Enhanced habit formation in Gilles de la Tourette syndrome.
Tics are sometimes described as voluntary movements performed in an automatic or habitual way. Here, we addressed the question of balance between goal-directed and habitual behavioural control in Gilles de la Tourette syndrome and formally tested the hypothesis of enhanced habit formation in these patients. To this aim, we administered a three-stage instrumental learning paradigm to 17 unmedicated and 17 antipsychotic-medicated patients with Gilles de la Tourette syndrome and matched controls. In the first stage of the task, participants learned stimulus-response-outcome associations. The subsequent outcome devaluation and 'slip-of-action' tests allowed evaluation of the participants' capacity to flexibly adjust their behaviour to changes in action outcome value. In this task, unmedicated patients relied predominantly on habitual, outcome-insensitive behavioural control. Moreover, in these patients, the engagement in habitual responses correlated with more severe tics. Medicated patients performed at an intermediate level between unmedicated patients and controls. Using diffusion tensor imaging on a subset of patients, we also addressed whether the engagement in habitual responding was related to structural connectivity within cortico-striatal networks. We showed that engagement in habitual behaviour in patients with Gilles de la Tourette syndrome correlated with greater structural connectivity within the right motor cortico-striatal network. In unmedicated patients, stronger structural connectivity of the supplementary motor cortex with the sensorimotor putamen predicted more severe tics. Overall, our results indicate enhanced habit formation in unmedicated patients with Gilles de la Tourette syndrome. Aberrant reinforcement signals to the sensorimotor striatum may be fundamental for the formation of stimulus-response associations and may contribute to the habitual behaviour and tics of this syndrome.
1 Sorbonne Universités, UPMC Univ Paris 06, UMR S 975, CNRS UMR 7225, ICM, F-75013, Paris, France 2 Assistance Publique-Hôpitaux de Paris, Department of Neurology, Groupe Hospitalier Pitié-Salpêtrière, 47 boulevard de l'Hôpital, F-75013, Paris, France.
Cécile
C
Delorme
3 Centre de Psychiatrie et Neuroscience - INSERM U894, 2 ter Rue d'Alésia - 75014 Paris, France 4 Laboratoire de Neurosciences Cognitives, Ecole Normale Supérieure, 29 rue d'Ulm, F-75002, Paris, France.
Alexandre
A
Salvador
1 Sorbonne Universités, UPMC Univ Paris 06, UMR S 975, CNRS UMR 7225, ICM, F-75013, Paris, France 5 Centre de NeuroImagerie de Recherche (CENIR), Sorbonne Universités, UPMC Univ Paris 06, UMR S 975, CNRS UMR 7225, ICM, F-75013, Paris, France.
Romain
R
Valabrègue
1 Sorbonne Universités, UPMC Univ Paris 06, UMR S 975, CNRS UMR 7225, ICM, F-75013, Paris, France 2 Assistance Publique-Hôpitaux de Paris, Department of Neurology, Groupe Hospitalier Pitié-Salpêtrière, 47 boulevard de l'Hôpital, F-75013, Paris, France.
Emmanuel
E
Roze
3 Centre de Psychiatrie et Neuroscience - INSERM U894, 2 ter Rue d'Alésia - 75014 Paris, France 6 Institute of Cognitive Neuroscience, Alexandra House 17 Queen Square, London WC1N 3AR, UK.
Stefano
S
Palminteri
1 Sorbonne Universités, UPMC Univ Paris 06, UMR S 975, CNRS UMR 7225, ICM, F-75013, Paris, France 2 Assistance Publique-Hôpitaux de Paris, Department of Neurology, Groupe Hospitalier Pitié-Salpêtrière, 47 boulevard de l'Hôpital, F-75013, Paris, France.
Marie
M
Vidailhet
7 Department of Psychology, University of Amsterdam, 1018 WB Amsterdam, The Netherlands.
Sanne
S
de Wit
8 Department of Psychology, University of Cambridge, Cambridge, UK.
Trevor
T
Robbins
1 Sorbonne Universités, UPMC Univ Paris 06, UMR S 975, CNRS UMR 7225, ICM, F-75013, Paris, France 2 Assistance Publique-Hôpitaux de Paris, Department of Neurology, Groupe Hospitalier Pitié-Salpêtrière, 47 boulevard de l'Hôpital, F-75013, Paris, France 9 French Reference Centre for Gilles de la Tourette Syndrome, Groupe Hospitalier Pitié-Salpêtrière, 47 boulevard de l'Hôpital, F-75013, Paris, France.
Andreas
A
Hartmann
1 Sorbonne Universités, UPMC Univ Paris 06, UMR S 975, CNRS UMR 7225, ICM, F-75013, Paris, France 2 Assistance Publique-Hôpitaux de Paris, Department of Neurology, Groupe Hospitalier Pitié-Salpêtrière, 47 boulevard de l'Hôpital, F-75013, Paris, France 9 French Reference Centre for Gilles de la Tourette Syndrome, Groupe Hospitalier Pitié-Salpêtrière, 47 boulevard de l'Hôpital, F-75013, Paris, France yworbe@gmail.com.
Yulia
Y
Worbe
D000328:Adult; D001921:Brain / Q000502:physiology*; D005260:Female; D006184:Habits; D006801:Humans; D008297:Male; D009415:Nerve Net / Q000502:physiology*; D011597:Psychomotor Performance / Q000502:physiology*; D005879:Tourette Syndrome / Q000175:diagnosis* / Q000523:psychology*
Gilles de la Tourette syndrome; dopamine; goal-directed behaviour; habitual behaviour; structural connectivity of cortico-striatal networks