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      Explicit and Implicit Emotion Processing in the Cerebellum: A Meta-analysis and Systematic Review

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          Abstract

          The cerebellum’s role in affective processing is increasingly recognized in the literature, but remains poorly understood, despite abundant clinical evidence for affective disruptions following cerebellar damage. To improve the characterization of emotion processing and investigate how attention allocation impacts this processing, we conducted a meta-analysis on task activation foci using GingerALE software. Eighty human neuroimaging studies of emotion including 2761 participants identified through Web of Science and ProQuest databases were analyzed collectively and then divided into two categories based on the focus of attention during the task: explicit or implicit emotion processing. The results examining the explicit emotion tasks identified clusters within the posterior cerebellar hemispheres (bilateral lobule VI/Crus I/II), the vermis, and left lobule V/VI that were likely to be activated across studies, while implicit tasks activated clusters including bilateral lobules VI/Crus I/II, right Crus II/lobule VIII, anterior lobule VI, and lobules I-IV/V. A direct comparison between these categories revealed five overlapping clusters in right lobules VI/Crus I/Crus II and left lobules V/VI/Crus I of the cerebellum common to both the explicit and implicit task contrasts. There were also three clusters activated significantly more for explicit emotion tasks compared to implicit tasks (right lobule VI, left lobule VI/vermis), and one cluster activated more for implicit than explicit tasks (left lobule VI). These findings support previous studies indicating affective processing activates both the lateral hemispheric lobules and the vermis of the cerebellum. The common and distinct activation of posterior cerebellar regions by tasks with explicit and implicit attention demonstrates the supportive role of this structure in recognizing, appraising, and reacting to emotional stimuli.

          Supplementary Information

          The online version contains supplementary material available at 10.1007/s12311-022-01459-4.

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          Most cited references63

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          The brain basis of emotion: a meta-analytic review.

          Researchers have wondered how the brain creates emotions since the early days of psychological science. With a surge of studies in affective neuroscience in recent decades, scientists are poised to answer this question. In this target article, we present a meta-analytic summary of the neuroimaging literature on human emotion. We compare the locationist approach (i.e., the hypothesis that discrete emotion categories consistently and specifically correspond to distinct brain regions) with the psychological constructionist approach (i.e., the hypothesis that discrete emotion categories are constructed of more general brain networks not specific to those categories) to better understand the brain basis of emotion. We review both locationist and psychological constructionist hypotheses of brain-emotion correspondence and report meta-analytic findings bearing on these hypotheses. Overall, we found little evidence that discrete emotion categories can be consistently and specifically localized to distinct brain regions. Instead, we found evidence that is consistent with a psychological constructionist approach to the mind: A set of interacting brain regions commonly involved in basic psychological operations of both an emotional and non-emotional nature are active during emotion experience and perception across a range of discrete emotion categories.
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            The organization of the human cerebellum estimated by intrinsic functional connectivity.

            The cerebral cortex communicates with the cerebellum via polysynaptic circuits. Separate regions of the cerebellum are connected to distinct cerebral areas, forming a complex topography. In this study we explored the organization of cerebrocerebellar circuits in the human using resting-state functional connectivity MRI (fcMRI). Data from 1,000 subjects were registered using nonlinear deformation of the cerebellum in combination with surface-based alignment of the cerebral cortex. The foot, hand, and tongue representations were localized in subjects performing movements. fcMRI maps derived from seed regions placed in different parts of the motor body representation yielded the expected inverted map of somatomotor topography in the anterior lobe and the upright map in the posterior lobe. Next, we mapped the complete topography of the cerebellum by estimating the principal cerebral target for each point in the cerebellum in a discovery sample of 500 subjects and replicated the topography in 500 independent subjects. The majority of the human cerebellum maps to association areas. Quantitative analysis of 17 distinct cerebral networks revealed that the extent of the cerebellum dedicated to each network is proportional to the network's extent in the cerebrum with a few exceptions, including primary visual cortex, which is not represented in the cerebellum. Like somatomotor representations, cerebellar regions linked to association cortex have separate anterior and posterior representations that are oriented as mirror images of one another. The orderly topography of the representations suggests that the cerebellum possesses at least two large, homotopic maps of the full cerebrum and possibly a smaller third map.
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              Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space

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                Author and article information

                Contributors
                julie.peron@unige.ch
                Journal
                Cerebellum
                Cerebellum
                Cerebellum (London, England)
                Springer US (New York )
                1473-4222
                1473-4230
                23 August 2022
                23 August 2022
                2023
                : 22
                : 5
                : 852-864
                Affiliations
                [1 ]GRID grid.24434.35, ISNI 0000 0004 1937 0060, Cognitive and Affective Neuroscience Laboratory, Center for Brain, Biology, and Behavior, , University of Nebraska-Lincoln, ; Lincoln, NE USA
                [2 ]GRID grid.8591.5, ISNI 0000 0001 2322 4988, Clinical and Experimental Neuropsychology Laboratory, Department of Psychology, , University of Geneva, ; 40 bd du Pont d’Arve, 1205 Geneva, Switzerland
                [3 ]GRID grid.150338.c, ISNI 0000 0001 0721 9812, Neuropsychology Unit, Neurology Department, , University Hospitals of Geneva, ; Geneva, Switzerland
                Author information
                http://orcid.org/0000-0003-2985-3640
                Article
                1459
                10.1007/s12311-022-01459-4
                10485090
                35999332
                aafe88e4-ead0-4f87-b7f9-da451507aa93
                © The Author(s) 2022

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 9 August 2022
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001711, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung;
                Award ID: 105314_182221
                Award Recipient :
                Funded by: University of Geneva
                Categories
                Original Article
                Custom metadata
                © Springer Science+Business Media, LLC, part of Springer Nature 2023

                Neurology
                cerebellum,emotion,meta-analysis,fmri,explicit attention,implicit attention
                Neurology
                cerebellum, emotion, meta-analysis, fmri, explicit attention, implicit attention

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