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      Impaired Effective Connectivity During a Cerebellar-Mediated Sensorimotor Synchronization Task in Schizophrenia

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          Abstract

          Prominent conceptual models characterize schizophrenia as a dysconnectivity syndrome, with recent research focusing on the contributions of the cerebellum in this framework. The present study examined the role of the cerebellum and its effective connectivity to the cerebrum during sensorimotor synchronization in schizophrenia. Specifically, the role of the cerebellum in temporally coordinating cerebral motor activity was examined through path analysis. Thirty-one individuals diagnosed with schizophrenia and 40 healthy controls completed a finger-tapping fMRI task including tone-paced synchronization and self-paced continuation tapping at a 500 ms intertap interval (ITI). Behavioral data revealed shorter and more variable ITIs during self-paced continuation, greater clock (vs motor) variance, and greater force of tapping in the schizophrenia group. In a whole-brain analysis, groups showed robust activation of the cerebellum during self-paced continuation but not during tone-paced synchronization. However, effective connectivity analysis revealed decreased connectivity in individuals with schizophrenia between the cerebellum and primary motor cortex but increased connectivity between cerebellum and thalamus during self-paced continuation compared with healthy controls. These findings in schizophrenia indicate diminished temporal coordination of cerebral motor activity by cerebellum during the continuation tapping portion of sensorimotor synchronization. Taken together with the behavioral finding of greater temporal variability in schizophrenia, these effective connectivity results are consistent with structural and temporal models of dysconnectivity in the disorder.

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          Most cited references56

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          What makes us tick? Functional and neural mechanisms of interval timing.

          Time is a fundamental dimension of life. It is crucial for decisions about quantity, speed of movement and rate of return, as well as for motor control in walking, speech, playing or appreciating music, and participating in sports. Traditionally, the way in which time is perceived, represented and estimated has been explained using a pacemaker-accumulator model that is not only straightforward, but also surprisingly powerful in explaining behavioural and biological data. However, recent advances have challenged this traditional view. It is now proposed that the brain represents time in a distributed manner and tells the time by detecting the coincidental activation of different neural populations.
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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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              Sensorimotor synchronization: a review of recent research (2006-2012).

              Sensorimotor synchronization (SMS) is the coordination of rhythmic movement with an external rhythm, ranging from finger tapping in time with a metronome to musical ensemble performance. An earlier review (Repp, 2005) covered tapping studies; two additional reviews (Repp, 2006a, b) focused on music performance and on rate limits of SMS, respectively. The present article supplements and extends these earlier reviews by surveying more recent research in what appears to be a burgeoning field. The article comprises four parts, dealing with (1) conventional tapping studies, (2) other forms of moving in synchrony with external rhythms (including dance and nonhuman animals' synchronization abilities), (3) interpersonal synchronization (including musical ensemble performance), and (4) the neuroscience of SMS. It is evident that much new knowledge about SMS has been acquired in the last 7 years.
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                Author and article information

                Journal
                Schizophrenia Bulletin
                Oxford University Press (OUP)
                0586-7614
                1745-1701
                May 2019
                April 25 2019
                May 25 2018
                May 2019
                April 25 2019
                May 25 2018
                : 45
                : 3
                : 531-541
                Affiliations
                [1 ]Department of Psychological & Brain Sciences, Indiana University, Bloomington, IN
                [2 ]Larue D. Carter Memorial Hospital, Indianapolis, IN
                [3 ]Department of Psychiatry, Indiana University School of Medicine, Indianapolis, IN
                [4 ]Imaging Research Facility, Indiana University College of Arts and Sciences, Bloomington, IN
                Article
                10.1093/schbul/sby064
                6483568
                29800417
                09170cb8-a829-490d-bac2-5f655eaf4739
                © 2018

                https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model

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