Social communication in Tourette syndrome: a glimpse at the contribution of the insula and the prefrontal cortex

Social communication in Tourette syndrome: a glimpse at the contribution of the insula and the... Sir, We read with great interest the paper ‘Tourette syndrome: a disorder of the social decision-making network’, recently published in Brain (Albin, 2018). In this article, Albin explored the possibility that Tourette syndrome is characterized by neural abnormalities localized to several important brain regions associated with social behaviour and social decision-making. The author focused on several brain structures such as the amygdala, the periaqueductal grey, the hypothalamus, and basal ganglia, outlining key details on the relevance of these neural structures to support the view of this syndrome as disorder of social communication. Despite the growing body of evidence from psychometric studies (Eddy, 2018) showing abnormalities of social cognition in Tourette syndrome, the social behaviour dimension has been relatively under-explored. A core phenomenological feature of the Tourette spectrum is obscene (coprophenomena, e.g. coprolalia, coprographia and copropraxia) and non-obscene socially inappropriate behaviours (NOSIBs). Although social disinhibition appears to be a highly heritable symptom type within Tourette syndrome-related phenotypes (Hirschtritt et al., 2016), its association with a dysfunctional connectivity within the social behaviour network (SBN) has not been investigated in case-control studies. Brain imaging studies investigating the functional neuroanatomy of social behavioural anomalies are surprisingly scant and limited to single case studies. In Stern et al. (2000) the insular activity was particularly pre-eminent in a Tourette syndrome patient affected by coprolalia, whereas Gates et al. (2004) described a Tourette syndrome patient in whom coprolalia was associated with activation of the left middle frontal gyrus. As a complement to Albin’s thought-provoking view and in keeping with the findings from these isolated case studies, we believe it is interesting to expand the discussion to two further neural regions that are key components of the SBN, namely the insula and the ventro-medial prefrontal cortex (vmPFC). A recent review of our group (Vicario et al., 2017) suggested that dysfunction of these two cortical regions has a central role in the pathogenesis of defects in social decision-making behaviours, such as moral reasoning and decision-making, across different neurological and psychiatric disorders, including obsessive-compulsive disorder, the second most common behavioural comorbidity of Tourette syndrome. Importantly, the neural connectivity of both these regions is altered in Tourette syndrome (Jeffries et al., 2002; Müller-Vahl et al., 2009; Tinaz et al., 2015; Cavanna et al., 2017; Greene et al., 2017). Tinaz et al. (2015) used graph theory-based neural network analysis of resting state functional MRI data to demonstrate higher connectivity of the right dorsal anterior insula with urge- and tic-related cortico-striato-thalamic regions, as well as a positive correlation between functional connectivity between this portion of the insula and the supplementary motor area and severity of premonitory urges. This change of functional connectivity could affect social cognitive fitness besides influencing awareness and processing of bodily sensations. The insular cortex has been linked to affiliative behavioural patterns in an intracortical microstimulation study on non-human primates, with particular regard to social and communicative behaviour (Caruana et al., 2011). Moreover, a variety of orofacial motor programmes, crucial for social communication including affiliative behaviour, has been localized to the anterior and centro-ventral insular sectors (Jezzini et al., 2012). A body of human imaging studies exploring empathy for others’ pain have shown activations in the anterior insula, also involved in the direct experience of pain. This evidence supports the computational role of the anterior insula in processing emotionally charged states in order to guide adaptive, goal-directed behaviours in dynamic social contexts (Bernhardt and Singer, 2012). Kim et al. (2016) reported greater insular activation in response to tasks involving the Theory of Mind (ToM) dimension, i.e. the ability to think about mental states such as beliefs and emotions, a social cognition dimension, which is known to be affected in Tourette syndrome (Eddy et al., 2011). New imaging studies are therefore needed to understand which subdivisions of the insula are characterized by dysfunctional connectivity in Tourette syndrome, and how this relates to social cognition performance. In a recent, large voxel-based morphometry study, Greene et al. (2017) reported reduced white matter volume bilaterally in the orbital and medial prefrontal cortex of Tourette syndrome patients. Different subregions of the orbital frontal cortex appear to be associated with different features of social cognition (Nestor et al., 2013). Moreover, in healthy subjects the volume of the orbital prefrontal cortex was found to correlate with the size of social networks (Powell et al., 2012). Shamay-Tsoory et al. (2007) also documented an impairment of the ‘affective’ subtype of the ToM dimension in association with dysfunctional connectivity of the vmPFC. Like for the insular region, more research is necessary to understand the correlation between structural and functional connectivity changes and social cognition performance in patients with Tourette syndrome. Overall, our considerations corroborate the hypothesis of a social communication deficit in Tourette syndrome, at the same time highlighting the importance to include the insula and the PFC as two key structures requiring exploration in future research on the social behaviour network of Tourette syndrome. References Albin RL . Tourette syndrome: a disorder of the social decision-making network . Brain 2018 ; 141 : 332 – 47 . Google Scholar CrossRef Search ADS PubMed Bernhardt BC , Singer T . The neural basis of empathy . Annu Rev Neurosci 2012 ; 35 : 1 – 23 . Google Scholar CrossRef Search ADS PubMed Caruana F , Jezzini A , Sbriscia-Fioretti B , Rizzolatti G , Gallese V . Emotional and social behaviors elicited by electrical stimulation of the insula in the macaque monkey . Curr Biol 2011 ; 21 : 195 – 9 . Google Scholar CrossRef Search ADS PubMed Cavanna AE , Black KJ , Hallett M , Voon V . neurobiology of the premonitory urge in Tourette's syndrome: pathophysiology and treatment implications . J Neuropsychiatry Clin Neurosci 2017 ; 29 : 95 – 104 . Google Scholar CrossRef Search ADS PubMed Eddy CM . Social cognition and self-other distinctions in neuropsychiatry: insights from schizophrenia and Tourette syndrome . Prog Neuropsychopharmacol Biol Psychiatry 2018 ; 82 : 69 – 85 . Google Scholar CrossRef Search ADS PubMed Eddy CM , Mitchell IJ , Beck SR , Cavanna AE , Rickards H . Social reasoning in Tourette syndrome . Cogn Neuropsychiatry 2011 ; 16 : 326 – 4 Google Scholar CrossRef Search ADS PubMed Gates L , Clarke JR , Stokes A , Somorjai R , Jarmasz M , Vandorpe R et al. . Neuroanatomy of coprolalia in Tourette syndrome using functional magnetic resonanceimaging . Prog Neuropsychopharmacol Biol Psychiatry 2004 ; 28 : 397 – 400 . Google Scholar CrossRef Search ADS PubMed Greene DJ , Williams Iii AC , Koller JM , Schlaggar BL , Black KJ . Brain structure in pediatric Tourette syndrome . Mol Psychiatry 2017 ; 22 : 972 – 80 . Google Scholar CrossRef Search ADS PubMed Hirschtritt ME , Darrow SM , Illmann C , Osiecki L , Grados M , Sandor P et al. . Tourette Syndrome Association International Consortium for Genetics (TSAICG). Social disinhibition is a heritable subphenotype of tics in Tourette syndrome . Neurology 2016 ; 87 : 497 – 504 . Google Scholar CrossRef Search ADS PubMed Jeffries KJ , Schooler C , Schoenbach C , Herscovitch P , Chase TN , Braun AR . The functional neuroanatomy of Tourette's syndrome: an FDG PET study III: functional coupling of regional cerebral metabolic rates . Neuropsychopharmacology 2002 ; 27 : 92 – 104 . Google Scholar CrossRef Search ADS PubMed Jezzini A , Caruana F , Stoianov I , Gallese V , Rizzolatti G . Functional organization of the insula and inner perisylvian regions . Proc Natl Acad Sci USA 2012 ; 109 : 10077 – 82 . Google Scholar CrossRef Search ADS PubMed Kim E , Kyeong S , Cheon KA , Park B , Oh MK , Chun JW et al. . Neural responses to affective and cognitive theory of mind in children and adolescents with autism spectrum disorder . Neurosci Lett 2016 ; 621 : 117 – 25 . Google Scholar CrossRef Search ADS PubMed Müller-Vahl KR , Kaufmann J , Grosskreutz J , Dengler R , Emrich HM , Peschel T . Prefrontal and anterior cingulate cortex abnormalities in Tourette Syndrome: evidence from voxel-based morphometry and magnetization transfer imaging . BMC Neurosci 2009 ; 10 : 47 . Google Scholar CrossRef Search ADS PubMed Nestor PG , Nakamura M , Niznikiewicz M , Thompson E , Levitt JJ , Choate V et al. . In search of the functional neuroanatomy of sociality: MRI subdivisions of orbital frontal cortex and social cognition . Soc Cogn Affect Neurosci 2013 ; 8 : 460 – 7 . Google Scholar CrossRef Search ADS PubMed Powell J , Lewis PA , Roberts N , García-Fiñana M , Dunbar RI . Orbital prefrontal cortex volume predicts social network size: an imaging study of individual differences in humans . Proc Biol Sci 2012 ; 279 : 2157 – 62 . Google Scholar CrossRef Search ADS PubMed Shamay-Tsoory SG , Tibi-Elhanany Y , Aharon-Peretz J . The green-eyed monster and malicious joy: the neuroanatomical bases on envy and gloating (schadenfreude) . Brain 2007 ; 130 : 1663 – 78 . Google Scholar CrossRef Search ADS PubMed Stern E , Silbersweig DA , Chee KY , Holmes A , Robertson MM , Trimble M et al. . A functional neuroanatomy of tics in Tourette syndrome . Arch Gen Psychiatry 2000 ; 57 : 741 – 8 . Google Scholar CrossRef Search ADS PubMed Tinaz S , Malone P , Hallett M , Horovitz SG . Role of the right dorsal anterior insula in the urge to tic in Tourette syndrome . Mov Disord 2015 ; 30 : 1190 – 7 . Google Scholar CrossRef Search ADS PubMed Vicario CM , Rafal RD , Martino D , Avenanti A . Core, social and moral disgust are bounded: a review on behavioral and neural bases of repugnance in clinical disorders . Neurosci Biobehav Rev 2017 ; 80 : 185 – 200 . Google Scholar CrossRef Search ADS PubMed © The Author(s) (2018). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Brain Oxford University Press

Social communication in Tourette syndrome: a glimpse at the contribution of the insula and the prefrontal cortex

Brain , Volume 141 (8) – Aug 1, 2018

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© The Author(s) (2018). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For permissions, please email: journals.permissions@oup.com
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Abstract

Sir, We read with great interest the paper ‘Tourette syndrome: a disorder of the social decision-making network’, recently published in Brain (Albin, 2018). In this article, Albin explored the possibility that Tourette syndrome is characterized by neural abnormalities localized to several important brain regions associated with social behaviour and social decision-making. The author focused on several brain structures such as the amygdala, the periaqueductal grey, the hypothalamus, and basal ganglia, outlining key details on the relevance of these neural structures to support the view of this syndrome as disorder of social communication. Despite the growing body of evidence from psychometric studies (Eddy, 2018) showing abnormalities of social cognition in Tourette syndrome, the social behaviour dimension has been relatively under-explored. A core phenomenological feature of the Tourette spectrum is obscene (coprophenomena, e.g. coprolalia, coprographia and copropraxia) and non-obscene socially inappropriate behaviours (NOSIBs). Although social disinhibition appears to be a highly heritable symptom type within Tourette syndrome-related phenotypes (Hirschtritt et al., 2016), its association with a dysfunctional connectivity within the social behaviour network (SBN) has not been investigated in case-control studies. Brain imaging studies investigating the functional neuroanatomy of social behavioural anomalies are surprisingly scant and limited to single case studies. In Stern et al. (2000) the insular activity was particularly pre-eminent in a Tourette syndrome patient affected by coprolalia, whereas Gates et al. (2004) described a Tourette syndrome patient in whom coprolalia was associated with activation of the left middle frontal gyrus. As a complement to Albin’s thought-provoking view and in keeping with the findings from these isolated case studies, we believe it is interesting to expand the discussion to two further neural regions that are key components of the SBN, namely the insula and the ventro-medial prefrontal cortex (vmPFC). A recent review of our group (Vicario et al., 2017) suggested that dysfunction of these two cortical regions has a central role in the pathogenesis of defects in social decision-making behaviours, such as moral reasoning and decision-making, across different neurological and psychiatric disorders, including obsessive-compulsive disorder, the second most common behavioural comorbidity of Tourette syndrome. Importantly, the neural connectivity of both these regions is altered in Tourette syndrome (Jeffries et al., 2002; Müller-Vahl et al., 2009; Tinaz et al., 2015; Cavanna et al., 2017; Greene et al., 2017). Tinaz et al. (2015) used graph theory-based neural network analysis of resting state functional MRI data to demonstrate higher connectivity of the right dorsal anterior insula with urge- and tic-related cortico-striato-thalamic regions, as well as a positive correlation between functional connectivity between this portion of the insula and the supplementary motor area and severity of premonitory urges. This change of functional connectivity could affect social cognitive fitness besides influencing awareness and processing of bodily sensations. The insular cortex has been linked to affiliative behavioural patterns in an intracortical microstimulation study on non-human primates, with particular regard to social and communicative behaviour (Caruana et al., 2011). Moreover, a variety of orofacial motor programmes, crucial for social communication including affiliative behaviour, has been localized to the anterior and centro-ventral insular sectors (Jezzini et al., 2012). A body of human imaging studies exploring empathy for others’ pain have shown activations in the anterior insula, also involved in the direct experience of pain. This evidence supports the computational role of the anterior insula in processing emotionally charged states in order to guide adaptive, goal-directed behaviours in dynamic social contexts (Bernhardt and Singer, 2012). Kim et al. (2016) reported greater insular activation in response to tasks involving the Theory of Mind (ToM) dimension, i.e. the ability to think about mental states such as beliefs and emotions, a social cognition dimension, which is known to be affected in Tourette syndrome (Eddy et al., 2011). New imaging studies are therefore needed to understand which subdivisions of the insula are characterized by dysfunctional connectivity in Tourette syndrome, and how this relates to social cognition performance. In a recent, large voxel-based morphometry study, Greene et al. (2017) reported reduced white matter volume bilaterally in the orbital and medial prefrontal cortex of Tourette syndrome patients. Different subregions of the orbital frontal cortex appear to be associated with different features of social cognition (Nestor et al., 2013). Moreover, in healthy subjects the volume of the orbital prefrontal cortex was found to correlate with the size of social networks (Powell et al., 2012). Shamay-Tsoory et al. (2007) also documented an impairment of the ‘affective’ subtype of the ToM dimension in association with dysfunctional connectivity of the vmPFC. Like for the insular region, more research is necessary to understand the correlation between structural and functional connectivity changes and social cognition performance in patients with Tourette syndrome. Overall, our considerations corroborate the hypothesis of a social communication deficit in Tourette syndrome, at the same time highlighting the importance to include the insula and the PFC as two key structures requiring exploration in future research on the social behaviour network of Tourette syndrome. References Albin RL . Tourette syndrome: a disorder of the social decision-making network . Brain 2018 ; 141 : 332 – 47 . Google Scholar CrossRef Search ADS PubMed Bernhardt BC , Singer T . The neural basis of empathy . Annu Rev Neurosci 2012 ; 35 : 1 – 23 . Google Scholar CrossRef Search ADS PubMed Caruana F , Jezzini A , Sbriscia-Fioretti B , Rizzolatti G , Gallese V . Emotional and social behaviors elicited by electrical stimulation of the insula in the macaque monkey . Curr Biol 2011 ; 21 : 195 – 9 . Google Scholar CrossRef Search ADS PubMed Cavanna AE , Black KJ , Hallett M , Voon V . neurobiology of the premonitory urge in Tourette's syndrome: pathophysiology and treatment implications . J Neuropsychiatry Clin Neurosci 2017 ; 29 : 95 – 104 . Google Scholar CrossRef Search ADS PubMed Eddy CM . Social cognition and self-other distinctions in neuropsychiatry: insights from schizophrenia and Tourette syndrome . Prog Neuropsychopharmacol Biol Psychiatry 2018 ; 82 : 69 – 85 . Google Scholar CrossRef Search ADS PubMed Eddy CM , Mitchell IJ , Beck SR , Cavanna AE , Rickards H . Social reasoning in Tourette syndrome . Cogn Neuropsychiatry 2011 ; 16 : 326 – 4 Google Scholar CrossRef Search ADS PubMed Gates L , Clarke JR , Stokes A , Somorjai R , Jarmasz M , Vandorpe R et al. . Neuroanatomy of coprolalia in Tourette syndrome using functional magnetic resonanceimaging . Prog Neuropsychopharmacol Biol Psychiatry 2004 ; 28 : 397 – 400 . Google Scholar CrossRef Search ADS PubMed Greene DJ , Williams Iii AC , Koller JM , Schlaggar BL , Black KJ . Brain structure in pediatric Tourette syndrome . Mol Psychiatry 2017 ; 22 : 972 – 80 . Google Scholar CrossRef Search ADS PubMed Hirschtritt ME , Darrow SM , Illmann C , Osiecki L , Grados M , Sandor P et al. . Tourette Syndrome Association International Consortium for Genetics (TSAICG). Social disinhibition is a heritable subphenotype of tics in Tourette syndrome . Neurology 2016 ; 87 : 497 – 504 . Google Scholar CrossRef Search ADS PubMed Jeffries KJ , Schooler C , Schoenbach C , Herscovitch P , Chase TN , Braun AR . The functional neuroanatomy of Tourette's syndrome: an FDG PET study III: functional coupling of regional cerebral metabolic rates . Neuropsychopharmacology 2002 ; 27 : 92 – 104 . Google Scholar CrossRef Search ADS PubMed Jezzini A , Caruana F , Stoianov I , Gallese V , Rizzolatti G . Functional organization of the insula and inner perisylvian regions . Proc Natl Acad Sci USA 2012 ; 109 : 10077 – 82 . Google Scholar CrossRef Search ADS PubMed Kim E , Kyeong S , Cheon KA , Park B , Oh MK , Chun JW et al. . Neural responses to affective and cognitive theory of mind in children and adolescents with autism spectrum disorder . Neurosci Lett 2016 ; 621 : 117 – 25 . Google Scholar CrossRef Search ADS PubMed Müller-Vahl KR , Kaufmann J , Grosskreutz J , Dengler R , Emrich HM , Peschel T . Prefrontal and anterior cingulate cortex abnormalities in Tourette Syndrome: evidence from voxel-based morphometry and magnetization transfer imaging . BMC Neurosci 2009 ; 10 : 47 . Google Scholar CrossRef Search ADS PubMed Nestor PG , Nakamura M , Niznikiewicz M , Thompson E , Levitt JJ , Choate V et al. . In search of the functional neuroanatomy of sociality: MRI subdivisions of orbital frontal cortex and social cognition . Soc Cogn Affect Neurosci 2013 ; 8 : 460 – 7 . Google Scholar CrossRef Search ADS PubMed Powell J , Lewis PA , Roberts N , García-Fiñana M , Dunbar RI . Orbital prefrontal cortex volume predicts social network size: an imaging study of individual differences in humans . Proc Biol Sci 2012 ; 279 : 2157 – 62 . Google Scholar CrossRef Search ADS PubMed Shamay-Tsoory SG , Tibi-Elhanany Y , Aharon-Peretz J . The green-eyed monster and malicious joy: the neuroanatomical bases on envy and gloating (schadenfreude) . Brain 2007 ; 130 : 1663 – 78 . Google Scholar CrossRef Search ADS PubMed Stern E , Silbersweig DA , Chee KY , Holmes A , Robertson MM , Trimble M et al. . A functional neuroanatomy of tics in Tourette syndrome . Arch Gen Psychiatry 2000 ; 57 : 741 – 8 . Google Scholar CrossRef Search ADS PubMed Tinaz S , Malone P , Hallett M , Horovitz SG . Role of the right dorsal anterior insula in the urge to tic in Tourette syndrome . Mov Disord 2015 ; 30 : 1190 – 7 . Google Scholar CrossRef Search ADS PubMed Vicario CM , Rafal RD , Martino D , Avenanti A . Core, social and moral disgust are bounded: a review on behavioral and neural bases of repugnance in clinical disorders . Neurosci Biobehav Rev 2017 ; 80 : 185 – 200 . Google Scholar CrossRef Search ADS PubMed © The Author(s) (2018). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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BrainOxford University Press

Published: Aug 1, 2018

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