Spontaneous entry into an "offline" state during wakefulness: A mechanism of memory consolidation? Journal of Cognitive Neuroscience, 32, 1714-1734, 2020; Killingsworth, M. A., & Gilbert, D. T. A wandering mind is an unhappy mind. Science, 330, 932, 2010]. The function of alternating between online and offline forms of wakefulness remains unknown. We hypothesized that rapidly switching between online and offline states enables the brain to alternate between the competing demands of encoding new information and consolidating already-encoded information. A total of 46 participants (34 female) trained on a memory task just before a 30-min retention interval, during which they completed a simple attention task while undergoing simultaneous high-density EEG and pupillometry recording. We used a data-driven method to parse this retention interval into a sequence of discrete online and offline states, with a 5-sec temporal resolution. We found evidence for three distinct states, one of which was an offline state with features well-suited to support memory consolidation, including increased EEG slow oscillation power, reduced attention to the external environment, and increased pupil diameter (a proxy for increased norepinephrine). Participants who spent more time in this offline state following encoding showed improved memory at delayed test. These observations are consistent with the hypothesis that even brief, seconds-long entry into an offline state may support the early stages of memory consolidation.
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15
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Wang QW, Qin J, Chen YF, Tu Y, Xing YY, Wang Y, Yang LY, Lu SY, Geng L, Shi W, Yang Y, Yao J. 16p11.2 CNV gene Doc2α functions in neurodevelopment and social behaviors through interaction with Secretagogin. Cell Rep 2023; 42:112691. [PMID: 37354460 DOI: 10.1016/j.celrep.2023.112691] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/12/2022] [Revised: 04/22/2023] [Accepted: 06/08/2023] [Indexed: 06/26/2023] Open
Abstract
Copy-number variations (CNVs) of the human 16p11.2 genetic locus are associated with neurodevelopmental disorders, including autism spectrum disorders (ASDs) and schizophrenia. However, it remains largely unclear how this locus is involved in the disease pathogenesis. Doc2α is localized within this locus. Here, using in vivo and ex vivo electrophysiological and morphological approaches, we show that Doc2α-deficient mice have neuronal morphological abnormalities and defects in neural activity. Moreover, the Doc2α-deficient mice exhibit social and repetitive behavioral deficits. Furthermore, we demonstrate that Doc2α functions in behavioral and neural phenotypes through interaction with Secretagogin (SCGN). Finally, we demonstrate that SCGN functions in social/repetitive behaviors, glutamate release, and neuronal morphology of the mice through its Doc2α-interacting activity. Therefore, Doc2α likely contributes to neurodevelopmental disorders through its interaction with SCGN.
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Affiliation(s)
- Qiu-Wen Wang
- State Key Laboratory of Membrane Biology, Tsinghua-Peking Center for Life Sciences, IDG/McGovern Institute for Brain Research, School of Life Sciences, Tsinghua University, Beijing 100084, China
| | - Junhong Qin
- Key Laboratory of Birth Defects and Related Diseases of Women and Children, Department of Paediatrics, West China Second University Hospital, State Key Laboratory of Biotherapy, Sichuan University, Chengdu 610041, China; School of Life Sciences, Tsinghua University, Beijing 100084, China
| | - Yan-Fen Chen
- State Key Laboratory of Membrane Biology, Tsinghua-Peking Center for Life Sciences, IDG/McGovern Institute for Brain Research, School of Life Sciences, Tsinghua University, Beijing 100084, China
| | - Yingfeng Tu
- Key Laboratory of Birth Defects and Related Diseases of Women and Children, Department of Paediatrics, West China Second University Hospital, State Key Laboratory of Biotherapy, Sichuan University, Chengdu 610041, China; School of Life Sciences, Tsinghua University, Beijing 100084, China
| | - Yun-Yun Xing
- Jiangsu Key Laboratory of Language and Cognitive Neuroscience, School of Linguistic Sciences and Arts, Jiangsu Normal University, Xuzhou 221116, China; Jiangsu Collaborative Innovation Center for Language Ability, Xuzhou 221009, China
| | - Yuchen Wang
- School of Engineering Medicine and School of Biological Science and Medical Engineering, Beihang University, Beijing 100191, China
| | - Lv-Yu Yang
- State Key Laboratory of Membrane Biology, Tsinghua-Peking Center for Life Sciences, IDG/McGovern Institute for Brain Research, School of Life Sciences, Tsinghua University, Beijing 100084, China
| | - Si-Yao Lu
- Jiangsu Key Laboratory of Language and Cognitive Neuroscience, School of Linguistic Sciences and Arts, Jiangsu Normal University, Xuzhou 221116, China; Jiangsu Collaborative Innovation Center for Language Ability, Xuzhou 221009, China
| | - Libo Geng
- Jiangsu Key Laboratory of Language and Cognitive Neuroscience, School of Linguistic Sciences and Arts, Jiangsu Normal University, Xuzhou 221116, China; Jiangsu Collaborative Innovation Center for Language Ability, Xuzhou 221009, China
| | - Wei Shi
- School of Engineering Medicine and School of Biological Science and Medical Engineering, Beihang University, Beijing 100191, China.
| | - Yiming Yang
- Jiangsu Key Laboratory of Language and Cognitive Neuroscience, School of Linguistic Sciences and Arts, Jiangsu Normal University, Xuzhou 221116, China; Jiangsu Collaborative Innovation Center for Language Ability, Xuzhou 221009, China.
| | - Jun Yao
- State Key Laboratory of Membrane Biology, Tsinghua-Peking Center for Life Sciences, IDG/McGovern Institute for Brain Research, School of Life Sciences, Tsinghua University, Beijing 100084, China.
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16
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Xie B, Zhen Z, Guo O, Li H, Guo M, Zhen J. Progress on the hippocampal circuits and functions based on sharp wave ripples. Brain Res Bull 2023:110695. [PMID: 37353037 DOI: 10.1016/j.brainresbull.2023.110695] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/21/2023] [Revised: 06/18/2023] [Accepted: 06/20/2023] [Indexed: 06/25/2023]
Abstract
Sharp wave ripples (SWRs) are high-frequency synchronization events generated by hippocampal neuronal circuits during various forms of learning and reactivated during memory consolidation and recall. There is mounting evidence that SWRs are essential for storing spatial and social memories in rodents and short-term episodic memories in humans. Sharp wave ripples originate mainly from the hippocampal CA3 and subiculum, and can be transmitted to modulate neuronal activity in cortical and subcortical regions for long-term memory consolidation and behavioral guidance. Different hippocampal subregions have distinct functions in learning and memory. For instance, the dorsal CA1 is critical for spatial navigation, episodic memory, and learning, while the ventral CA1 and dorsal CA2 may work cooperatively to store and consolidate social memories. Here, we summarize recent studies demonstrating that SWRs are essential for the consolidation of spatial, episodic, and social memories in various hippocampal-cortical pathways, and review evidence that SWR dysregulation contributes to cognitive impairments in neurodegenerative and neurodevelopmental diseases.
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Affiliation(s)
- Boxu Xie
- Department of Neurology, The Second Hospital of Hebei Medical University, Shijiazhuang, China
| | - Zhihang Zhen
- Department of Neurology, The Second Hospital of Hebei Medical University, Shijiazhuang, China
| | - Ouyang Guo
- Department of Biology, Boston University, Boston, MA, United States
| | - Heming Li
- Department of Neurology, The Second Hospital of Hebei Medical University, Shijiazhuang, China
| | - Moran Guo
- Neurological Laboratory of Hebei Province, Shijiazhuang, China
| | - Junli Zhen
- Department of Neurology, The Second Hospital of Hebei Medical University, Shijiazhuang, China; Neurological Laboratory of Hebei Province, Shijiazhuang, China.
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17
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Simor P, Peigneux P, Bódizs R. Sleep and dreaming in the light of reactive and predictive homeostasis. Neurosci Biobehav Rev 2023; 147:105104. [PMID: 36804397 DOI: 10.1016/j.neubiorev.2023.105104] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/30/2022] [Revised: 02/07/2023] [Accepted: 02/16/2023] [Indexed: 02/19/2023]
Abstract
Dreams are often viewed as fascinating but irrelevant mental epihenomena of the sleeping mind with questionable functional relevance. Despite long hours of oneiric activity, and high individual differences in dream recall, dreams are lost into oblivion. Here, we conceptualize dreaming and dream amnesia as inherent aspects of the reactive and predictive homeostatic functions of sleep. Mental activity during sleep conforms to the interplay of restorative processes and future anticipation, and particularly during the second half of the night, it unfolds as a special form of non-constrained, self-referent, and future-oriented cognitive process. Awakening facilitates constrained, goal-directed prospection that competes for shared neural resources with dream production and dream recall, and contributes to dream amnesia. We present the neurophysiological aspects of reactive and predictive homeostasis during sleep, highlighting the putative role of cortisol in predictive homeostasis and forgetting dreams. The theoretical and methodological aspects of our proposal are discussed in relation to the study of dreaming, dream recall, and sleep-related cognitive processes.
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Affiliation(s)
- Péter Simor
- Institute of Psychology, ELTE, Eötvös Loránd University, Budapest, Hungary; UR2NF, Neuropsychology and Functional Neuroimaging Research Unit at CRCN - Center for Research in Cognition and Neurosciences and UNI - ULB Neurosciences Institute, Université Libre de Bruxelles (ULB), Brussels, Belgium
| | - Philippe Peigneux
- UR2NF, Neuropsychology and Functional Neuroimaging Research Unit at CRCN - Center for Research in Cognition and Neurosciences and UNI - ULB Neurosciences Institute, Université Libre de Bruxelles (ULB), Brussels, Belgium
| | - Róbert Bódizs
- Institute of Behavioural Sciences, Semmelweis University, Budapest, Hungary.
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18
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Muñoz-Torres Z, Corsi-Cabrera M, Velasco F, Velasco AL. Amygdala and hippocampus dialogue with neocortex during human sleep and wakefulness. Sleep 2023; 46:6702585. [PMID: 36124713 DOI: 10.1093/sleep/zsac224] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/28/2022] [Revised: 09/03/2022] [Indexed: 01/13/2023] Open
Abstract
ABSTRACT Previous studies have described synchronic electroencephalographic (EEG) patterns of the background activity that is characteristic of several vigilance states. STUDY OBJECTIVES To explore whether the background synchronous activity of the amygdala-hippocampal-neocortical circuit is modified during sleep in the delta, theta, alpha, sigma, beta, and gamma bands characteristic of each sleep state. METHODS By simultaneously recording intracranial and noninvasive scalp EEG (10-20 system) in epileptic patients who were candidates for neurosurgery, we explored synchronous activity among the amygdala, hippocampus, and neocortex during wakefulness (W), Non-Rapid Eye Movement (NREM), and Rapid-Eye Movement (REM) sleep. RESULTS Our findings reveal that hippocampal-cortical synchrony in the sleep spindle frequencies was spread across the cortex and was higher during NREM versus W and REM, whereas the amygdala showed punctual higher synchronization with the temporal lobe. Contrary to expectations, delta synchrony between the amygdala and frontal lobe and between the hippocampus and temporal lobe was higher during REM than NREM. Gamma and alpha showed higher synchrony between limbic structures and the neocortex during wakefulness versus sleep, while synchrony among deep structures showed a mixed pattern. On the one hand, amygdala-hippocampal synchrony resembled cortical activity (i.e. higher gamma and alpha synchrony in W); on the other, it showed its own pattern in slow frequency oscillations. CONCLUSIONS This is the first study to depict diverse patterns of synchronic interaction among the frequency bands during distinct vigilance states in a broad human brain circuit with direct anatomical and functional connections that play a crucial role in emotional processes and memory.
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Affiliation(s)
- Zeidy Muñoz-Torres
- Psychobiology and Neuroscience, Faculty of Psychology, Universidad Nacional Autónoma de México, Mexico, Mexico.,Neural Dynamics Group, Center for the Sciences of Complexity, Universidad Nacional Autónoma de México, Mexico, Mexico
| | - María Corsi-Cabrera
- Unit of Neurodevelopment, Institute of Neurobiology, Universidad Nacional Autónoma de México, Queretaro, Mexico.,Laboratory of Sleep, Faculty of Psychology, Universidad Nacional Autónoma de México, Mexico, Mexico
| | - Francisco Velasco
- Clinic of Epilepsy, Unit of Functional Neurosurgery, Stereotaxy and Radiosurgery, Hospital General de México, Mexico, Mexico
| | - Ana Luisa Velasco
- Clinic of Epilepsy, Unit of Functional Neurosurgery, Stereotaxy and Radiosurgery, Hospital General de México, Mexico, Mexico
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19
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Mushtaq M, Marshall L, Bazhenov M, Mölle M, Martinetz T. Differential thalamocortical interactions in slow and fast spindle generation: A computational model. PLoS One 2022; 17:e0277772. [PMID: 36508417 PMCID: PMC9744318 DOI: 10.1371/journal.pone.0277772] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/28/2022] [Accepted: 11/02/2022] [Indexed: 12/14/2022] Open
Abstract
Cortical slow oscillations (SOs) and thalamocortical sleep spindles are two prominent EEG rhythms of slow wave sleep. These EEG rhythms play an essential role in memory consolidation. In humans, sleep spindles are categorized into slow spindles (8-12 Hz) and fast spindles (12-16 Hz), with different properties. Slow spindles that couple with the up-to-down phase of the SO require more experimental and computational investigation to disclose their origin, functional relevance and most importantly their relation with SOs regarding memory consolidation. To examine slow spindles, we propose a biophysical thalamocortical model with two independent thalamic networks (one for slow and the other for fast spindles). Our modeling results show that fast spindles lead to faster cortical cell firing, and subsequently increase the amplitude of the cortical local field potential (LFP) during the SO down-to-up phase. Slow spindles also facilitate cortical cell firing, but the response is slower, thereby increasing the cortical LFP amplitude later, at the SO up-to-down phase of the SO cycle. Neither the SO rhythm nor the duration of the SO down state is affected by slow spindle activity. Furthermore, at a more hyperpolarized membrane potential level of fast thalamic subnetwork cells, the activity of fast spindles decreases, while the slow spindles activity increases. Together, our model results suggest that slow spindles may facilitate the initiation of the following SO cycle, without however affecting expression of the SO Up and Down states.
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Affiliation(s)
| | - Lisa Marshall
- Institute of Experimental and Clinical Pharmacology, University of Lübeck, Lübeck, Germany
- Center for Brain, Behavior and Metabolism, Lübeck, Germany
- University Clinic Hospital Schleswig Holstein, Lübeck, Germany
| | - Maxim Bazhenov
- Department of Medicine, University of California, San Diego, La Jolla, California, United States of America
| | - Matthias Mölle
- Center for Brain, Behavior and Metabolism, Lübeck, Germany
| | - Thomas Martinetz
- Institute for Neuro- and Bioinformatics, Lübeck, Germany
- Center for Brain, Behavior and Metabolism, Lübeck, Germany
- * E-mail:
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20
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Howard MD, Skorheim SW, Pilly PK. A model of bi-directional interactions between complementary learning systems for memory consolidation of sequential experiences. Front Syst Neurosci 2022; 16:972235. [PMID: 36313529 PMCID: PMC9606815 DOI: 10.3389/fnsys.2022.972235] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/18/2022] [Accepted: 09/26/2022] [Indexed: 11/13/2022] Open
Abstract
The standard theory of memory consolidation posits a dual-store memory system: a fast-learning fast-decaying hippocampus that transfers memories to slow-learning long-term cortical storage. Hippocampal lesions interrupt this transfer, so recent memories are more likely to be lost than more remote memories. Existing models of memory consolidation that simulate this temporally graded retrograde amnesia operate only on static patterns or unitary variables as memories and study only one-way interaction from the hippocampus to the cortex. However, the mechanisms underlying the consolidation of episodes, which are sequential in nature and comprise multiple events, are not well-understood. The representation of learning for sequential experiences in the cortical-hippocampal network as a self-consistent dynamical system is not sufficiently addressed in prior models. Further, there is evidence for a bi-directional interaction between the two memory systems during offline periods, whereby the reactivation of waking neural patterns originating in the cortex triggers time-compressed sequential replays in the hippocampus, which in turn drive the consolidation of the pertinent sequence in the cortex. We have developed a computational model of memory encoding, consolidation, and recall for storing temporal sequences that explores the dynamics of this bi-directional interaction and time-compressed replays in four simulation experiments, providing novel insights into whether hippocampal learning needs to be suppressed for stable memory consolidation and into how new and old memories compete for limited replay opportunities during offline periods. The salience of experienced events, based on factors such as recency and frequency of use, is shown to have considerable impact on memory consolidation because it biases the relative probability that a particular event will be cued in the cortex during offline periods. In the presence of hippocampal learning during sleep, our model predicts that the fast-forgetting hippocampus can continually refresh the memory traces of a given episodic sequence if there are no competing experiences to be replayed.
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21
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Abstract
Over the past few decades, the importance of sleep has become increasingly recognized for many physiologic functions, including cognition. Many studies have reported the deleterious effect of sleep loss or sleep disruption on cognitive performance. Beyond ensuring adequate sleep quality and duration, discovering methods to enhance sleep to augment its restorative effects is important to improve learning in many populations, such as the military, students, age-related cognitive decline, and cognitive disorders.
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Affiliation(s)
- Roneil G Malkani
- Division of Sleep Medicine, Department of Neurology, Center for Circadian and Sleep Medicine, Northwestern University Feinberg School of Medicine, 710 North Lake Shore Drive, Suite 525, Chicago, IL 60611, USA; Jesse Brown Veterans Affairs Medical Center, Chicago, IL 60612, USA.
| | - Phyllis C Zee
- Division of Sleep Medicine, Department of Neurology, Center for Circadian and Sleep Medicine, Northwestern University Feinberg School of Medicine, 710 North Lake Shore Drive, Suite 520, Chicago, IL 60611, USA
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22
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Maccabeo A, van 't Klooster MA, Schaft E, Demuru M, Zweiphenning W, Gosselaar P, Gebbink T, Otte WM, Zijlmans M. Spikes and High Frequency Oscillations in Lateral Neocortical Temporal Lobe Epilepsy: Can They Predict the Success Chance of Hippocampus-Sparing Resections? Front Neurol 2022; 13:797075. [PMID: 35983430 PMCID: PMC9379925 DOI: 10.3389/fneur.2022.797075] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/18/2021] [Accepted: 05/23/2022] [Indexed: 11/27/2022] Open
Abstract
Purpose We investigated the distribution of spikes and HFOs recorded during intraoperative electrocorticography (ioECoG) and tried to elaborate a predictive model for postsurgical outcomes of patients with lateral neocortical temporal lobe epilepsy (TLE) whose mesiotemporal structures are left in situ. Methods We selected patients with temporal lateral neocortical epilepsy focus who underwent ioECoG-tailored resections without amygdalo–hippocampectomies. We visually marked spikes, ripples (80–250 Hz), and fast ripples (FRs; 250–500 Hz) on neocortical and mesiotemporal channels before and after resections. We looked for differences in event rates and resection ratios between good (Engel 1A) and poor outcome groups and performed logistic regression analysis to identify outcome predictors. Results Fourteen out of 24 included patients had a good outcome. The poor-outcome patients showed higher rates of ripples on neocortical channels distant from the resection in pre- and post-ioECoG than people with good outcomes (ppre = 0.04, ppost = 0.05). Post-ioECoG FRs were found only in poor-outcome patients (N = 3). A prediction model based on regression analysis showed low rates of mesiotemporal post-ioECoG ripples (ORmesio = 0.13, pmesio = 0.04) and older age at epilepsy onset (OR = 1.76, p = 0.04) to be predictors of good seizure outcome. Conclusion HFOs in ioECoG may help to inform the neurosurgeon of the hippocampus-sparing resection success chance in patients with lateral neocortical TLE.
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Affiliation(s)
- Alessandra Maccabeo
- Department of Neurology and Neurosurgery, University Medical Center Utrecht Brain Center, University Medical Center Utrecht, Utrecht, Netherlands
| | - Maryse A. van 't Klooster
- Department of Neurology and Neurosurgery, University Medical Center Utrecht Brain Center, University Medical Center Utrecht, Utrecht, Netherlands
| | - Eline Schaft
- Department of Neurology and Neurosurgery, University Medical Center Utrecht Brain Center, University Medical Center Utrecht, Utrecht, Netherlands
| | - Matteo Demuru
- Department of Neurology and Neurosurgery, University Medical Center Utrecht Brain Center, University Medical Center Utrecht, Utrecht, Netherlands
- Stichting Epilepsie Instellingen Nederland, Heemstede, Netherlands
| | - Willemiek Zweiphenning
- Department of Neurology and Neurosurgery, University Medical Center Utrecht Brain Center, University Medical Center Utrecht, Utrecht, Netherlands
| | - Peter Gosselaar
- Department of Neurology and Neurosurgery, University Medical Center Utrecht Brain Center, University Medical Center Utrecht, Utrecht, Netherlands
| | - Tineke Gebbink
- Department of Neurology and Neurosurgery, University Medical Center Utrecht Brain Center, University Medical Center Utrecht, Utrecht, Netherlands
| | - Wim M. Otte
- Department of Neurology and Neurosurgery, University Medical Center Utrecht Brain Center, University Medical Center Utrecht, Utrecht, Netherlands
| | - Maeike Zijlmans
- Department of Neurology and Neurosurgery, University Medical Center Utrecht Brain Center, University Medical Center Utrecht, Utrecht, Netherlands
- Stichting Epilepsie Instellingen Nederland, Heemstede, Netherlands
- *Correspondence: Maeike Zijlmans
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23
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Gaviraghi Mussoi J, Stanley MC, Cain KE. Importance of sleep for avian vocal communication. Biol Lett 2022; 18:20220223. [PMID: 35975628 PMCID: PMC9382451 DOI: 10.1098/rsbl.2022.0223] [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] [Indexed: 11/12/2022] Open
Abstract
Sleep is one of the few truly ubiquitous animal behaviours, and though many animals spend enormous periods of time asleep, we have only begun to understand the consequences of sleep disturbances. In humans, sleep is crucial for effective communication. Birds are classic models for understanding the evolution and mechanisms of human language and speech. Bird vocalizations are remarkably diverse, critical, fitness-related behaviours, and the way sleep affects vocalizations is likely similarly varied. However, research on the effects of sleep disturbances on avian vocalizations is shockingly scarce. Consequently, there is a critical gap in our understanding of the extent to which sleep disturbances disrupt communication. Here, we argue that sleep disturbances are likely to affect all birds' vocal performance by interfering with motivation, memory consolidation and vocal maintenance. Further, we suggest that quality sleep is likely essential when learning new vocalizations and that sleep disturbances will have especially strong effects on learned vocalizations. Finally, we advocate for future research to address gaps in our understanding of how sleep influences vocal learning and performance in birds.
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Affiliation(s)
| | - Margaret C Stanley
- School of Biological Sciences, The University of Auckland, Auckland, New Zealand
| | - Kristal E Cain
- School of Biological Sciences, The University of Auckland, Auckland, New Zealand
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Totty MS, Maren S. Neural Oscillations in Aversively Motivated Behavior. Front Behav Neurosci 2022; 16:936036. [PMID: 35846784 PMCID: PMC9284508 DOI: 10.3389/fnbeh.2022.936036] [Citation(s) in RCA: 13] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/04/2022] [Accepted: 06/14/2022] [Indexed: 12/12/2022] Open
Abstract
Fear and anxiety-based disorders are highly debilitating and among the most prevalent psychiatric disorders. These disorders are associated with abnormal network oscillations in the brain, yet a comprehensive understanding of the role of network oscillations in the regulation of aversively motivated behavior is lacking. In this review, we examine the oscillatory correlates of fear and anxiety with a particular focus on rhythms in the theta and gamma-range. First, we describe neural oscillations and their link to neural function by detailing the role of well-studied theta and gamma rhythms to spatial and memory functions of the hippocampus. We then describe how theta and gamma oscillations act to synchronize brain structures to guide adaptive fear and anxiety-like behavior. In short, that hippocampal network oscillations act to integrate spatial information with motivationally salient information from the amygdala during states of anxiety before routing this information via theta oscillations to appropriate target regions, such as the prefrontal cortex. Moreover, theta and gamma oscillations develop in the amygdala and neocortical areas during the encoding of fear memories, and interregional synchronization reflects the retrieval of both recent and remotely encoded fear memories. Finally, we argue that the thalamic nucleus reuniens represents a key node synchronizing prefrontal-hippocampal theta dynamics for the retrieval of episodic extinction memories in the hippocampus.
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B. Szabo A, Cretin B, Gérard F, Curot J, J. Barbeau E, Pariente J, Dahan L, Valton L. Sleep: The Tip of the Iceberg in the Bidirectional Link Between Alzheimer's Disease and Epilepsy. Front Neurol 2022; 13:836292. [PMID: 35481265 PMCID: PMC9035794 DOI: 10.3389/fneur.2022.836292] [Citation(s) in RCA: 12] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/15/2021] [Accepted: 02/14/2022] [Indexed: 11/13/2022] Open
Abstract
The observation that a pathophysiological link might exist between Alzheimer's disease (AD) and epilepsy dates back to the identification of the first cases of the pathology itself and is now strongly supported by an ever-increasing mountain of literature. An overwhelming majority of data suggests not only a higher prevalence of epilepsy in Alzheimer's disease compared to healthy aging, but also that AD patients with a comorbid epileptic syndrome, even subclinical, have a steeper cognitive decline. Moreover, clinical and preclinical investigations have revealed a marked sleep-related increase in the frequency of epileptic activities. This characteristic might provide clues to the pathophysiological pathways underlying this comorbidity. Furthermore, the preferential sleep-related occurrence of epileptic events opens up the possibility that they might hasten cognitive decline by interfering with the delicately orchestrated synchrony of oscillatory activities implicated in sleep-related memory consolidation. Therefore, we scrutinized the literature for mechanisms that might promote sleep-related epileptic activity in AD and, possibly dementia onset in epilepsy, and we also aimed to determine to what degree and through which processes such events might alter the progression of AD. Finally, we discuss the implications for patient care and try to identify a common basis for methodological considerations for future research and clinical practice.
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Affiliation(s)
- Anna B. Szabo
- Centre de Recherches sur la Cognition Animale, Centre de Biologie Intégrative, Université de Toulouse, CNRS, UPS, Toulouse, France
- Centre de Recherche Cerveau & Cognition (CerCo), UMR 5549, CNRS-UPS, Toulouse, France
- *Correspondence: Anna B. Szabo
| | - Benjamin Cretin
- Clinical Neuropsychology Unit, Neurology Department, CM2R (Memory Resource and Research Centre), University Hospital of Strasbourg, Strasbourg, France
- CNRS, ICube Laboratory, UMR 7357 and FMTS (Fédération de Médecine Translationnelle de Strasbourg), Team IMIS, University of Strasbourg, Strasbourg, France
- CMRR d'Alsace, Service de Neurologie des Hôpitaux Universitaires de Strasbourg, Pôle Tête et Cou, Strasbourg, France
| | - Fleur Gérard
- Centre de Recherche Cerveau & Cognition (CerCo), UMR 5549, CNRS-UPS, Toulouse, France
- Neurology Department, Hôpital Purpan Centre Hospitalier Universitaire de Toulouse, Toulouse, France
| | - Jonathan Curot
- Centre de Recherche Cerveau & Cognition (CerCo), UMR 5549, CNRS-UPS, Toulouse, France
- Neurology Department, Hôpital Purpan Centre Hospitalier Universitaire de Toulouse, Toulouse, France
| | - Emmanuel J. Barbeau
- Centre de Recherche Cerveau & Cognition (CerCo), UMR 5549, CNRS-UPS, Toulouse, France
| | - Jérémie Pariente
- Neurology Department, Hôpital Purpan Centre Hospitalier Universitaire de Toulouse, Toulouse, France
- Toulouse NeuroImaging Center (ToNIC), INSERM-University of Toulouse Paul Sabatier, Toulouse, France
| | - Lionel Dahan
- Centre de Recherches sur la Cognition Animale, Centre de Biologie Intégrative, Université de Toulouse, CNRS, UPS, Toulouse, France
| | - Luc Valton
- Centre de Recherche Cerveau & Cognition (CerCo), UMR 5549, CNRS-UPS, Toulouse, France
- Neurology Department, Hôpital Purpan Centre Hospitalier Universitaire de Toulouse, Toulouse, France
- Luc Valton
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Hoedlmoser K, Peigneux P, Rauchs G. Recent advances in memory consolidation and information processing during sleep. J Sleep Res 2022; 31:e13607. [DOI: 10.1111/jsr.13607] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/15/2022] [Revised: 03/25/2022] [Accepted: 03/25/2022] [Indexed: 12/20/2022]
Affiliation(s)
- Kerstin Hoedlmoser
- Department of Psychology, Centre for Cognitive Neuroscience (CCNS), Laboratory for “Sleep, Cognition and Consciousness Research” University of Salzburg Salzburg Austria
| | - Philippe Peigneux
- UR2NF – Neuropsychology and Functional Neuroimaging Research Unit affiliated at CRCN – Centre for Research in Cognition and Neurosciences and UNI – ULB Neuroscience Institute Bruxelles Belgium
| | - Géraldine Rauchs
- UNICAEN, INSERM, U1237, PhIND “Physiopathology and Imaging of Neurological Disorders”, Institut Blood and Brain @ Caen‐Normandie Normandie Univ Caen France
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Lei Z, Henderson K, Keleman K. A neural circuit linking learning and sleep in Drosophila long-term memory. Nat Commun 2022; 13:609. [PMID: 35105888 PMCID: PMC8807839 DOI: 10.1038/s41467-022-28256-1] [Citation(s) in RCA: 11] [Impact Index Per Article: 3.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/16/2021] [Accepted: 01/07/2022] [Indexed: 12/02/2022] Open
Abstract
Animals retain some but not all experiences in long-term memory (LTM). Sleep supports LTM retention across animal species. It is well established that learning experiences enhance post-learning sleep. However, the underlying mechanisms of how learning mediates sleep for memory retention are not clear. Drosophila males display increased amounts of sleep after courtship learning. Courtship learning depends on Mushroom Body (MB) neurons, and post-learning sleep is mediated by the sleep-promoting ventral Fan-Shaped Body neurons (vFBs). We show that post-learning sleep is regulated by two opposing output neurons (MBONs) from the MB, which encode a measure of learning. Excitatory MBONs-γ2α'1 becomes increasingly active upon increasing time of learning, whereas inhibitory MBONs-β'2mp is activated only by a short learning experience. These MB outputs are integrated by SFS neurons, which excite vFBs to promote sleep after prolonged but not short training. This circuit may ensure that only longer or more intense learning experiences induce sleep and are thereby consolidated into LTM.
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Affiliation(s)
- Zhengchang Lei
- Janelia Research Campus, HHMI, 19700 Helix Dr, Ashburn, VA, 20147, USA
| | - Kristin Henderson
- Janelia Research Campus, HHMI, 19700 Helix Dr, Ashburn, VA, 20147, USA
| | - Krystyna Keleman
- Janelia Research Campus, HHMI, 19700 Helix Dr, Ashburn, VA, 20147, USA.
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Shahveisi K, Abdoli N, Farnia V, Khazaie H, Hosseini M, Ghazvini H, Khodamoradi M. REM sleep deprivation before extinction or reinstatement alters methamphetamine reward memory via D1-like dopamine receptors. Pharmacol Biochem Behav 2022; 213:173319. [PMID: 34990706 DOI: 10.1016/j.pbb.2021.173319] [Citation(s) in RCA: 12] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/03/2021] [Revised: 11/26/2021] [Accepted: 12/25/2021] [Indexed: 12/14/2022]
Abstract
We aimed to determine whether REM sleep deprivation (RSD) affects extinction and reinstatement of methamphetamine (METH) reward memory in male rats and also to evaluate the possible role of dopamine D1-like and D2-like dopamine (DA) receptors in these processes. Male rats were trained to acquire METH-induced place preference (2 mg/kg, i.p.). METH reward memory was then reinstated following a 10-day extinction period. The animals underwent a 72-hour sleep deprivation episode by multiple platforms method (in separate groups), either before the extraction or before the reinstatement of METH reward memory. The animals received SCH 23390 (0.01 or 0.05 mg/kg, i.p.) or sulpiride (20 or 60 mg/kg, i.p.) as antagonists of D1-like and D2-like DA receptors, respectively, either immediately following each daily extinction session or before the reinstatement of METH-seeking behavior. The RSD episode postponed extinction and facilitated reinstatement of METH reward memory. Administration of SCH 23390, but not sulpiride, facilitated METH extinction and decreased reinstatement of the extinguished METH-seeking behavior. Moreover, locomotor activity was not affected by METH and/or the RSD paradigm. The results would seem to suggest that the D1-like, but not the D2-like, DA receptors may be involved in the extinction and reinstatement of the extinguished METH reward memory in RSD animals. Nonetheless, more investigations are needed to elucidate the exact mechanisms involved.
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Affiliation(s)
- Kaveh Shahveisi
- Sleep Disorders Research Center, Kermanshah University of Medical Sciences, Kermanshah, Iran
| | - Nasrin Abdoli
- Substance Abuse Prevention Research Center, Health Institute, Kermanshah University of Medical Sciences, Kermanshah, Iran
| | - Vahid Farnia
- Substance Abuse Prevention Research Center, Health Institute, Kermanshah University of Medical Sciences, Kermanshah, Iran
| | - Habibolah Khazaie
- Sleep Disorders Research Center, Kermanshah University of Medical Sciences, Kermanshah, Iran
| | - Mahmoud Hosseini
- Division of Neurocognitive Sciences, Psychiatry and Behavioral Sciences Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
| | - Hamed Ghazvini
- Department of Neuroscience, School of Advanced Technologies in Medicine, Mazandaran University of Medical Sciences, Sari, Iran
| | - Mehdi Khodamoradi
- Substance Abuse Prevention Research Center, Health Institute, Kermanshah University of Medical Sciences, Kermanshah, Iran.
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Karalis N, Sirota A. Breathing coordinates cortico-hippocampal dynamics in mice during offline states. Nat Commun 2022; 13:467. [PMID: 35075139 PMCID: PMC8786964 DOI: 10.1038/s41467-022-28090-5] [Citation(s) in RCA: 91] [Impact Index Per Article: 30.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/04/2021] [Accepted: 12/13/2021] [Indexed: 12/18/2022] Open
Abstract
Network dynamics have been proposed as a mechanistic substrate for the information transfer across cortical and hippocampal circuits. However, little is known about the mechanisms that synchronize and coordinate these processes across widespread brain regions during offline states. Here we address the hypothesis that breathing acts as an oscillatory pacemaker, persistently coupling distributed brain circuit dynamics. Using large-scale recordings from a number of cortical and subcortical brain regions in behaving mice, we uncover the presence of an intracerebral respiratory corollary discharge, that modulates neural activity across these circuits. During offline states, the respiratory modulation underlies the coupling of hippocampal sharp-wave ripples and cortical DOWN/UP state transitions, which mediates systems memory consolidation. These results highlight breathing, a perennial brain rhythm, as an oscillatory scaffold for the functional coordination of the limbic circuit that supports the segregation and integration of information flow across neuronal networks during offline states.
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Affiliation(s)
- Nikolaos Karalis
- Faculty of Medicine, Ludwig-Maximilian University, Munich, 82152, Martinsried, Germany.
- Friedrich Miescher Institute for Biomedical Research, 4058, Basel, Switzerland.
| | - Anton Sirota
- Faculty of Medicine, Ludwig-Maximilian University, Munich, 82152, Martinsried, Germany.
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30
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Dissanayaka T, Zoghi M, Farrell M, Egan G, Jaberzadeh S. The effects of monophasic anodal transcranial pulsed current stimulation on corticospinal excitability and motor performance in healthy young adults: A randomized double-blind sham-controlled study. Brain Connect 2021; 12:260-274. [PMID: 34963309 DOI: 10.1089/brain.2020.0949] [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] [Indexed: 11/13/2022] Open
Abstract
INTRODUCTION Transcranial pulsed current stimulation (tPCS) could be used to deliver electrical pulses at different frequencies to entrain the cortical neurons of the brain. Frequency dependence of these pulses in the induction of changes in corticospinal excitability (CSE) has not been reported. OBJECTIVE We aimed to assess the effect of anodal tPCS (a-tPCS) at theta (4 Hz), and gamma (75 Hz) frequencies on CSE as assessed by the peak-to-peak amplitude of transcranial magnetic stimulation (TMS) induced motor evoked potentials (MEPs) and motor performance. METHOD In a randomized double-blinded sham-controlled cross over design study, seventeen healthy participants attended three experimental sessions and received either a-tPCS at 4 Hz, 75 Hz, or sham a-tPCS with 1.5 mA for 15 min. The amplitude of TMS induced resting MEPs and time for completion of the grooved pegboard test were recorded at baseline, immediately after, and 30-min after a-tPCS. RESULTS Both a-tPCS at 75 Hz and 4 Hz showed significantly increased CSE compared to sham. The a-tPCS at 75 Hz induced significantly higher CSE changes compared to 4 Hz. There was a significant increase in intracortical facilitation and a significant reduction in short-interval intra-cortical inhibition with both 4 and 75 Hz stimulation. However, the inhibition and facilitation did not correlate with CSE. Motor performance was unaffected by the interventions. CONCLUSION The high CSE changes in M1 in a-tPCS at 75 Hz provides an initial understanding of the frequency-specific effect of a-tPCS. More research is needed to establish this concept and to assess its behavioural relevance.
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Affiliation(s)
- Thusharika Dissanayaka
- Monash University, 2541, 6/63, Frankston-flinders road, Frankston, Frankston, Victoria, Australia, 3199;
| | - Maryam Zoghi
- La Trobe University, 2080, Melbourne, Victoria, Australia;
| | - Michael Farrell
- Monash University, 2541, Medical Imaging and Radiation Sciences, Wellington Road, Clayton, Victoria, Australia, 3800.,Monash University;
| | - Gary Egan
- Monash University, Monash Biomedical Imaging; School of Psychological Sciences, Melbourne, Victoria, Australia.,ARC Centre of Excellence for Integrative Brain Function, Melbourne, Australia;
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31
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Howe AG, Blair HT. Modulation of lateral septal and dorsomedial striatal neurons by hippocampal sharp-wave ripples, theta rhythm, and running speed. Hippocampus 2021; 32:153-178. [PMID: 34918836 PMCID: PMC9299855 DOI: 10.1002/hipo.23398] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/23/2020] [Revised: 05/04/2021] [Accepted: 11/28/2021] [Indexed: 11/12/2022]
Abstract
Single units were recorded in hippocampus, lateral septum (LS), and dorsomedial striatum (DMS) while freely behaving rats (n = 3) ran trials in a T‐maze task and rested in a holding bucket between trials. In LS, 28% (64/226) of recorded neurons were excited and 14% (31/226) were inhibited during sharp wave ripples (SWRs). LS neurons that were excited during SWRs fired preferentially on the downslope of hippocampal theta rhythm and had firing rates that were positively correlated with running speed; LS neurons that were inhibited during SWRs fired preferentially on the upslope of hippocampal theta rhythm and had firing rates that were negatively correlated with running speed. In DMS, only 3.3% (12/366) of recorded neurons were excited and 5.7% (21/366) were inhibited during SWRs. As in LS, DMS neurons that were excited by SWRs tended to have firing rates that were positively modulated by running speed, whereas DMS neurons that were inhibited by SWRs tended to have firing rates that were negatively modulated by running speed. But in contrast with LS, these two DMS subpopulations did not clearly segregate their spikes to different phases of the theta cycle. Based on these results and a review of prior findings, we discuss how concurrent activation of spatial trajectories in hippocampus and motor representations in LS and DMS may contribute to neural computations that support reinforcement learning and value‐based decision making.
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Affiliation(s)
- Andrew G Howe
- Department of Psychology, UCLA, Los Angeles, California, USA
| | - Hugh T Blair
- Department of Psychology, UCLA, Los Angeles, California, USA
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32
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Kozma R, Baars BJ, Geld N. Evolutionary Advantages of Stimulus-Driven EEG Phase Transitions in the Upper Cortical Layers. Front Syst Neurosci 2021; 15:784404. [PMID: 34955771 PMCID: PMC8692947 DOI: 10.3389/fnsys.2021.784404] [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: 09/27/2021] [Accepted: 11/03/2021] [Indexed: 11/13/2022] Open
Abstract
Spatio-temporal brain activity monitored by EEG recordings in humans and other mammals has identified beta/gamma oscillations (20-80 Hz), which are self-organized into spatio-temporal structures recurring at theta/alpha rates (4-12 Hz). These structures have statistically significant correlations with sensory stimuli and reinforcement contingencies perceived by the subject. The repeated collapse of self-organized structures at theta/alpha rates generates laterally propagating phase gradients (phase cones), ignited at some specific location of the cortical sheet. Phase cones have been interpreted as neural signatures of transient perceptual experiences according to the cinematic theory of brain dynamics. The rapid expansion of essentially isotropic phase cones is consistent with the propagation of perceptual broadcasts postulated by Global Workspace Theory (GWT). What is the evolutionary advantage of brains operating with repeatedly collapsing dynamics? This question is answered using thermodynamic concepts. According to neuropercolation theory, waking brains are described as non-equilibrium thermodynamic systems operating at the edge of criticality, undergoing repeated phase transitions. This work analyzes the role of long-range axonal connections and metabolic processes in the regulation of critical brain dynamics. Historically, the near 10 Hz domain has been associated with conscious sensory integration, cortical "ignitions" linked to conscious visual perception, and conscious experiences. We can therefore combine a very large body of experimental evidence and theory, including graph theory, neuropercolation, and GWT. This cortical operating style may optimize a tradeoff between rapid adaptation to novelty vs. stable and widespread self-organization, therefore resulting in significant Darwinian benefits.
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Affiliation(s)
- Robert Kozma
- Center for Large-Scale Intelligent Optimization and Networks, Department of Mathematics, University of Memphis, Memphis, TN, United States
| | - Bernard J. Baars
- Center for the Future Mind, Florida Atlantic University, Boca Raton, FL, United States
- Society for MindBrain Sciences, San Diego, CA, United States
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Parmar S, Tadavarty R, Sastry BR. G-protein coupled receptors and synaptic plasticity in sleep deprivation. World J Psychiatry 2021; 11:954-980. [PMID: 34888167 PMCID: PMC8613756 DOI: 10.5498/wjp.v11.i11.954] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/25/2021] [Revised: 06/05/2021] [Accepted: 09/19/2021] [Indexed: 02/06/2023] Open
Abstract
Insufficient sleep has been correlated to many physiological and psychoneurological disorders. Over the years, our understanding of the state of sleep has transcended from an inactive period of rest to a more active state involving important cellular and molecular processes. In addition, during sleep, electrophysiological changes also occur in pathways in specific regions of the mammalian central nervous system (CNS). Activity mediated synaptic plasticity in the CNS can lead to long-term and sometimes permanent strengthening and/or weakening synaptic strength affecting neuronal network behaviour. Memory consolidation and learning that take place during sleep cycles, can be affected by changes in synaptic plasticity during sleep disturbances. G-protein coupled receptors (GPCRs), with their versatile structural and functional attributes, can regulate synaptic plasticity in CNS and hence, may be potentially affected in sleep deprived conditions. In this review, we aim to discuss important functional changes that can take place in the CNS during sleep and sleep deprivation and how changes in GPCRs can lead to potential problems with therapeutics with pharmacological interventions.
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Affiliation(s)
- Shweta Parmar
- Department of Anesthesiology, Pharmacology and Therapeutics, The University of British Columbia, Vancouver V6T 1Z3, British Columbia, Canada
| | - Ramakrishna Tadavarty
- Department of Anesthesiology, Pharmacology and Therapeutics, The University of British Columbia, Vancouver V6T 1Z3, British Columbia, Canada
| | - Bhagavatula R Sastry
- Department of Anesthesiology, Pharmacology and Therapeutics, The University of British Columbia, Vancouver V6T 1Z3, British Columbia, Canada
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Czarnecki P, Lin J, Aton SJ, Zochowski M. Dynamical Mechanism Underlying Scale-Free Network Reorganization in Low Acetylcholine States Corresponding to Slow Wave Sleep. FRONTIERS IN NETWORK PHYSIOLOGY 2021; 1:759131. [PMID: 35785148 PMCID: PMC9249096 DOI: 10.3389/fnetp.2021.759131] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 08/15/2021] [Accepted: 10/07/2021] [Indexed: 11/13/2022]
Abstract
Sleep is indispensable for most animals' cognitive functions, and is hypothesized to be a major factor in memory consolidation. Although we do not fully understand the mechanisms of network reorganisation driving memory consolidation, available data suggests that sleep-associated neurochemical changes may be important for such processes. In particular, global acetylcholine levels change across the sleep/wake cycle, with high cholinergic tone during wake and REM sleep and low cholinergic tone during slow wave sleep. Furthermore, experimental perturbation of cholinergic tone has been shown to impact memory storage. Through in silico modeling of neuronal networks, we show how spiking dynamics change in highly heterogenous networks under varying levels of cholinergic tone, with neuronal networks under high cholinergic modulation firing asynchronously and at high frequencies, while those under low cholinergic modulation exhibit synchronous patterns of activity. We further examined the network's dynamics and its reorganization mediated via changing levels of acetylcholine within the context of different scale-free topologies, comparing network activity within the hub cells, a small group of neurons having high degree connectivity, and with the rest of the network. We show a dramatic, state-dependent change in information flow throughout the network, with highly active hub cells integrating information in a high-acetylcholine state, and transferring it to rest of the network in a low-acetylcholine state. This result is experimentally corroborated by frequency-dependent frequency changes observed in vivo experiments. Together, these findings provide insight into how new neurons are recruited into memory traces during sleep, a mechanism which may underlie system memory consolidation.
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Affiliation(s)
- Paulina Czarnecki
- Department of Mathematics, University of Michigan, Ann Arbor, MI, United States
| | - Jack Lin
- Neuroscience Graduate Program, University of Michigan, Ann Arbor, MI, United States
| | - Sara J. Aton
- Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI, United States
| | - Michal Zochowski
- Department of Physics and Biophysics Program, University of Michigan, Ann Arbor, MI, United States
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Ahnaou A, Drinkenburg WHIM. Sleep, neuronal hyperexcitability, inflammation and neurodegeneration: Does early chronic short sleep trigger and is it the key to overcoming Alzheimer's disease? Neurosci Biobehav Rev 2021; 129:157-179. [PMID: 34214513 DOI: 10.1016/j.neubiorev.2021.06.039] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/06/2020] [Revised: 05/13/2021] [Accepted: 06/25/2021] [Indexed: 01/13/2023]
Abstract
Evidence links neuroinflammation to Alzheimer's disease (AD); however, its exact contribution to the onset and progression of the disease is poorly understood. Symptoms of AD can be seen as the tip of an iceberg, consisting of a neuropathological build-up in the brain of extracellular amyloid-β (Aβ) plaques and intraneuronal hyperphosphorylated aggregates of Tau (pTau), which are thought to stem from an imbalance between its production and clearance resulting in loss of synaptic health and dysfunctional cortical connectivity. The glymphatic drainage system, which is particularly active during sleep, plays a key role in the clearance of proteinopathies. Poor sleep can cause hyperexcitability and promote Aβ and tau pathology leading to systemic inflammation. The early neuronal hyperexcitability of γ-aminobutyric acid (GABA)-ergic inhibitory interneurons and impaired inhibitory control of cortical pyramidal neurons lie at the crossroads of excitatory/inhibitory imbalance and inflammation. We outline, with a prospective framework, a possible vicious spiral linking early chronic short sleep, neuronal hyperexcitability, inflammation and neurodegeneration. Understanding the early predictors of AD, through an integrative approach, may hold promise for reducing attrition in the late stages of neuroprotective drug development.
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Affiliation(s)
- A Ahnaou
- Dept. of Neuroscience Discovery, Janssen Research & Development, A Division of Janssen Pharmaceutica NV, Turnhoutseweg 30, Beerse, B-2340, Belgium.
| | - W H I M Drinkenburg
- Dept. of Neuroscience Discovery, Janssen Research & Development, A Division of Janssen Pharmaceutica NV, Turnhoutseweg 30, Beerse, B-2340, Belgium
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Farhadian N, Khazaie H, Nami M, Khazaie S. The role of daytime napping in declarative memory performance: a systematic review. Sleep Med 2021; 84:134-141. [PMID: 34148000 DOI: 10.1016/j.sleep.2021.05.019] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/21/2020] [Revised: 04/25/2021] [Accepted: 05/20/2021] [Indexed: 10/21/2022]
Abstract
Sleep plays an important role in stabilizing and reinforcing memory of newly acquired information. Like nocturnal sleep, a daytime nap is shown to effectively contribute to memory processing. However, studies are often focused on nocturnal sleep. This review has aimed at systematically compiling the results of studies which have examined the effects of napping on declarative memory performance in healthy adults. Such studies have focused on different aspects of memory reinforcement following a diurnal nap including the involved mechanisms in memory reconsolidation, type of declarative tasks, cross-gender differences, the role of age, duration of nap and its delayed onset. One of the reviewed studies reported that even as short as 6 min of napping exerts a positive effect on memory function. Evidence from these studies indicates hippocampal-dependent enhancement of the learned information. Diurnal naps predominantly include non-rapid eye movement sleep with slow waves yielding potential effects on declarative memory. Evidence has shown that the empowered learning and retrieval depends upon spindle density during the nap. Moreover, the role of coordinated autonomic and central events in enhancing declarative memory has also been reported. Slow waves and sleep spindles are known to fuel declarative memory function during the NREM-2 (N2) stage of sleep.
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Affiliation(s)
- Negin Farhadian
- Substance Abuse Prevention Research Center, Health Institute, Kermanshah University of Medical Sciences, Kermanshah, Iran; Sleep Disorders Research Center, Kermanshah University of Medical Sciences, Kermanshah, Iran
| | - Habibolah Khazaie
- Sleep Disorders Research Center, Kermanshah University of Medical Sciences, Kermanshah, Iran
| | - Mohammad Nami
- Department of Neuroscience, School of Advanced Medical Sciences and Technologies, Shiraz University of Medical Sciences, Shiraz, Iran; Neuroscience Center, INDICASAT, Panama City, Republic of Panama; Society for Brain Mapping and Therapeutics and Brain Mapping Foundation, Los Angeles, CA, USA
| | - Sepideh Khazaie
- Sleep Disorders Research Center, Kermanshah University of Medical Sciences, Kermanshah, Iran; Student Research Committee, University of Medical Sciences, Kermanshah, Iran.
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37
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Joechner AK, Wehmeier S, Werkle-Bergner M. Electrophysiological indicators of sleep-associated memory consolidation in 5- to 6-year-old children. Psychophysiology 2021; 58:e13829. [PMID: 33951193 DOI: 10.1111/psyp.13829] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/29/2020] [Revised: 03/01/2021] [Accepted: 03/17/2021] [Indexed: 12/21/2022]
Abstract
In adults, the synchronized interplay of sleep spindles (SP) and slow oscillations (SO) supports memory consolidation. Given tremendous developmental changes in SP and SO morphology, it remains elusive whether across childhood the same mechanisms as identified in adults are functional. Based on topography and frequency, we characterize slow and fast SPs and their temporal coupling to SOs in 24 pre-school children. Further, we ask whether slow and fast SPs and their modulation during SOs are associated with behavioral indicators of declarative memory consolidation as suggested by the literature on adults. Employing an individually tailored approach, we reliably identify an inherent, development-specific fast centro-parietal SP type, nested in the adult-like slow SP frequency range, along with a dominant slow frontal SP type. Further, we provide evidence that the modulation of fast centro-parietal SPs during SOs is already present in pre-school children. However, the temporal coordination between fast centro-parietal SPs and SOs is weaker and less precise than expected from research on adults. While we do not find evidence for a critical contribution of SP-SO coupling for memory consolidation, crucially, slow frontal and fast centro-parietal SPs are each differentially related to sleep-associated consolidation of items of varying quality. Whereas a higher number of slow frontal SPs is associated with stronger maintenance of medium-quality memories, a higher number of fast centro-parietal SPs is linked to a greater gain of low-quality items. Our results demonstrate two functionally relevant inherent SP types in pre-school children although SP-SO coupling is not yet fully mature.
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Affiliation(s)
- Ann-Kathrin Joechner
- Center for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, Germany
| | - Sarah Wehmeier
- Center for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, Germany
| | - Markus Werkle-Bergner
- Center for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, Germany
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38
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Imbrosci B, Nitzan N, McKenzie S, Donoso JR, Swaminathan A, Böhm C, Maier N, Schmitz D. Subiculum as a generator of sharp wave-ripples in the rodent hippocampus. Cell Rep 2021; 35:109021. [PMID: 33882307 PMCID: PMC9239734 DOI: 10.1016/j.celrep.2021.109021] [Citation(s) in RCA: 13] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/27/2020] [Revised: 02/22/2021] [Accepted: 03/31/2021] [Indexed: 12/04/2022] Open
Abstract
Sharp wave-ripples (SWRs) represent synchronous discharges of hippocampal neurons and are believed to play a major role in memory consolidation. A large body of evidence suggests that SWRs are exclusively generated in the CA3-CA2 network. In contrast, here, we provide several lines of evidence showing that the subiculum can function as a secondary SWRs generator. SWRs with subicular origin propagate forward into the entorhinal cortex as well as backward into the hippocampus proper. Our findings suggest that the output structures of the hippocampus are not only passively facilitating the transfer of SWRs to the cortex, but they also can actively contribute to the genesis of SWRs. We hypothesize that SWRs with a subicular origin may be important for the consolidation of information conveyed to the hippocampus via the temporoammonic pathway. Imbrosci et al. show that the subiculum can work as a secondary generator of sharp wave-ripples (SWRs). SWRs with their origin in subiculum can propagate to the entorhinal cortex and backward to CA1 and CA3.
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Affiliation(s)
- Barbara Imbrosci
- German Center for Neurodegenerative Diseases (DZNE) Berlin, 10117 Berlin, Germany; Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117 Berlin, Germany
| | - Noam Nitzan
- Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117 Berlin, Germany
| | - Sam McKenzie
- Neuroscience Institute, New York University, New York, NY 10016, USA
| | - José R Donoso
- Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117 Berlin, Germany; Bernstein Center for Computational Neuroscience (BCCN) Berlin, 10115 Berlin, Germany
| | - Aarti Swaminathan
- Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117 Berlin, Germany
| | - Claudia Böhm
- Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117 Berlin, Germany
| | - Nikolaus Maier
- Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117 Berlin, Germany
| | - Dietmar Schmitz
- German Center for Neurodegenerative Diseases (DZNE) Berlin, 10117 Berlin, Germany; Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117 Berlin, Germany; NeuroCure Cluster of Excellence, Charitéplatz 1, 10117 Berlin, Germany; Bernstein Center for Computational Neuroscience (BCCN) Berlin, 10115 Berlin, Germany; Einstein Center for Neurosciences (ECN) Berlin, 10117 Berlin, Germany; Max-Delbrück-Centrum (MDC) for Molecular Medicine, 13125 Berlin, Germany.
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39
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Russo S, Pigorini A, Mikulan E, Sarasso S, Rubino A, Zauli FM, Parmigiani S, d'Orio P, Cattani A, Francione S, Tassi L, Bassetti CLA, Lo Russo G, Nobili L, Sartori I, Massimini M. Focal lesions induce large-scale percolation of sleep-like intracerebral activity in awake humans. Neuroimage 2021; 234:117964. [PMID: 33771696 DOI: 10.1016/j.neuroimage.2021.117964] [Citation(s) in RCA: 27] [Impact Index Per Article: 6.8] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/06/2020] [Revised: 02/15/2021] [Accepted: 03/08/2021] [Indexed: 11/26/2022] Open
Abstract
Focal cortical lesions are known to result in large-scale functional alterations involving distant areas; however, little is known about the electrophysiological mechanisms underlying these network effects. Here, we addressed this issue by analysing the short and long distance intracranial effects of controlled structural lesions in humans. The changes in Stereo-Electroencephalographic (SEEG) activity after Radiofrequency-Thermocoagulation (RFTC) recorded in 21 epileptic subjects were assessed with respect to baseline resting wakefulness and sleep activity. In addition, Cortico-Cortical Evoked Potentials (CCEPs) recorded before the lesion were employed to interpret these changes with respect to individual long-range connectivity patterns. We found that small structural ablations lead to the generation and large-scale propagation of sleep-like slow waves within the awake brain. These slow waves match those recorded in the same subjects during sleep, are prevalent in perilesional areas, but can percolate up to distances of 60 mm through specific long-range connections, as predicted by CCEPs. Given the known impact of slow waves on information processing and cortical plasticity, demonstrating their intrusion and percolation within the awake brain add key elements to our understanding of network dysfunction after cortical injuries.
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Affiliation(s)
- S Russo
- Department of Biomedical and Clinical Sciences "L. Sacco", University of Milan, Milan, Italy
| | - A Pigorini
- Department of Biomedical and Clinical Sciences "L. Sacco", University of Milan, Milan, Italy
| | - E Mikulan
- Department of Biomedical and Clinical Sciences "L. Sacco", University of Milan, Milan, Italy
| | - S Sarasso
- Department of Biomedical and Clinical Sciences "L. Sacco", University of Milan, Milan, Italy
| | - A Rubino
- "C. Munari" Epilepsy Surgery Centre, Department of Neuroscience, Niguarda Hospital, Milan 20162, Italy
| | - F M Zauli
- Department of Biomedical and Clinical Sciences "L. Sacco", University of Milan, Milan, Italy
| | - S Parmigiani
- Department of Biomedical and Clinical Sciences "L. Sacco", University of Milan, Milan, Italy
| | - P d'Orio
- "C. Munari" Epilepsy Surgery Centre, Department of Neuroscience, Niguarda Hospital, Milan 20162, Italy; Institute of Neuroscience, CNR, via Volturno 39E, 43125 Parma, Italy
| | - A Cattani
- Department of Biomedical and Clinical Sciences "L. Sacco", University of Milan, Milan, Italy; Department of Psychiatry, University of Wisconsin-Madison, Madison, WI, 53719, USA
| | - S Francione
- "C. Munari" Epilepsy Surgery Centre, Department of Neuroscience, Niguarda Hospital, Milan 20162, Italy
| | - L Tassi
- "C. Munari" Epilepsy Surgery Centre, Department of Neuroscience, Niguarda Hospital, Milan 20162, Italy
| | - C L A Bassetti
- Department of Neurology, Inselspital, University of Bern, Switzerland
| | - G Lo Russo
- "C. Munari" Epilepsy Surgery Centre, Department of Neuroscience, Niguarda Hospital, Milan 20162, Italy
| | - L Nobili
- Child Neuropsychiatry, IRCCS Istituto G. Gaslini, Genova 16147, Italy; Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DiNOGMI), University of Genoa, Genoa, Italy
| | - I Sartori
- "C. Munari" Epilepsy Surgery Centre, Department of Neuroscience, Niguarda Hospital, Milan 20162, Italy
| | - M Massimini
- Department of Biomedical and Clinical Sciences "L. Sacco", University of Milan, Milan, Italy; IRCCS, Fondazione Don Carlo Gnocchi, Milan 20148, Italy; Azrieli Program in Brain, Mind and Consciousness, Canadian Institute for Advanced Research, Toronto, Canada.
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40
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Heller HC. Question what is "known". Neurobiol Sleep Circadian Rhythms 2021; 10:100062. [PMID: 33681534 PMCID: PMC7930578 DOI: 10.1016/j.nbscr.2021.100062] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/25/2021] [Revised: 02/12/2021] [Accepted: 02/15/2021] [Indexed: 01/07/2023] Open
Abstract
We can “know” good data as true, but we cannot accept as fact interpretations of those data. Example: the assumption that both NREM and REM sleep are functional responses to prior wake, And, their cycling is controlled by a fixed period oscillator. Further research shows NREM and REM sleep are in a homeostatic relationship. Questioning interpretations can lead to valuable new research.
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41
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Ferraris M, Cassel JC, Pereira de Vasconcelos A, Stephan A, Quilichini PP. The nucleus reuniens, a thalamic relay for cortico-hippocampal interaction in recent and remote memory consolidation. Neurosci Biobehav Rev 2021; 125:339-354. [PMID: 33631314 DOI: 10.1016/j.neubiorev.2021.02.025] [Citation(s) in RCA: 27] [Impact Index Per Article: 6.8] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/07/2020] [Revised: 02/15/2021] [Accepted: 02/16/2021] [Indexed: 12/12/2022]
Abstract
The consolidation of declarative memories is believed to occur mostly during sleep and involves a dialogue between two brain regions, the hippocampus and the medial prefrontal cortex. The information encoded during experience by neuronal assemblies is replayed during sleep leading to the progressive strengthening and integration of the memory trace in the prefrontal cortex. The gradual transfer of information from the hippocampus to the medial prefrontal cortex for long-term storage requires the synchronization of cortico-hippocampal networks by different oscillations, like ripples, spindles, and slow oscillations. Recent studies suggest the involvement of a third partner, the nucleus reuniens, in memory consolidation. Its bidirectional connections with the hippocampus and medial prefrontal cortex place the reuniens in a key position to relay information between the two structures. Indeed, many topical works reveal the original role that the nucleus reuniens occupies in different recent and remote memories consolidation. This review aimed to examine these contributions, as well as its functional embedment in this complex memory network, and provide some insights on the possible mechanisms.
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Affiliation(s)
- Maëva Ferraris
- Aix Marseille Univ, INSERM, INS, Inst Neurosci Syst, Marseille, France
| | - Jean-Christophe Cassel
- Laboratoire De Neurosciences Cognitives Et Adaptatives, Université De Strasbourg, F-67000, Strasbourg, France; LNCA, UMR 7364 - CNRS, F-67000, Strasbourg, France
| | - Anne Pereira de Vasconcelos
- Laboratoire De Neurosciences Cognitives Et Adaptatives, Université De Strasbourg, F-67000, Strasbourg, France; LNCA, UMR 7364 - CNRS, F-67000, Strasbourg, France
| | - Aline Stephan
- Laboratoire De Neurosciences Cognitives Et Adaptatives, Université De Strasbourg, F-67000, Strasbourg, France; LNCA, UMR 7364 - CNRS, F-67000, Strasbourg, France
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42
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Travelling spindles create necessary conditions for spike-timing-dependent plasticity in humans. Nat Commun 2021; 12:1027. [PMID: 33589639 PMCID: PMC7884835 DOI: 10.1038/s41467-021-21298-x] [Citation(s) in RCA: 39] [Impact Index Per Article: 9.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/08/2020] [Accepted: 01/12/2021] [Indexed: 12/22/2022] Open
Abstract
Sleep spindles facilitate memory consolidation in the cortex during mammalian non-rapid eye movement sleep. In rodents, phase-locked firing during spindles may facilitate spike-timing-dependent plasticity by grouping pre-then-post-synaptic cell firing within ~25 ms. Currently, microphysiological evidence in humans for conditions conducive for spike-timing-dependent plasticity during spindles is absent. Here, we analyze field potentials and unit firing from middle/upper layers during spindles from 10 × 10 microelectrode arrays at 400 μm pitch in humans. We report strong tonic and phase-locked increases in firing and co-firing within 25 ms during spindles, especially those co-occurring with down-to-upstate transitions. Co-firing, spindle co-occurrence, and spindle coherence are greatest within ~2 mm, and high co-firing of units on different contacts depends on high spindle coherence between those contacts. Spindles propagate at ~0.28 m/s in distinct patterns, with correlated cell co-firing sequences. Spindles hence organize spatiotemporal patterns of neuronal co-firing in ways that may provide pre-conditions for plasticity during non-rapid eye movement sleep. Sleep spindles during non-rapid eye movement are important for memory consolidation and require specific neuronal firing conditions in non-human mammals. Here, the authors show these conditions are present in humans, potentially facilitating spike-timing-dependent plasticity.
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43
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Findlay G, Tononi G, Cirelli C. The evolving view of replay and its functions in wake and sleep. ACTA ACUST UNITED AC 2021; 1:zpab002. [PMID: 33644760 PMCID: PMC7898724 DOI: 10.1093/sleepadvances/zpab002] [Citation(s) in RCA: 21] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/14/2020] [Revised: 01/20/2021] [Indexed: 12/28/2022]
Abstract
The term hippocampal replay originally referred to the temporally compressed reinstantiation, during rest, of sequential neural activity observed during prior active wake. Since its description in the 1990s, hippocampal replay has often been viewed as the key mechanism by which a memory trace is repeatedly rehearsed at high speeds during sleep and gradually transferred to neocortical circuits. However, the methods used to measure the occurrence of replay remain debated, and it is now clear that the underlying neural events are considerably more complicated than the traditional narratives had suggested. “Replay-like” activity happens during wake, can play out in reverse order, may represent trajectories never taken by the animal, and may have additional functions beyond memory consolidation, from learning values and solving the problem of credit assignment to decision-making and planning. Still, we know little about the role of replay in cognition, and to what extent it differs between wake and sleep. This may soon change, however, because decades-long efforts to explain replay in terms of reinforcement learning (RL) have started to yield testable predictions and possible explanations for a diverse set of observations. Here, we (1) survey the diverse features of replay, focusing especially on the latest findings; (2) discuss recent attempts at unifying disparate experimental results and putatively different cognitive functions under the banner of RL; (3) discuss methodological issues and theoretical biases that impede progress or may warrant a partial revaluation of the current literature, and finally; (4) highlight areas of considerable uncertainty and promising avenues of inquiry.
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Affiliation(s)
- Graham Findlay
- Department of Psychiatry, University of Wisconsin-Madison, Madison, WI, USA.,Neuroscience Training Program, University of Wisconsin-Madison, Madison, WI, USA
| | - Giulio Tononi
- Department of Psychiatry, University of Wisconsin-Madison, Madison, WI, USA
| | - Chiara Cirelli
- Department of Psychiatry, University of Wisconsin-Madison, Madison, WI, USA
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44
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Lo EBL, Laferriere LJC, Stewart MR, Milanovic M, Kinney M, Bowie CR, Dringenberg HC. Does Napping Enhance the Consolidation of Clinically Relevant Information? A Comparison of Individuals with Low and Elevated Depressive Symptoms. Nat Sci Sleep 2021; 13:141-152. [PMID: 33603524 PMCID: PMC7882434 DOI: 10.2147/nss.s297872] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/17/2020] [Accepted: 01/19/2021] [Indexed: 11/23/2022] Open
Abstract
PURPOSE Sleep, both overnight and daytime naps, can facilitate the consolidation of declarative memories in healthy humans. However, it is unclear whether such beneficial effects of sleep occur in special populations, such as individuals with elevated neuropsychiatric symptoms, and if they apply to clinically relevant material that may have personal significance to those populations. METHODS We examined memory retention over a 60-minute interval of wakefulness or nap opportunity in participants with low or elevated scores (≤13 and ≥21, respectively) on the Beck Depression Inventory-II (BDI-II). Memory for depression-related information was assessed by (a) free-recall of a video depicting a personal experience narrative of the impact of depression on cognition and workplace performance; and (b) a paired-associates task linking depression-related cognitive symptoms to appropriate coping strategies. RESULTS The results showed no overall difference in recall between the nap and waking condition. However, across the full sample of participants, there were significant positive correlations between total sleep time and paired associates recall, and slow wave sleep (SWS) percentage and story free recall performance. Unexpectedly, participants with elevated BDI-II scores exhibited better free-recall performance compared to those with low scores. CONCLUSION These results suggest that sleep, specifically SWS, may stabilize memories for clinically relevant information in populations with low and elevated depressive symptoms. The superior recall in participants with elevated-BDI scores may be related to the personal significance and stronger encoding of depression-related information. These observations raise the possibility that mnemonic deficits in depressed patients may be, at least in part, related to the type of information used to assess memory performance.
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Affiliation(s)
- Edwyn B L Lo
- Department of Psychology, Queen's University, Kingston, Ontario, Canada
| | | | - Matthew R Stewart
- Department of Psychology, Queen's University, Kingston, Ontario, Canada
| | - Melissa Milanovic
- Department of Psychology, Queen's University, Kingston, Ontario, Canada
| | - Melinda Kinney
- Department of Psychology, Queen's University, Kingston, Ontario, Canada
| | - Christopher R Bowie
- Department of Psychology, Queen's University, Kingston, Ontario, Canada.,Centre for Neuroscience Studies, Queen's University, Kingston, Ontario, Canada
| | - Hans C Dringenberg
- Department of Psychology, Queen's University, Kingston, Ontario, Canada.,Centre for Neuroscience Studies, Queen's University, Kingston, Ontario, Canada
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45
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Higgins C, Liu Y, Vidaurre D, Kurth-Nelson Z, Dolan R, Behrens T, Woolrich M. Replay bursts in humans coincide with activation of the default mode and parietal alpha networks. Neuron 2020; 109:882-893.e7. [PMID: 33357412 PMCID: PMC7927915 DOI: 10.1016/j.neuron.2020.12.007] [Citation(s) in RCA: 70] [Impact Index Per Article: 14.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/03/2020] [Revised: 10/15/2020] [Accepted: 12/04/2020] [Indexed: 11/04/2022]
Abstract
Our brains at rest spontaneously replay recently acquired information, but how this process is orchestrated to avoid interference with ongoing cognition is an open question. Here we investigated whether replay coincided with spontaneous patterns of whole-brain activity. We found, in two separate datasets, that replay sequences were packaged into transient bursts occurring selectively during activation of the default mode network (DMN) and parietal alpha networks. These networks are believed to support inwardly oriented attention and inhibit bottom-up sensory processing and were characterized by widespread synchronized oscillations coupled to increases in high frequency power, mechanisms thought to coordinate information flow between disparate cortical areas. Our data reveal a tight correspondence between two widely studied phenomena in neural physiology and suggest that the DMN may coordinate replay bursts in a manner that minimizes interference with ongoing cognition.
Replay in humans coincides with activity in specific resting brain networks Clusters of heightened default mode and alpha activity are linked to replay bursts These networks are characterized by highly synchronized brain-wide oscillations High-frequency power bursts are uniquely linked to default mode network activation
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Affiliation(s)
- Cameron Higgins
- Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, UK.
| | - Yunzhe Liu
- Wellcome Trust Centre for Neuroimaging, University College London, London, UK; Max Planck University College London Centre for Computational Psychiatry and Ageing Research, University College London, London, UK
| | - Diego Vidaurre
- Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, UK; Center of Functionally Integrative Neuroscience, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
| | - Zeb Kurth-Nelson
- Max Planck University College London Centre for Computational Psychiatry and Ageing Research, University College London, London, UK; Deepmind, London, UK
| | - Ray Dolan
- Wellcome Trust Centre for Neuroimaging, University College London, London, UK; Max Planck University College London Centre for Computational Psychiatry and Ageing Research, University College London, London, UK
| | - Timothy Behrens
- Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, UK; Wellcome Trust Centre for Neuroimaging, University College London, London, UK
| | - Mark Woolrich
- Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, UK
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46
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Dudysová D, Janků K, Šmotek M, Saifutdinova E, Kopřivová J, Bušková J, Mander BA, Brunovský M, Zach P, Korčák J, Andrashko V, Viktorinová M, Tylš F, Bravermanová A, Froese T, Páleníček T, Horáček J. The Effects of Daytime Psilocybin Administration on Sleep: Implications for Antidepressant Action. Front Pharmacol 2020; 11:602590. [PMID: 33343372 PMCID: PMC7744693 DOI: 10.3389/fphar.2020.602590] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/03/2020] [Accepted: 11/13/2020] [Indexed: 12/02/2022] Open
Abstract
Serotonergic agonist psilocybin is a psychedelic with antidepressant potential. Sleep may interact with psilocybin’s antidepressant properties like other antidepressant drugs via induction of neuroplasticity. The main aim of the study was to evaluate the effect of psilocybin on sleep architecture on the night after psilocybin administration. Regarding the potential antidepressant properties, we hypothesized that psilocybin, similar to other classical antidepressants, would reduce rapid eye movement (REM) sleep and prolong REM sleep latency. Moreover, we also hypothesized that psilocybin would promote slow-wave activity (SWA) expression in the first sleep cycle, a marker of sleep-related neuroplasticity. Twenty healthy volunteers (10 women, age 28–53) underwent two drug administration sessions, psilocybin or placebo, in a randomized, double-blinded design. Changes in sleep macrostructure, SWA during the first sleep cycle, whole night EEG spectral power across frequencies in non-rapid eye movement (NREM) and REM sleep, and changes in subjective sleep measures were analyzed. The results revealed prolonged REM sleep latency after psilocybin administration and a trend toward a decrease in overall REM sleep duration. No changes in NREM sleep were observed. Psilocybin did not affect EEG power spectra in NREM or REM sleep when examined across the whole night. However, psilocybin suppressed SWA in the first sleep cycle. No evidence was found for sleep-related neuroplasticity, however, a different dosage, timing, effect on homeostatic regulation of sleep, or other mechanisms related to antidepressant effects may play a role. Overall, this study suggests that potential antidepressant properties of psilocybin might be related to changes in sleep.
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Affiliation(s)
- Daniela Dudysová
- National Institute of Mental Health, Klecany, Czechia.,Third Faculty of Medicine, Charles University, Prague, Czechia
| | - Karolina Janků
- National Institute of Mental Health, Klecany, Czechia.,Third Faculty of Medicine, Charles University, Prague, Czechia
| | - Michal Šmotek
- National Institute of Mental Health, Klecany, Czechia.,Third Faculty of Medicine, Charles University, Prague, Czechia
| | - Elizaveta Saifutdinova
- National Institute of Mental Health, Klecany, Czechia.,Czech Technical University in Prague, Prague, Czechia
| | - Jana Kopřivová
- National Institute of Mental Health, Klecany, Czechia.,Third Faculty of Medicine, Charles University, Prague, Czechia
| | - Jitka Bušková
- National Institute of Mental Health, Klecany, Czechia.,Third Faculty of Medicine, Charles University, Prague, Czechia
| | - Bryce Anthony Mander
- Department of Psychiatry and Human Behavior, School of Medicine, Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, CA, United States
| | - Martin Brunovský
- National Institute of Mental Health, Klecany, Czechia.,Third Faculty of Medicine, Charles University, Prague, Czechia
| | - Peter Zach
- National Institute of Mental Health, Klecany, Czechia
| | - Jakub Korčák
- National Institute of Mental Health, Klecany, Czechia
| | | | - Michaela Viktorinová
- National Institute of Mental Health, Klecany, Czechia.,Third Faculty of Medicine, Charles University, Prague, Czechia
| | - Filip Tylš
- National Institute of Mental Health, Klecany, Czechia.,Third Faculty of Medicine, Charles University, Prague, Czechia
| | - Anna Bravermanová
- National Institute of Mental Health, Klecany, Czechia.,First Faculty of Medicine, Charles University, Prague, Czechia
| | - Tom Froese
- Embodied Cognitive Science Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan
| | - Tomáš Páleníček
- National Institute of Mental Health, Klecany, Czechia.,Third Faculty of Medicine, Charles University, Prague, Czechia
| | - Jiří Horáček
- National Institute of Mental Health, Klecany, Czechia.,Third Faculty of Medicine, Charles University, Prague, Czechia
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47
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Dissanayaka T, Zoghi M, Farrell M, Egan G, Jaberzadeh S. The effects of a single-session cathodal transcranial pulsed current stimulation on corticospinal excitability: A randomized sham-controlled double-blinded study. Eur J Neurosci 2020; 52:4908-4922. [PMID: 33128480 DOI: 10.1111/ejn.14916] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/06/2019] [Revised: 06/16/2020] [Accepted: 07/11/2020] [Indexed: 12/17/2022]
Abstract
Transcranial pulsed current stimulation (tPCS) of the human motor cortex has received much attention in recent years. Although the effect of anodal tPCS with different frequencies has been investigated, the effect of cathodal tPCS (c-tPCS) has not been explored yet. Therefore, the aim of the present study was to investigate the effect of c-tPCS at 4 and 75 Hz frequencies on corticospinal excitability (CSE) and motor performance. In a randomized sham-controlled crossover design, fifteen healthy participants attended three experimental sessions and received either c-tPCS at 75 Hz, 4 Hz or sham with 1.5 mA for 15 min. Transcranial magnetic stimulation and grooved pegboard test were performed before, immediately after and 30 min after the completion of stimulation at rest. The findings indicate that c-tPCS at both 4 and 75 Hz significantly increased CSE compared to sham. Both c-tPCS at 75 and 4 Hz showed a significant increase in intracortical facilitation compared to sham, whereas the effect on short-interval intracortical inhibition was not significant. The c-tPCS at 4 Hz but not 75 Hz induced modulation of intracortical facilitation correlated with the CSE. Motor performance did not show any significant changes. These results suggest that, compared with sham stimulation, c-tPCS at both 4 and 75 Hz induces an increase in CSE.
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Affiliation(s)
- Thusharika Dissanayaka
- Non-invasive Brain Stimulation & Neuroplasticity Laboratory, Department of Physiotherapy, School of Primary and Allied Health Care, Faculty of Medicine, Nursing and Health Sciences, Monash University, Melbourne, Vic., Australia
| | - Maryam Zoghi
- Department of Rehabilitation, Nutrition and Sport, School of Allied health, La Trobe University, Bundoora, Melbourne, Vic., Australia
| | - Michael Farrell
- Monash Biomedical Imaging, Monash University, Melbourne, Vic., Australia.,Department of Medical Imaging and Radiation Sciences, Monash University, Clayton, Vic., Australia
| | - Gary Egan
- Monash Biomedical Imaging, Monash University, Melbourne, Vic., Australia
| | - Shapour Jaberzadeh
- Non-invasive Brain Stimulation & Neuroplasticity Laboratory, Department of Physiotherapy, School of Primary and Allied Health Care, Faculty of Medicine, Nursing and Health Sciences, Monash University, Melbourne, Vic., Australia
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48
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Mander BA. Local Sleep and Alzheimer's Disease Pathophysiology. Front Neurosci 2020; 14:525970. [PMID: 33071726 PMCID: PMC7538792 DOI: 10.3389/fnins.2020.525970] [Citation(s) in RCA: 54] [Impact Index Per Article: 10.8] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/11/2020] [Accepted: 09/01/2020] [Indexed: 12/11/2022] Open
Abstract
Even prior to the onset of the prodromal stages of Alzheimer's disease (AD), a constellation of sleep disturbances are apparent. A series of epidemiological studies indicate that multiple forms of these sleep disturbances are associated with increased risk for developing mild cognitive impairment (MCI) and AD, even triggering disease onset at an earlier age. Through the combination of causal manipulation studies in humans and rodents, as well as targeted examination of sleep disturbance with respect to AD biomarkers, mechanisms linking sleep disturbance to AD are beginning to emerge. In this review, we explore recent evidence linking local deficits in brain oscillatory function during sleep with local AD pathological burden and circuit-level dysfunction and degeneration. In short, three deficits in the local expression of sleep oscillations have been identified in relation to AD pathophysiology: (1) frequency-specific frontal deficits in slow wave expression during non-rapid eye movement (NREM) sleep, (2) deficits in parietal sleep spindle expression, and (3) deficits in the quality of electroencephalographic (EEG) desynchrony characteristic of REM sleep. These deficits are noteworthy since they differ from that seen in normal aging, indicating the potential presence of an abnormal aging process. How each of these are associated with β-amyloid (Aβ) and tau pathology, as well as neurodegeneration of circuits sensitive to AD pathophysiology, are examined in the present review, with a focus on the role of dysfunction within fronto-hippocampal and subcortical sleep-wake circuits. It is hypothesized that each of these local sleep deficits arise from distinct network-specific dysfunctions driven by regionally-specific accumulation of AD pathologies, as well as their associated neurodegeneration. Overall, the evolution of these local sleep deficits offer unique windows into the circuit-specific progression of distinct AD pathophysiological processes prior to AD onset, as well as their impact on brain function. This includes the potential erosion of sleep-dependent memory mechanisms, which may contribute to memory decline in AD. This review closes with a discussion of the remaining critical knowledge gaps and implications of this work for future mechanistic studies and studies implementing sleep-based treatment interventions.
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Affiliation(s)
- Bryce A. Mander
- Department of Psychiatry and Human Behavior, University of California, Irvine, Irvine, CA, United States
- Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, CA, United States
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49
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Paller KA, Creery JD, Schechtman E. Memory and Sleep: How Sleep Cognition Can Change the Waking Mind for the Better. Annu Rev Psychol 2020; 72:123-150. [PMID: 32946325 DOI: 10.1146/annurev-psych-010419-050815] [Citation(s) in RCA: 67] [Impact Index Per Article: 13.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/26/2022]
Abstract
The memories that we retain can serve many functions. They guide our future actions, form a scaffold for constructing the self, and continue to shape both the self and the way we perceive the world. Although most memories we acquire each day are forgotten, those integrated within the structure of multiple prior memories tend to endure. A rapidly growing body of research is steadily elucidating how the consolidation of memories depends on their reactivation during sleep. Processing memories during sleep not only helps counteract their weakening but also supports problem solving, creativity, and emotional regulation. Yet, sleep-based processing might become maladaptive, such as when worries are excessively revisited. Advances in research on memory and sleep can thus shed light on how this processing influences our waking life, which can further inspire the development of novel strategies for decreasing detrimental rumination-like activity during sleep and for promoting beneficial sleep cognition.
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Affiliation(s)
- Ken A Paller
- Department of Psychology and Cognitive Neuroscience Program, Northwestern University, Evanston, Illinois 60208, USA; , ,
| | - Jessica D Creery
- Department of Psychology and Cognitive Neuroscience Program, Northwestern University, Evanston, Illinois 60208, USA; , ,
| | - Eitan Schechtman
- Department of Psychology and Cognitive Neuroscience Program, Northwestern University, Evanston, Illinois 60208, USA; , ,
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50
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Barron HC, Auksztulewicz R, Friston K. Prediction and memory: A predictive coding account. Prog Neurobiol 2020; 192:101821. [PMID: 32446883 PMCID: PMC7305946 DOI: 10.1016/j.pneurobio.2020.101821] [Citation(s) in RCA: 96] [Impact Index Per Article: 19.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/27/2019] [Revised: 02/26/2020] [Accepted: 04/29/2020] [Indexed: 01/27/2023]
Abstract
The hippocampus is crucial for episodic memory, but it is also involved in online prediction. Evidence suggests that a unitary hippocampal code underlies both episodic memory and predictive processing, yet within a predictive coding framework the hippocampal-neocortical interactions that accompany these two phenomena are distinct and opposing. Namely, during episodic recall, the hippocampus is thought to exert an excitatory influence on the neocortex, to reinstate activity patterns across cortical circuits. This contrasts with empirical and theoretical work on predictive processing, where descending predictions suppress prediction errors to 'explain away' ascending inputs via cortical inhibition. In this hypothesis piece, we attempt to dissolve this previously overlooked dialectic. We consider how the hippocampus may facilitate both prediction and memory, respectively, by inhibiting neocortical prediction errors or increasing their gain. We propose that these distinct processing modes depend upon the neuromodulatory gain (or precision) ascribed to prediction error units. Within this framework, memory recall is cast as arising from fictive prediction errors that furnish training signals to optimise generative models of the world, in the absence of sensory data.
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Affiliation(s)
- Helen C Barron
- Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK; Wellcome Centre for Integrative Neuroimaging, University of Oxford, FMRIB, John Radcliffe Hospital, Oxford, OX3 9DU, UK.
| | - Ryszard Auksztulewicz
- Max Planck Institute for Empirical Aesthetics, Frankfurt Am Main, 60322, Germany; Department of Biomedical Sciences, City University of Hong Kong, Hong Kong
| | - Karl Friston
- The Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London, WC1N 3BG, UK
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