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Magielse N, Heuer K, Toro R, Schutter DJLG, Valk SL. A Comparative Perspective on the Cerebello-Cerebral System and Its Link to Cognition. CEREBELLUM (LONDON, ENGLAND) 2023; 22:1293-1307. [PMID: 36417091 PMCID: PMC10657313 DOI: 10.1007/s12311-022-01495-0] [Citation(s) in RCA: 10] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Accepted: 11/11/2022] [Indexed: 11/24/2022]
Abstract
The longstanding idea that the cerebral cortex is the main neural correlate of human cognition can be elaborated by comparative analyses along the vertebrate phylogenetic tree that support the view that the cerebello-cerebral system is suited to support non-motor functions more generally. In humans, diverse accounts have illustrated cerebellar involvement in cognitive functions. Although the neocortex, and its transmodal association cortices such as the prefrontal cortex, have become disproportionately large over primate evolution specifically, human neocortical volume does not appear to be exceptional relative to the variability within primates. Rather, several lines of evidence indicate that the exceptional volumetric increase of the lateral cerebellum in conjunction with its connectivity with the cerebral cortical system may be linked to non-motor functions and mental operation in primates. This idea is supported by diverging cerebello-cerebral adaptations that potentially coevolve with cognitive abilities across other vertebrates such as dolphins, parrots, and elephants. Modular adaptations upon the vertebrate cerebello-cerebral system may thus help better understand the neuroevolutionary trajectory of the primate brain and its relation to cognition in humans. Lateral cerebellar lobules crura I-II and their reciprocal connections to the cerebral cortical association areas appear to have substantially expanded in great apes, and humans. This, along with the notable increase in the ventral portions of the dentate nucleus and a shift to increased relative prefrontal-cerebellar connectivity, suggests that modular cerebellar adaptations support cognitive functions in humans. In sum, we show how comparative neuroscience provides new avenues to broaden our understanding of cerebellar and cerebello-cerebral functions in the context of cognition.
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Affiliation(s)
- Neville Magielse
- Institute of Neuroscience and Medicine (INM-7: Brain and Behaviour), Research Center Jülich, Jülich, Germany
- Otto Hahn Cognitive Neurogenetics Group, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
- Institute of Systems Neuroscience, Heinrich Heine University, Düsseldorf, Germany
| | - Katja Heuer
- Institute Pasteur, Unité de Neuroanatomie Appliquée et Théorique, Université Paris Cité, Paris, France
- Department of Neuropsychology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
| | - Roberto Toro
- Institute Pasteur, Unité de Neuroanatomie Appliquée et Théorique, Université Paris Cité, Paris, France
| | - Dennis J L G Schutter
- Experimental Psychology, Helmholtz Institute, Utrecht University, Utrecht, The Netherlands
| | - Sofie L Valk
- Institute of Neuroscience and Medicine (INM-7: Brain and Behaviour), Research Center Jülich, Jülich, Germany.
- Otto Hahn Cognitive Neurogenetics Group, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.
- Institute of Systems Neuroscience, Heinrich Heine University, Düsseldorf, Germany.
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Cordoni G, Ciarcelluti G, Pasqualotto A, Perri A, Bissiato V, Norscia I. Is it for real? Structural differences between play and real fighting in adult chimpanzees (Pan troglodytes). Am J Primatol 2023; 85:e23537. [PMID: 37461284 DOI: 10.1002/ajp.23537] [Citation(s) in RCA: 6] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/16/2022] [Revised: 06/23/2023] [Accepted: 07/08/2023] [Indexed: 08/15/2023]
Abstract
In primates, as well as in other mammals, play fighting (PF) is a complex form of playful activity that is structurally similar to real fighting (RF) and may also be used in a competitive way. Here, we verify the structural key differences that can distinguish PF from RF in adult chimpanzees (Pan troglodytes). We collected 962 h of video recording on 30 adult individuals belonging to four chimpanzee groups (Mona Chimpanzee Sanctuary, Spain; La Vallée des Singes and ZooParc de Beauval, France). We applied different indices-two of which were borrowed from the ecological measures of biodiversity-to test for structural differences between PF (345 sessions) and RF (461 sessions) in the levels of behavior repetition (Repeatability of Same Behavior Index, RSBI), distribution uniformity (Pielou Index, J), variability (Shannon Index, H') and, symmetry (i.e., reciprocal exchange of offensive/defensive behaviors; Asymmetry Index, AI). Moreover, we compared the session duration between PF and RF. We found that duration and RSBI were higher in PF than RF while AI was higher in RF than PF. No difference was found between J and H'. Interestingly, both females and males maintained similar ranking positions (determined via Normalized David's scores) in RF and PF. Our study indicates that session duration, behavior repetition, and symmetry can be distinctive structural key features of PF whereas dominance role-reversal, behavior variability, and distribution uniformity were not. PF in adult chimpanzees may have elements of serious contexts (e.g., absence of role-reversal as in RF) which is in line with the view that play is a blended, multifunctional behavior deriving from the re-combination of different behavioral systems. Our findings highlight the need to investigate play structure and manifestation in a nuanced way to better understand the actual motivation that underlies what appears to be play.
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Affiliation(s)
- Giada Cordoni
- Department of Life Sciences and Systems Biology, University of Torino, Turin, Italy
| | - Giulia Ciarcelluti
- Department of Life Sciences and Systems Biology, University of Torino, Turin, Italy
| | - Altea Pasqualotto
- Department of Life Sciences and Systems Biology, University of Torino, Turin, Italy
| | - Annarita Perri
- Department of Life Sciences and Systems Biology, University of Torino, Turin, Italy
| | - Veronica Bissiato
- Department of Life Sciences and Systems Biology, University of Torino, Turin, Italy
| | - Ivan Norscia
- Department of Life Sciences and Systems Biology, University of Torino, Turin, Italy
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Elbeltagi R, Al-Beltagi M, Saeed NK, Alhawamdeh R. Play therapy in children with autism: Its role, implications, and limitations. World J Clin Pediatr 2023; 12:1-22. [PMID: 36685315 PMCID: PMC9850869 DOI: 10.5409/wjcp.v12.i1.1] [Citation(s) in RCA: 6] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/27/2022] [Revised: 11/08/2022] [Accepted: 11/23/2022] [Indexed: 01/03/2023] Open
Abstract
Play is a pleasurable physical or mental activity that enhances the child's skills involving negotiation abilities, problem-solving, manual dexterity, sharing, decision-making, and working in a group. Play affects all the brain's areas, structures, and functions. Children with autism have adaptive behavior, adaptive response, and social interaction limitations. This review explores the different applications of play therapy in helping children with autism disorder. Play is usually significantly impaired in children with autism. Play therapy is mainly intended to help children to honor their unique mental abilities and developmental levels. The main aim of play therapy is to prevent or solve psychosocial difficulties and achieve optimal child-healthy growth and development. Play therapy helps children with autism to engage in play activities of their interest and choice to express themselves in the most comfortable ways. It changes their way of self-expression from unwanted behaviors to more non-injurious expressive behavior using toys or activities of their choice as their words. Play therapy also helps those children to experience feeling out various interaction styles. Every child with autism is unique and responds differently. Therefore, different types of intervention, like play therapy, could fit the differences in children with autism. Proper evaluation of the child is mandatory to evaluate which type fits the child more than the others. This narrative review revised the different types of play therapy that could fit children with autism in an evidence-based way. Despite weak evidence, play therapy still has potential benefits for patients and their families.
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Affiliation(s)
- Reem Elbeltagi
- Department of Medicine, Royal College of Surgeons in Ireland - Bahrain, Busaiteen 15503, Bahrain
| | - Mohammed Al-Beltagi
- Department of Pediatrics, Faculty of Medicine, Tanta University, Tanta 31527, Egypt
- Department of Pediatrics, University Medical Center, King Abdulla Medical City, Dr. Sulaiman Al-Habib Medical Group, Manama 26671, Bahrain
| | - Nermin Kamal Saeed
- Pathology Department, Salmaniya Medical Complex, Manama 12, Bahrain
- Pathology Department, Irish Royal College of Surgeon, Bahrain, Busaiteen 15503, Bahrain
| | - Rawan Alhawamdeh
- Pediatrics Research and Development Department, Genomics Creativity and Play Center, Manama 0000, Bahrain
- School of Continuing Education, Masters in Psychology, Harvard University, Cambridge, MA 02138, United States
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Bittar TP, Labonté B. Functional Contribution of the Medial Prefrontal Circuitry in Major Depressive Disorder and Stress-Induced Depressive-Like Behaviors. Front Behav Neurosci 2021; 15:699592. [PMID: 34234655 PMCID: PMC8257081 DOI: 10.3389/fnbeh.2021.699592] [Citation(s) in RCA: 44] [Impact Index Per Article: 11.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/23/2021] [Accepted: 05/20/2021] [Indexed: 12/13/2022] Open
Abstract
Despite decades of research on the neurobiology of major depressive disorder (MDD), the mechanisms underlying its expression remain unknown. The medial prefrontal cortex (mPFC), a hub region involved in emotional processing and stress response elaboration, is highly impacted in MDD patients and animal models of chronic stress. Recent advances showed alterations in the morphology and activity of mPFC neurons along with profound changes in their transcriptional programs. Studies at the circuitry level highlighted the relevance of deciphering the contributions of the distinct prefrontal circuits in the elaboration of adapted and maladapted behavioral responses in the context of chronic stress. Interestingly, MDD presents a sexual dimorphism, a feature recognized in the molecular field but understudied on the circuit level. This review examines the recent literature and summarizes the contribution of the mPFC circuitry in the expression of MDD in males and females along with the morphological and functional alterations that change the activity of these neuronal circuits in human MDD and animal models of depressive-like behaviors.
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Affiliation(s)
- Thibault P. Bittar
- CERVO Brain Research Centre, Québec, QC, Canada
- Department of Psychiatry and Neuroscience, Faculty of Medicine, Université Laval, Québec, QC, Canada
| | - Benoit Labonté
- CERVO Brain Research Centre, Québec, QC, Canada
- Department of Psychiatry and Neuroscience, Faculty of Medicine, Université Laval, Québec, QC, Canada
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Cabrera-Álvarez MJ, Clayton NS. Neural Processes Underlying Tool Use in Humans, Macaques, and Corvids. Front Psychol 2020; 11:560669. [PMID: 33117228 PMCID: PMC7561402 DOI: 10.3389/fpsyg.2020.560669] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/09/2020] [Accepted: 08/31/2020] [Indexed: 11/25/2022] Open
Abstract
It was thought that tool use in animals is an adaptive specialization. Recent studies, however, have shown that some non-tool-users, such as rooks and jays, can use and manufacture tools in laboratory settings. Despite the abundant evidence of tool use in corvids, little is known about the neural mechanisms underlying tool use in this family of birds. This review summarizes the current knowledge on the neural processes underlying tool use in humans, macaques and corvids. We suggest a possible neural network for tool use in macaques and hope this might inspire research to discover a similar brain network in corvids. We hope to establish a framework to elucidate the neural mechanisms that supported the convergent evolution of tool use in birds and mammals.
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Ash H, Ziegler TE, Colman RJ. Early learning in the common marmoset (Callithrix jacchus): Behavior in the family group is related to preadolescent cognitive performance. Am J Primatol 2020; 82:e23159. [PMID: 32515834 PMCID: PMC7440670 DOI: 10.1002/ajp.23159] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/17/2019] [Revised: 05/15/2020] [Accepted: 05/24/2020] [Indexed: 12/16/2022]
Abstract
Early environment can have a major impact on development, with family life known to play an important role. Longitudinal studies can therefore help increase our understanding of variance in cognitive abilities in young animals, as well as over time. We followed 22 marmosets (11 male and 11 female) from infancy through to early adolescence. At 3 months old, the marmosets were trained to reliably touch a rewarded stimulus. At 5 months, behavior was observed within the natal group. At 9 months, the marmosets were given a visual discrimination task to assess learning ability. Mann-Whitney U tests found no sex or family size differences in number of errors at 3 or 9 months. While no significant relationships were found between behavior in the family and learning at 3 months, significant negative correlations were found between duration spent in locomotion and learning errors (p = .05), as well as between frequency of calm vocalizations and learning errors (p = .001) at 9 months. A U-shape curve was found between amount of social play and learning at 9 months. Positive family interactions, including moderate amounts of play, as well as calm individual behavior, may therefore be important in learning. This study sheds light on cognitive development in much younger marmosets than previously studied, and helps increase understanding of how individual differences in learning may arise.
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Affiliation(s)
- Hayley Ash
- Wisconsin National Primate Research Center, University of Wisconsin, Madison, WI, USA
| | - Toni E. Ziegler
- Wisconsin National Primate Research Center, University of Wisconsin, Madison, WI, USA
| | - Ricki J. Colman
- Wisconsin National Primate Research Center, University of Wisconsin, Madison, WI, USA
- Department of Cell and Regenerative Biology, University of Wisconsin School of Medicine and Public Health, Wisconsin Institutes for Medical Research, 1111 Highland Avenue, Madison, WI, USA
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Powell LE, Barton RA, Street SE. Maternal investment, life histories and the evolution of brain structure in primates. Proc Biol Sci 2019; 286:20191608. [PMID: 31530145 PMCID: PMC6784728 DOI: 10.1098/rspb.2019.1608] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/08/2019] [Accepted: 08/15/2019] [Indexed: 12/16/2022] Open
Abstract
Life history is a robust correlate of relative brain size: larger-brained mammals and birds have slower life histories and longer lifespans than smaller-brained species. The cognitive buffer hypothesis (CBH) proposes an adaptive explanation for this relationship: large brains may permit greater behavioural flexibility and thereby buffer the animal from unpredictable environmental challenges, allowing for reduced mortality and increased lifespan. By contrast, the developmental costs hypothesis (DCH) suggests that life-history correlates of brain size reflect the extension of maturational processes needed to accommodate the evolution of large brains, predicting correlations with pre-adult life-history phases. Here, we test novel predictions of the hypotheses in primates applied to the neocortex and cerebellum, two major brain structures with distinct developmental trajectories. While neocortical growth is allocated primarily to pre-natal development, the cerebellum exhibits relatively substantial post-natal growth. Consistent with the DCH, neocortical expansion is related primarily to extended gestation while cerebellar expansion to extended post-natal development, particularly the juvenile period. Contrary to the CBH, adult lifespan explains relatively little variance in the whole brain or neocortex volume once pre-adult life-history phases are accounted for. Only the cerebellum shows a relationship with lifespan after accounting for developmental periods. Our results substantiate and elaborate on the role of maternal investment and offspring development in brain evolution, suggest that brain components can evolve partly independently through modifications of distinct developmental phases, and imply that environmental input during post-natal maturation may be particularly crucial for the development of cerebellar function. They also suggest that relatively extended post-natal maturation times provide a developmental mechanism for the marked expansion of the cerebellum in the apes.
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Affiliation(s)
- Lauren E. Powell
- Evolutionary Anthropology Research Group, Department of Anthropology, Durham University, South Road, Durham DH1 3LE, UK
| | | | - Sally E. Street
- Evolutionary Anthropology Research Group, Department of Anthropology, Durham University, South Road, Durham DH1 3LE, UK
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Miquel M, Nicola SM, Gil-Miravet I, Guarque-Chabrera J, Sanchez-Hernandez A. A Working Hypothesis for the Role of the Cerebellum in Impulsivity and Compulsivity. Front Behav Neurosci 2019; 13:99. [PMID: 31133834 PMCID: PMC6513968 DOI: 10.3389/fnbeh.2019.00099] [Citation(s) in RCA: 61] [Impact Index Per Article: 10.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/26/2019] [Accepted: 04/23/2019] [Indexed: 12/27/2022] Open
Abstract
Growing evidence associates cerebellar abnormalities with several neuropsychiatric disorders in which compulsive symptomatology and impulsivity are part of the disease pattern. Symptomatology of autism, addiction, obsessive-compulsive (OCD), and attention deficit/hyperactivity (ADHD) disorders transcends the sphere of motor dysfunction and essentially entails integrative processes under control of prefrontal-thalamic-cerebellar loops. Patients with brain lesions affecting the cortico-striatum thalamic circuitry and the cerebellum indeed exhibit compulsive symptoms. Specifically, lesions of the posterior cerebellar vermis cause affective dysregulation and deficits in executive function. These deficits may be due to impairment of one of the main functions of the cerebellum, implementation of forward internal models of the environment. Actions that are independent of internal models may not be guided by predictive relationships or a mental representation of the goal. In this review article, we explain how this deficit might affect executive functions. Additionally, regionalized cerebellar lesions have been demonstrated to impair other brain functions such as the emergence of habits and behavioral inhibition, which are also altered in compulsive disorders. Similar to the infralimbic cortex, clinical studies and research in animal models suggest that the cerebellum is not required for learning goal-directed behaviors, but it is critical for habit formation. Despite this accumulating data, the role of the cerebellum in compulsive symptomatology and impulsivity is still a matter of discussion. Overall, findings point to a modulatory function of the cerebellum in terminating or initiating actions through regulation of the prefrontal cortices. Specifically, the cerebellum may be crucial for restraining ongoing actions when environmental conditions change by adjusting prefrontal activity in response to the new external and internal stimuli, thereby promoting flexible behavioral control. We elaborate on this explanatory framework and propose a working hypothesis for the involvement of the cerebellum in compulsive and impulsive endophenotypes.
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Affiliation(s)
- Marta Miquel
- Área de Psicobiología, School of Health Science, Universitat Jaume I, Castellón de la Plana, Spain
| | - Saleem M Nicola
- Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, NY, United States.,Department of Psychiatry and Behavioral Sciences, Albert Einstein College of Medicine, Bronx, NY, United States
| | - Isis Gil-Miravet
- Área de Psicobiología, School of Health Science, Universitat Jaume I, Castellón de la Plana, Spain
| | - Julian Guarque-Chabrera
- Área de Psicobiología, School of Health Science, Universitat Jaume I, Castellón de la Plana, Spain
| | - Aitor Sanchez-Hernandez
- Área de Psicobiología, School of Health Science, Universitat Jaume I, Castellón de la Plana, Spain
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Weele CMV, Siciliano CA, Tye KM. Dopamine tunes prefrontal outputs to orchestrate aversive processing. Brain Res 2018; 1713:16-31. [PMID: 30513287 DOI: 10.1016/j.brainres.2018.11.044] [Citation(s) in RCA: 56] [Impact Index Per Article: 8.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/27/2018] [Revised: 11/25/2018] [Accepted: 11/30/2018] [Indexed: 01/06/2023]
Abstract
Decades of research suggest that the mesocortical dopamine system exerts powerful control over mPFC physiology and function. Indeed, dopamine signaling in the medial prefrontal cortex (mPFC) is implicated in a vast array of processes, including working memory, stimulus discrimination, stress responses, and emotional and behavioral control. Consequently, even slight perturbations within this delicate system result in profound disruptions of mPFC-mediated processes. Many neuropsychiatric disorders are associated with dysregulation of mesocortical dopamine, including schizophrenia, depression, attention deficit hyperactivity disorder, post-traumatic stress disorder, among others. Here, we review the anatomy and functions of the mesocortical dopamine system. In contrast to the canonical role of striatal dopamine in reward-related functions, recent work has revealed that mesocortical dopamine fine-tunes distinct efferent projection populations in a manner that biases subsequent behavior towards responding to stimuli associated with potentially aversive outcomes. We propose a framework wherein dopamine can serve as a signal for switching mPFC states by orchestrating how information is routed to the rest of the brain.
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Affiliation(s)
- Caitlin M Vander Weele
- The Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA
| | - Cody A Siciliano
- The Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA
| | - Kay M Tye
- The Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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Parrots have evolved a primate-like telencephalic-midbrain-cerebellar circuit. Sci Rep 2018; 8:9960. [PMID: 29967361 PMCID: PMC6028647 DOI: 10.1038/s41598-018-28301-4] [Citation(s) in RCA: 35] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/26/2017] [Accepted: 06/20/2018] [Indexed: 01/13/2023] Open
Abstract
It is widely accepted that parrots show remarkable cognitive abilities. In mammals, the evolution of complex cognitive abilities is associated with increases in the size of the telencephalon and cerebellum as well as the pontine nuclei, which connect these two regions. Parrots have relatively large telencephalons that rival those of primates, but whether there are also evolutionary changes in their telencephalon-cerebellar relay nuclei is unknown. Like mammals, birds have two brainstem pontine nuclei that project to the cerebellum and receive projections from the telencephalon. Unlike mammals, birds also have a pretectal nucleus that connects the telencephalon with the cerebellum: the medial spiriform nucleus (SpM). We found that SpM, but not the pontine nuclei, is greatly enlarged in parrots and its relative size significantly correlated with the relative size of the telencephalon across all birds. This suggests that the telencephalon-SpM-cerebellar pathway of birds may play an analogous role to cortico-ponto-cerebellar pathways of mammals in controlling fine motor skills and complex cognitive processes. We conclude that SpM is key to understanding the role of telencephalon-cerebellar pathways in the evolution of complex cognitive abilities in birds.
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