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      Premonitory urges are associated with decreased grey matter thickness within the insula and sensorimotor cortex in young people with Tourette syndrome

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          Abstract

          Tourette syndrome ( TS) is a neurological disorder characterized by vocal and motor tics and is associated with cortical–striatal–thalamic–cortical circuit ( CSTC) dysfunction and hyperexcitability of cortical limbic and motor regions, which are thought to lead to the occurrence of tics. Importantly, individuals with TS often report that their tics are preceded by ‘premonitory sensory phenomena’ ( PSP) that are described as uncomfortable cognitive or bodily sensations that precede the execution of a tic, and are experienced as a strong urge for motor discharge. While the precise role played by PSP in the occurrence of tics is controversial, PSP are nonetheless of considerable theoretical and clinical importance in TS, not least because they form the core component in many of the behavioural therapies that are currently used in the treatment of tic disorders. In this study, we investigated the brain structure correlates of PSP. Specifically, we conducted a whole‐brain analysis of cortical (grey matter) thickness in 29 children and young adults with TS and investigated the association between grey matter thickness and PSP. We demonstrate for the first time that PSP are inversely associated with grey matter thickness measurements within the insula and sensorimotor cortex. We also demonstrate that grey matter thickness is significantly reduced in these areas in individuals with TS relative to a closely age‐ and gender‐matched group of typically developing individuals and that PSP ratings are significantly correlated with tic severity.

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          Most cited references16

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          Circuitry and functional aspects of the insular lobe in primates including humans.

          The progress made in understanding the insula in the decade following an earlier review (Augustine, Neurol. Res., 7 (1985) 2-10) is examined in this review. In these ten years, connections have been described between the insula and the orbital cortex, frontal operculum, lateral premotor cortex, ventral granular cortex, and medial area 6 in the frontal lobe. Insular connections between the second somatosensory area and retroinsular area of the parietal lobe have been documented. The insula was found to connect with the temporal pole and the superior temporal sulcus of the temporal lobe. It has an abundance of local intrainsular connections and projections to subdivisions of the cingulate gyrus. The insula has connections with the lateral, lateral basal, central, cortical and medial amygdaloid nuclei. It also connects with nonamygdaloid areas such as the perirhinal cortex, entorhinal, and periamygdaloid cortex. The thalamic taste area, the parvicellular part of the ventral posteromedial nucleus, projects fibers to the ipsilateral insular-opercular cortex. In the past decade, confirmation has been given to the insula as a visceral sensory area, visceral motor area, motor association area, vestibular area, and language area. Recent studies have expanded the role of the insula as a somatosensory area, emphasizing its multifaceted, sensory role. The idea of the insula as limbic integration cortex has been affirmed and its role in Alzheimer's disease suggested.
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            Premonitory Urge for Tics Scale (PUTS): initial psychometric results and examination of the premonitory urge phenomenon in youths with Tic disorders.

            Although motor tics and/or vocal tics are the defining features of chronic tic disorder (CTD) and Tourette syndrome (TS), older youths and adults often report their tics to be preceded by an unpleasant sensation or "premonitory urge." While premonitory urge phenomena may play an important role in behavioral interventions for CTD/TS, standardized assessments for premonitory urges do not exist. The current study of 42 youths with TS or CTD presents initial psychometric data for a new, brief self-report scale designed to measure tic-related premonitory urges. Results showed that the Premonitory Urge for Tics Scale (PUTS) was internally consistent (alpha = .81) and temporally stable at 1 (r = 0.79, p < .01) and 2 (r = 0.86, p < .01) weeks. PUTS scores were also correlated with overall tic severity as measured by the Yale Global Tic Severity Scale (YGTSS; r = 0.31, p < .05) and the YGTSS number (r = 0.35, p < .05), complexity (r = 0.49, p < .01), and interference (r = 0.36, p < .05) subscales. Finally, an examination of the psychiatric correlates of the premonitory urge phenomenon yielded significant correlations between the PUTS and the Child Behavior Checklist (CBCL) anxiety/depression (r = 0.33, p < .05), and withdrawal (r = 0.38, p < .05) subscales as well as the Children's Yale-Brown Obsessive Compulsive Scale (CYBOCS; r = 0.31, p < .05). However, a cross-sectional examination of the data showed that the psychometric properties of the PUTS were not acceptable for youths 10 years of age and younger. Likewise, significant correlations found between the YGTSS subscales, CBCL subscales, CYBOCS, and the PUTS did not emerge in this younger age group. The clinical and theoretical implications of these findings are discussed.
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              Neural correlates of tic generation in Tourette syndrome: an event-related functional MRI study.

              Little is known about the neural correlates of tics and associated urges. In the present study, we aimed to explore the neural basis of tics in patients with Tourette syndrome by using event-related functional MRI (fMRI). Ten patients (6 women, 4 men; age: mean +/- SD = 31 +/- 11.2) were studied while spontaneously exhibiting a variety of motor and vocal tics. On the basis of synchronized video/audio recordings, fMRI activities were analysed 2 s before and at tic onset irrespective of the clinical phenomenology. We identified a brain network of paralimbic areas such as anterior cingulate and insular cortex, supplementary motor area (SMA) and parietal operculum (PO) predominantly activated before tic onset (P < 0.05, corrected for multiple comparisons). In contrast, at the beginning of tic action, significant fMRI activities were found in sensorimotor areas including superior parietal lobule bilaterally and cerebellum. The results of this study indicate that paralimbic and sensory association areas are critically implicated in tic generation, similar to movements triggered internally by unpleasant sensations, as has been shown for pain or itching.
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                Author and article information

                Journal
                J Neuropsychol
                J Neuropsychol
                10.1111/(ISSN)1748-6653
                JNP
                Journal of Neuropsychology
                John Wiley and Sons Inc. (Hoboken )
                1748-6645
                1748-6653
                05 November 2015
                March 2016
                : 10
                : 1 ( doiID: 10.1111/jnp.2016.10.issue-1 )
                : 143-153
                Affiliations
                [ 1 ] School of PsychologyUniversity of Nottingham UK
                [ 2 ] Institute of Mental Health School of MedicineUniversity of Nottingham UK
                [ 3 ] Medical Physics & Clinical EngineeringQueen's Medical Centre NottinghamUK
                Author notes
                [*] [* ]Correspondence should be addressed to Stephen R. Jackson, School of Psychology, University of Nottingham, University Park, Nottingham NG7 2RD, UK (email: Stephen.jackson@ 123456nottingham.ac.uk ).
                Author information
                http://orcid.org/0000-0002-5676-4072
                Article
                JNP12089
                10.1111/jnp.12089
                4982075
                26538289
                59bf1ec2-e5e8-4d9d-bbfe-68e78635dfaf
                © 2015 The Authors. Journal of Neuropsychology published by John Wiley & Sons Ltd on behalf of British Psychological Society

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 29 July 2015
                : 12 September 2015
                Page count
                Pages: 11
                Funding
                Funded by: James Tudor Foundation
                Award ID: G0901321
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                jnp12089
                March 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.4 mode:remove_FC converted:16.08.2016

                Clinical Psychology & Psychiatry
                tourette syndrome,cortical thickness,premonitory urges,premonitory sensory phenomena,magnetic resonance imaging,insula,sensorimotor cortex

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