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Functional Territories of Human Dentate Nucleus

View ORCID ProfileXavier Guell, Anila M D’Mello, Nicholas A Hubbard, Rachel R Romeo, John DE Gabrieli, Susan Whitfield-Gabrieli, Jeremy D Schmahmann, Sheeba Arnold Anteraper
doi: https://doi.org/10.1101/608620
Xavier Guell
McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United StatesLaboratory for Neuroanatomy and Cerebellar Neurobiology, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, United States
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  • ORCID record for Xavier Guell
  • For correspondence: xaviergp@mit.edu
Anila M D’Mello
McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
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Nicholas A Hubbard
McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
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Rachel R Romeo
McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United StatesBoston Children’s Hospital, Division of Developmental Medicine, Boston, United States
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John DE Gabrieli
McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
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Susan Whitfield-Gabrieli
McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United StatesDepartment of Psychology, Northeastern University, Boston, United States
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Jeremy D Schmahmann
Laboratory for Neuroanatomy and Cerebellar Neurobiology, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, United States
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Sheeba Arnold Anteraper
McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United StatesDepartment of Psychology, Northeastern University, Boston, United States
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ABSTRACT

Anatomical connections link the cerebellar cortex with multiple distinct sensory, motor, association, and paralimbic areas of the cerebrum. These projections allow a topographically precise cerebellar modulation of multiple domains of neurological function, and underscore the relevance of the cerebellum for the pathophysiology of numerous disorders in neurology and psychiatry. The majority of fibers that exit the cerebellar cortex synapse in the dentate nuclei (DN) before reaching extracerebellar structures such as cerebral cortex. Although the DN have a central position in the anatomy of the cerebello-cerebral circuits, the functional neuroanatomy of human DN remains largely unmapped. Neuroimaging research has redefined broad categories of functional division in the human brain showing that primary processing, attentional (task positive) processing, and default-mode (task negative) processing are three central poles of neural macro-scale functional organization. This new macro-scale understanding of the range and poles of brain function has revealed that a broad spectrum of human neural processing categories (primary, task positive, task negative) is represented not only in the cerebral cortex, but also in the thalamus, striatum, and cerebellar cortex. Whether functional organization in DN obeys a similar set of macroscale divisions, and whether DN are yet another compartment of representation of a broad spectrum of human neural processing categories, remains unknown. Here we show for the first time that human DN is optimally divided into three functional territories as indexed by high spatio-temporal resolution resting-state MRI in 60 healthy adolescents, and that these three distinct territories contribute uniquely to default-mode, salience-motor, and visual brain networks. These conclusions are supported by novel analytical strategies in human studies of DN organization, including 64-channel MRI imaging, data-driven methods, and replication in an independent sample. Our findings provide a systems neuroscience substrate for cerebellar output to influence multiple broad categories of neural control - namely default- mode, attentional, and multiple unimodal streams of information processing including motor and visual. They also provide a validated data-driven mapping of functions in human DN, crucial for the design of methodology and interpretation of results in future neuroimaging studies of brain function and dysfunction.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted April 13, 2019.
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Functional Territories of Human Dentate Nucleus
Xavier Guell, Anila M D’Mello, Nicholas A Hubbard, Rachel R Romeo, John DE Gabrieli, Susan Whitfield-Gabrieli, Jeremy D Schmahmann, Sheeba Arnold Anteraper
bioRxiv 608620; doi: https://doi.org/10.1101/608620
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Functional Territories of Human Dentate Nucleus
Xavier Guell, Anila M D’Mello, Nicholas A Hubbard, Rachel R Romeo, John DE Gabrieli, Susan Whitfield-Gabrieli, Jeremy D Schmahmann, Sheeba Arnold Anteraper
bioRxiv 608620; doi: https://doi.org/10.1101/608620

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