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      Abnormalities of intrinsic brain activity in essential tremor: A meta‐analysis of resting‐state functional imaging

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          Abstract

          Neuroimaging studies using a variety of techniques have demonstrated abnormal patterns of spontaneous brain activity in patients with essential tremor (ET). However, the findings are variable and inconsistent, hindering understanding of underlying neuropathology. We conducted a meta‐analysis of whole‐brain resting‐state functional neuroimaging studies in ET compared to healthy controls (HC), using anisotropic effect‐size seed‐based d mapping, to identify the most consistent brain activity alterations and their relation to clinical features. After systematic literature search, we included 13 studies reporting 14 comparisons, describing 286 ET patients and 254 HC. Subgroup analyses were conducted considering medication status, head tremor status, and methodological factors. Brain activity in ET is altered not only in the cerebellum and cerebral motor cortex, but also in nonmotor cortical regions including prefrontal cortex and insula. Most of the results remained unchanged in subgroup analyses of patients with head tremor, medication‐naive patients, studies with statistical threshold correction, and the large subgroup of studies using functional magnetic resonance imaging. These findings not only show consistent and robust abnormalities in specific brain regions but also provide new information on the biology of patient heterogeneity, and thus help to elucidate the pathophysiology of ET.

          Abstract

          Neuroimaging studies using a variety of techniques have demonstrated abnormal patterns of spontaneous brain activity in patients with essential tremor (ET). However, the findings are variable and inconsistent, hindering understanding of underlying neuropathology. We conducted a meta‐analysis of whole‐brain resting‐state functional neuroimaging studies in ET compared to healthy controls, brain activity in ET is altered not only in the cerebellum and cerebral motor cortex, but also in non‐motor cortical regions including prefrontal cortex and insula.

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          Most cited references72

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          Correspondence of the brain's functional architecture during activation and rest.

          Neural connections, providing the substrate for functional networks, exist whether or not they are functionally active at any given moment. However, it is not known to what extent brain regions are continuously interacting when the brain is "at rest." In this work, we identify the major explicit activation networks by carrying out an image-based activation network analysis of thousands of separate activation maps derived from the BrainMap database of functional imaging studies, involving nearly 30,000 human subjects. Independently, we extract the major covarying networks in the resting brain, as imaged with functional magnetic resonance imaging in 36 subjects at rest. The sets of major brain networks, and their decompositions into subnetworks, show close correspondence between the independent analyses of resting and activation brain dynamics. We conclude that the full repertoire of functional networks utilized by the brain in action is continuously and dynamically "active" even when at "rest."
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            Searching for a baseline: functional imaging and the resting human brain.

            Functional brain imaging in humans has revealed task-specific increases in brain activity that are associated with various mental activities. In the same studies, mysterious, task-independent decreases have also frequently been encountered, especially when the tasks of interest have been compared with a passive state, such as simple fixation or eyes closed. These decreases have raised the possibility that there might be a baseline or resting state of brain function involving a specific set of mental operations. We explore this possibility, including the manner in which we might define a baseline and the implications of such a baseline for our understanding of brain function.
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              Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing.

              Patients with cerebellar damage often present with the cerebellar motor syndrome of dysmetria, dysarthria and ataxia, yet cerebellar lesions can also result in the cerebellar cognitive affective syndrome (CCAS), including executive, visual spatial, and linguistic impairments, and affective dysregulation. We have hypothesized that there is topographic organization in the human cerebellum such that the anterior lobe and lobule VIII contain the representation of the sensorimotor cerebellum; lobules VI and VII of the posterior lobe comprise the cognitive cerebellum; and the posterior vermis is the anatomical substrate of the limbic cerebellum. Here we analyze anatomical, functional neuroimaging, and clinical data to test this hypothesis. We find converging lines of evidence supporting regional organization of motor, cognitive, and limbic behaviors in the cerebellum. The cerebellar motor syndrome results when lesions involve the anterior lobe and parts of lobule VI, interrupting cerebellar communication with cerebral and spinal motor systems. Cognitive impairments occur when posterior lobe lesions affect lobules VI and VII (including Crus I, Crus II, and lobule VIIB), disrupting cerebellar modulation of cognitive loops with cerebral association cortices. Neuropsychiatric disorders manifest when vermis lesions deprive cerebro-cerebellar-limbic loops of cerebellar input. We consider this functional topography to be a consequence of the differential arrangement of connections of the cerebellum with the spinal cord, brainstem, and cerebral hemispheres, reflecting cerebellar incorporation into the distributed neural circuits subserving movement, cognition, and emotion. These observations provide testable hypotheses for future investigations. Copyright (c) 2009 Elsevier Srl. All rights reserved.
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                Author and article information

                Contributors
                qiyonggong@hmrrc.org.cn
                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
                26 March 2021
                July 2021
                : 42
                : 10 ( doiID: 10.1002/hbm.v42.10 )
                : 3156-3167
                Affiliations
                [ 1 ] Huaxi MR Research Center (HMRRC), Department of Radiology West China Hospital of Sichuan University Chengdu Sichuan China
                [ 2 ] Research Unit of Psychoradiology Chinese Academy of Medical Sciences Chengdu China
                [ 3 ] Functional and Molecular Imaging Key Laboratory of Sichuan Province West China Hospital of Sichuan University Chengdu China
                [ 4 ] Department of Neurology West China Hospital of Sichuan University Chengdu Sichuan China
                [ 5 ] Department of Psychiatry and Behavioral Neuroscience University of Cincinnati Cincinnati Ohio USA
                [ 6 ] Liverpool Magnetic Resonance Imaging Centre (LiMRIC) and Institute of Life Course and Medical Sciences University of Liverpool Liverpool UK
                Author notes
                [*] [* ] Correspondence

                Qiyong Gong, Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, No. 37 Guo Xue Xiang, Chengdu 610041, China.

                Email: qiyonggong@ 123456hmrrc.org.cn

                Author information
                https://orcid.org/0000-0002-0373-6035
                https://orcid.org/0000-0002-5912-4871
                Article
                HBM25425
                10.1002/hbm.25425
                8193520
                33769638
                458858a8-4d04-4f3c-bf19-ea27cb3943a3
                © 2021 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

                History
                : 12 March 2021
                : 09 December 2020
                : 13 March 2021
                Page count
                Figures: 3, Tables: 3, Pages: 12, Words: 9559
                Funding
                Funded by: China Postdoctoral Science Foundation , open-funder-registry 10.13039/501100002858;
                Award ID: 2020M683317
                Funded by: National Natural Science Foundation of China , open-funder-registry 10.13039/501100001809;
                Award ID: 81621003
                Award ID: 81820108018
                Award ID: 82001800
                Funded by: Post‐Doctor Research Project, West China Hospital, Sichuan University
                Award ID: 2019HXBH104
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                July 2021
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.0.2 mode:remove_FC converted:11.06.2021

                Neurology
                essential tremor,functional magnetic resonance imaging,meta‐analysis,psychoradiology,resting‐state

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