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      A Bayesian Account of the Sensory-Motor Interactions Underlying Symptoms of Tourette Syndrome

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          Abstract

          Tourette syndrome is a hyperkinetic movement disorder. Characteristic features include tics, recurrent movements that are experienced as compulsive and “unwilled”; uncomfortable premonitory sensations that resolve through tic release; and often, the ability to suppress tics temporarily. We demonstrate how these symptoms and features can be understood in terms of aberrant predictive (Bayesian) processing in hierarchical neural systems, explaining specifically: why tics arise, their “unvoluntary” nature, how premonitory sensations emerge, and why tic suppression works—sometimes. In our model, premonitory sensations and tics are generated through over-precise priors for sensation and action within somatomotor regions of the striatum. Abnormally high precision of priors arises through the dysfunctional synaptic integration of cortical inputs. These priors for sensation and action are projected into primary sensory and motor areas, triggering premonitory sensations and tics, which in turn elicit prediction errors for unexpected feelings and movements. We propose experimental paradigms to validate this Bayesian account of tics. Our model integrates behavioural, neuroimaging, and computational approaches to provide mechanistic insight into the pathophysiological basis of Tourette syndrome.

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          Modulation of striatal projection systems by dopamine.

          The basal ganglia are a chain of subcortical nuclei that facilitate action selection. Two striatal projection systems--so-called direct and indirect pathways--form the functional backbone of the basal ganglia circuit. Twenty years ago, investigators proposed that the striatum's ability to use dopamine (DA) rise and fall to control action selection was due to the segregation of D(1) and D(2) DA receptors in direct- and indirect-pathway spiny projection neurons. Although this hypothesis sparked a debate, the evidence that has accumulated since then clearly supports this model. Recent advances in the means of marking neural circuits with optical or molecular reporters have revealed a clear-cut dichotomy between these two cell types at the molecular, anatomical, and physiological levels. The contrast provided by these studies has provided new insights into how the striatum responds to fluctuations in DA signaling and how diseases that alter this signaling change striatal function.
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            Interoceptive predictions in the brain.

            Intuition suggests that perception follows sensation and therefore bodily feelings originate in the body. However, recent evidence goes against this logic: interoceptive experience may largely reflect limbic predictions about the expected state of the body that are constrained by ascending visceral sensations. In this Opinion article, we introduce the Embodied Predictive Interoception Coding model, which integrates an anatomical model of corticocortical connections with Bayesian active inference principles, to propose that agranular visceromotor cortices contribute to interoception by issuing interoceptive predictions. We then discuss how disruptions in interoceptive predictions could function as a common vulnerability for mental and physical illness.
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              Corticostriatal circuitry

              Corticostriatal connections play a central role in developing appropriate goal-directed behaviors, including the motivation and cognition to develop appropriate actions to obtain a specific outcome. The cortex projects to the striatum topographically. Thus, different regions of the striatum have been associated with these different functions: the ventral striatum with reward; the caudate nucleus with cognition; and the putamen with motor control. However, corticostriatal connections are more complex, and interactions between functional territories are extensive. These interactions occur in specific regions in which convergence of terminal fields from different functional cortical regions are found. This article provides an overview of the connections of the cortex to the striatum and their role in integrating information across reward, cognitive, and motor functions. Emphasis is placed on the interface between functional domains within the striatum.
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                Author and article information

                Contributors
                Journal
                Front Psychiatry
                Front Psychiatry
                Front. Psychiatry
                Frontiers in Psychiatry
                Frontiers Media S.A.
                1664-0640
                05 March 2019
                2019
                : 10
                : 29
                Affiliations
                [1] 1Sackler Centre for Consciousness Science, University of Sussex , Brighton, United Kingdom
                [2] 2Department of Neuroscience, Brighton and Sussex Medical School , Brighton, United Kingdom
                [3] 3Sussex Partnership NHS Foundation Trust , Brighton, United Kingdom
                [4] 4School of Engineering and Informatics, University of Sussex , Brighton, United Kingdom
                Author notes

                Edited by: Bharat B. Biswal, University of Medicine and Dentistry of New Jersey, United States

                Reviewed by: Yosuke Morishima, University of Bern, Switzerland; Ryuichiro Hashimoto, Showa University, Japan

                *Correspondence: Charlotte L. Rae c.rae@ 123456bsms.ac.uk

                This article was submitted to Computational Psychiatry, a section of the journal Frontiers in Psychiatry

                Article
                10.3389/fpsyt.2019.00029
                6412155
                30890965
                324b54e2-5002-490b-918f-a19a9fb5ced1
                Copyright © 2019 Rae, Critchley and Seth.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 08 June 2018
                : 17 January 2019
                Page count
                Figures: 4, Tables: 2, Equations: 0, References: 141, Pages: 15, Words: 11867
                Funding
                Funded by: Dr. Mortimer and Theresa Sackler Foundation 10.13039/501100003754
                Categories
                Psychiatry
                Hypothesis and Theory

                Clinical Psychology & Psychiatry
                active inference,basal ganglia,insula,motor cortex,tics,tourette syndrome

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