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      Distinctive tics suppression network in Gilles de la Tourette syndrome distinguished from suppression of natural urges using multimodal imaging

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          Abstract

          Background and objectives

          Gilles de la Tourette syndrome (GTS) is a neuropsychiatric disorder characterized by tics. A hallmark of GTS is the ability to voluntarily suppress tics. Our aim was to distinguish the neural circuits involved in the voluntary suppression of ocular tics in GTS patients from blink suppression in healthy subjects.

          Methods

          Fifteen GTS patients and 22 healthy control subjects were included in a multimodal study using eye-tracker recordings during functional MRI (fMRI). The ability to suppress tics/blinks was compared both on subjective (self-rating) and objective (eye-tracker) performance. For fMRI analysis we used a novel designed performance-adapted block design analysis of tic/blink suppression and release based on eye-tracker monitoring.

          Results

          We found that the subjective self-reported ability to suppress tics or blinks showed no significant correlation with objective task performance. In GTS during successful suppression of tics, the dorsal anterior cingulate cortex and associated limbic areas showed increased activation. During successful suppression of eye blinks in healthy subjects, the right ventrolateral prefrontal cortex and supplementary and cingulate motor areas showed increased activation.

          Conclusions

          These findings demonstrate that GTS patients use a characteristic limbic suppression strategy. In contrast, control subjects use the voluntary sensorimotor circuits and the classical ‘stop’ network to suppress natural urges. The employment of different neural suppression networks provides support for cognitive behavioral therapy in GTS.

          Highlights

          • Neural networks of tic suppression are specific and differ from blink suppression.

          • Tourette patients employ a limbic suppression strategy to suppress tics.

          • Controls use sensorimotor circuits and ‘stop’ networks for blink suppression.

          • Objective task performance is highly recommended during functional MRI of tics.

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          Most cited references46

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          Parallel organization of functionally segregated circuits linking basal ganglia and cortex.

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            Contributions of anterior cingulate cortex to behaviour.

            Assessments of anterior cingulate cortex in experimental animals and humans have led to unifying theories of its structural organization and contributions to mammalian behaviour. The anterior cingulate cortex forms a large region around the rostrum of the corpus callosum that is termed the anterior executive region. This region has numerous projections into motor systems, however, since these projections originate from different parts of anterior cingulate cortex and because functional studies have shown that it does not have a uniform contribution to brain functions, the anterior executive region is further subdivided into 'affect' and 'cognition' components. The affect division includes areas 25, 33 and rostral area 24, and has extensive connections with the amygdala and periaqueductal grey, and parts of it project to autonomic brainstem motor nuclei. In addition to regulating autonomic and endocrine functions, it is involved in conditioned emotional learning, vocalizations associated with expressing internal states, assessments of motivational content and assigning emotional valence to internal and external stimuli, and maternal-infant interactions. The cognition division includes caudal areas 24' and 32', the cingulate motor areas in the cingulate sulcus and nociceptive cortex. The cingulate motor areas project to the spinal cord and red nucleus and have premotor functions, while the nociceptive area is engaged in both response selection and cognitively demanding information processing. The cingulate epilepsy syndrome provides important support of experimental animal and human functional imaging studies for the role of anterior cingulate cortex in movement, affect and social behaviours. Excessive cingulate activity in cases with seizures confirmed in anterior cingulate cortex with subdural electrode recordings, can impair consciousness, alter affective state and expression, and influence skeletomotor and autonomic activity. Interictally, patients with anterior cingulate cortex epilepsy often display psychopathic or sociopathic behaviours. In other clinical examples of elevated anterior cingulate cortex activity it may contribute to tics, obsessive-compulsive behaviours, and aberrent social behaviour. Conversely, reduced cingulate activity following infarcts or surgery can contribute to behavioural disorders including akinetic mutism, diminished self-awareness and depression, motor neglect and impaired motor initiation, reduced responses to pain, and aberrent social behaviour. The role of anterior cingulate cortex in pain responsiveness is suggested by cingulumotomy results and functional imaging studies during noxious somatic stimulation. The affect division of anterior cingulate cortex modulates autonomic activity and internal emotional responses, while the cognition division is engaged in response selection associated with skeletomotor activity and responses to noxious stimuli. Overall, anterior cingulate cortex appears to play a crucial role in initiation, motivation, and goal-directed behaviours.(ABSTRACT TRUNCATED AT 400 WORDS)
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              Converging evidence for a fronto-basal-ganglia network for inhibitory control of action and cognition.

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                Author and article information

                Contributors
                Journal
                Neuroimage Clin
                Neuroimage Clin
                NeuroImage : Clinical
                Elsevier
                2213-1582
                19 September 2018
                2018
                19 September 2018
                : 20
                : 783-792
                Affiliations
                [a ]Department of Neurology and Clinical Neurophysiology, Amsterdam UMC, University of Amsterdam, Amsterdam, the Netherlands
                [b ]Brain Center Rudolf Magnus, Department of Neurology and Neurosurgery, University Medical Center Utrecht, the Netherlands
                [c ]Department of Clinical & Health Psychology, University of Utrecht, GGz Drenthe, Department of Psychiatry, University Medical Center Groningen, the Netherlands
                [d ]Department of Radiology, Amsterdam UMC, University of Amsterdam, Amsterdam, the Netherlands
                [e ]Department of Anatomy and Neurosciences, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, the Netherlands
                [f ]Netherlands Institute for Neuroscience, An Institute of the Royal Netherlands Academy of Arts and Sciences, Amsterdam, the Netherlands
                [g ]Department of Pediatrics/Child Neurology, Neuroscience Campus Amsterdam, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, the Netherlands
                [h ]Department of Psychiatry, Amsterdam UMC, Vrije Universiteit Amsterdam and GGZ inGeest, Amsterdam, the Netherlands
                [i ]BIC: Brain Imaging Center, Amsterdam UMC, University of Amsterdam, Amsterdam, the Netherlands
                [j ]Department of Neurology, University Medical Centre Groningen, University of Groningen, the Netherlands
                [k ]Stichting Epilepsie Instellingen Nederland (SEIN), Zwolle, the Netherlands
                Author notes
                [* ]Corresponding author at: Department of Neurology, University Medical Centre Groningen (UMCG), University of Groningen, PO Box 30.001, 9700 RB Groningen, the Netherlands. M.A.J.de.Koning-Tijssen@ 123456umcg.nl
                Article
                S2213-1582(18)30289-4
                10.1016/j.nicl.2018.09.014
                6169325
                30268027
                83457b85-5470-4b95-9f97-b44ab2eb899d
                © 2018 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 12 May 2018
                : 19 August 2018
                : 16 September 2018
                Categories
                Regular Article

                gilles de la tourette syndrome,functional magnetic resonance imaging,suppression,tics,urges

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