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      Sensorimotor, language, and working memory representation within the human cerebellum

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          Abstract

          The cerebellum is involved in a wide range of behaviours. A key organisational principle from animal studies is that somatotopically corresponding sensory input and motor output reside in the same cerebellar cortical areas. However, compelling evidence for a similar arrangement in humans and whether it extends to cognitive functions is lacking. To address this, we applied cerebellar optimised whole‐brain functional MRI in 20 healthy subjects. To assess spatial overlap within the sensorimotor and cognitive domains, we recorded activity to a sensory stimulus (vibrotactile) and a motor task; the Sternberg verbal working memory (VWM) task; and a verb generation paradigm. Consistent with animal data, sensory and motor activity overlapped with a somatotopic arrangement in ipsilateral areas of the anterior and posterior cerebellum. During the maintenance phase of the Sternberg task, a positive linear relationship between VWM load and activity was observed in right Lobule VI, extending into Crus I bilaterally. Articulatory movement gave rise to bilateral activity in medial Lobule VI. A conjunction of two independent language tasks localised activity during verb generation in right Lobule VI‐Crus I, which overlapped with activity during VWM. These results demonstrate spatial compartmentalisation of sensorimotor and cognitive function in the human cerebellum, with each area involved in more than one aspect of a given behaviour, consistent with an integrative function. Sensorimotor localisation was uniform across individuals, but the representation of cognitive tasks was more variable, highlighting the importance of individual scans for mapping higher order functions within the cerebellum.

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          Most cited references65

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          High-speed scanning in human memory.

          When subjects judge whether a test symbol is contained in a short memorized sequence of symbols, their mean reaction-time increases linearly with the length of the sequence. The linearity and slope of the function imply the existence of an internal serial-comparison process whose average rate is between 25 and 30 symbols per second.
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            Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity.

            The cerebellum processes information from functionally diverse regions of the cerebral cortex. Cerebellar input and output nuclei have connections with prefrontal, parietal, and sensory cortex as well as motor and premotor cortex. However, the topography of the connections between the cerebellar and cerebral cortices remains largely unmapped, as it is relatively unamenable to anatomical methods. We used resting-state functional magnetic resonance imaging to define subregions within the cerebellar cortex based on their functional connectivity with the cerebral cortex. We mapped resting-state functional connectivity voxel-wise across the cerebellar cortex, for cerebral-cortical masks covering prefrontal, motor, somatosensory, posterior parietal, visual, and auditory cortices. We found that the cerebellum can be divided into at least 2 zones: 1) a primary sensorimotor zone (Lobules V, VI, and VIII), which contains overlapping functional connectivity maps for domain-specific motor, somatosensory, visual, and auditory cortices; and 2) a supramodal zone (Lobules VIIa, Crus I, and II), which contains overlapping functional connectivity maps for prefrontal and posterior-parietal cortex. The cortical connectivity of the supramodal zone was driven by regions of frontal and parietal cortex which are not directly involved in sensory or motor processing, including dorsolateral prefrontal cortex and the frontal pole, and the inferior parietal lobule.
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              The Cerebellum: Adaptive Prediction for Movement and Cognition.

              Over the past 30 years, cumulative evidence has indicated that cerebellar function extends beyond sensorimotor control. This view has emerged from studies of neuroanatomy, neuroimaging, neuropsychology, and brain stimulation, with the results implicating the cerebellum in domains as diverse as attention, language, executive function, and social cognition. Although the literature provides sophisticated models of how the cerebellum helps refine movements, it remains unclear how the core mechanisms of these models can be applied when considering a broader conceptualization of cerebellar function. In light of recent multidisciplinary findings, we examine how two key concepts that have been suggested as general computational principles of cerebellar function- prediction and error-based learning- might be relevant in the operation of cognitive cerebro-cerebellar loops.
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                Author and article information

                Contributors
                jon.brooks@bristol.ac.uk
                Journal
                Hum Brain Mapp
                Hum Brain Mapp
                10.1002/(ISSN)1097-0193
                HBM
                Human Brain Mapping
                John Wiley & Sons, Inc. (Hoboken, USA )
                1065-9471
                1097-0193
                30 July 2019
                November 2019
                : 40
                : 16 ( doiID: 10.1002/hbm.v40.16 )
                : 4732-4747
                Affiliations
                [ 1 ] School of Physiology, Pharmacology and Neuroscience University of Bristol Bristol UK
                [ 2 ] Neurosurgery Department, Southmead Hospital North Bristol Trust Bristol UK
                [ 3 ] Neurosurgery Department, Bristol Royal Hospital for Children University Hospitals Bristol NHS Foundation Trust Bristol UK
                [ 4 ] Bristol Medical School University of Bristol Bristol UK
                [ 5 ] School of Psychological Science University of Bristol Bristol UK
                Author notes
                [*] [* ] Correspondence

                Dr Jonathan Brooks, School of Psychological Science, University of Bristol, Bristol, UK.

                Email: jon.brooks@ 123456bristol.ac.uk

                Author information
                https://orcid.org/0000-0003-3335-6209
                Article
                HBM24733
                10.1002/hbm.24733
                6865458
                31361075
                6fef53eb-b993-4d9d-b7c6-7955610add71
                © 2019 The Authors. Human Brain Mapping published by Wiley Periodicals, Inc.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 26 January 2019
                : 10 July 2019
                : 12 July 2019
                Page count
                Figures: 5, Tables: 0, Pages: 16, Words: 15364
                Funding
                Funded by: Action Medical Research , open-funder-registry 10.13039/501100000317;
                Award ID: SP4619
                Funded by: U.K. Medical Research Council , open-funder-registry 10.13039/501100000265;
                Award ID: G0700238
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                November 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.2 mode:remove_FC converted:15.11.2019

                Neurology
                cerebellum,fmri,language,sensorimotor,working memory
                Neurology
                cerebellum, fmri, language, sensorimotor, working memory

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