Evidence suggests that Tourette syndrome is characterized by an increase in dopamine transmission and structural as well as functional changes in fronto-striatal circuits that might lead to enhanced multi-component behaviour integration. Behavioural and neurophysiological data regarding multi-component behaviour was collected from 15 patients with Tourette syndrome (mean age = 30.40 ± 11.10) and 15 healthy controls (27.07 ± 5.44), using the stop-change task. In this task, participants are asked to sometimes withhold responses to a Go stimulus (stop cue) and change hands to respond to an alternative Go stimulus (change cue). Different onset asynchronies between stop and change cues were implemented (0 and 300 ms) in order to vary task difficulty. Tourette patients responded more accurately than healthy controls when there was no delay between stop and change stimulus, while there was no difference in the 300 ms delay condition. This performance advantage was reflected in a smaller P3 event related potential. Enhanced multi-component behaviour in Tourette syndrome is likely based on an enhanced ability to integrate information from multiple sources and translate it into an appropriate response sequence. This may be a consequence of chronic tic control in these patients, or a known fronto-striatal networks hyperconnectivity in Tourette syndrome.

Cognitive Neurophysiology Department of Child and Adolescent Psychiatry Faculty of Medicine of the TU Dresden Dresden Germany

Department of Paediatric and Adult Movement Disorders and Neuropsychiatry Institute of Neurogenetics Center for Brain Behaviour and Metabolism University of Lübeck Lübeck Germany

Department of Psychology Centre for Innovation in Mental Health University of Southampton Southampton UK

Experimental Neurobiology National Institute of Mental Health Klecany Czech Republic

See more in PubMed

Diagnostic and statistical manual of mental disorders: DSM-5. (American Psychiatric Publ, 2013). PubMed

Worbe Y, et al. Functional immaturity of cortico-basal ganglia networks in Gilles de la Tourette syndrome. Brain J. Neurol. 2012;135:1937–1946. doi: 10.1093/brain/aws056. PubMed DOI

Worbe Y, et al. Distinct structural changes underpin clinical phenotypes in patients with Gilles de la Tourette syndrome. Brain J. Neurol. 2010;133:3649–3660. doi: 10.1093/brain/awq293. PubMed DOI

Worbe Y, et al. Altered structural connectivity of cortico-striato-pallido-thalamic networks in Gilles de la Tourette syndrome. Brain J. Neurol. 2015;138:472–482. doi: 10.1093/brain/awu311. PubMed DOI PMC

Ganos C, Roessner V, Münchau A. The functional anatomy of Gilles de la Tourette syndrome. Neurosci. Biobehav. Rev. 2013;37:1050–1062. doi: 10.1016/j.neubiorev.2012.11.004. PubMed DOI

Verbruggen F, Schneider DW, Logan GD. How to stop and change a response: the role of goal activation in multitasking. J. Exp. Psychol. Hum. Percept. Perform. 2008;34:1212–1228. doi: 10.1037/0096-1523.34.5.1212. PubMed DOI

Beste C, Saft C. Action selection in a possible model of striatal medium spiny neuron dysfunction: behavioral and EEG data in a patient with benign hereditary chorea. Brain Struct. Funct. 2015;220:221–228. doi: 10.1007/s00429-013-0649-9. PubMed DOI

Mückschel M, Stock A-K, Beste C. Psychophysiological mechanisms of interindividual differences in goal activation modes during action cascading. Cereb. Cortex N. Y. N 1991. 2014;24:2120–2129. PubMed

Stock A-K, Arning L, Epplen JT, Beste C. DRD1 and DRD2 genotypes modulate processing modes of goal activation processes during action cascading. J. Neurosci. Off. J. Soc. Neurosci. 2014;34:5335–5341. doi: 10.1523/JNEUROSCI.5140-13.2014. PubMed DOI PMC

Stock A-K, Heintschel von Heinegg E, Köhling H-L, Beste C. Latent Toxoplasma gondii infection leads to improved action control. Brain. Behav. Immun. 2014;37:103–108. doi: 10.1016/j.bbi.2013.11.004. PubMed DOI

van Thriel, C. et al. Are multitasking abilities impaired in welders exposed to manganese? Translating cognitive neuroscience to neurotoxicology. Arch. Toxicol., doi:10.1007/s00204-017-1932-y (2017). PubMed

Yildiz A, et al. Feeling safe in the plane: neural mechanisms underlying superior action control in airplane pilot trainees–a combined EEG/MRS study. Hum. Brain Mapp. 2014;35:5040–5051. doi: 10.1002/hbm.22530. PubMed DOI PMC

Duncan J. The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour. Trends Cogn. Sci. 2010;14:172–179. doi: 10.1016/j.tics.2010.01.004. PubMed DOI

Gohil K, Stock A-K, Beste C. The importance of sensory integration processes for action cascading. Sci. Rep. 2015;5:9485. doi: 10.1038/srep09485. PubMed DOI PMC

Beste C, Dziobek I, Hielscher H, Willemssen R, Falkenstein M. Effects of stimulus-response compatibility on inhibitory processes in Parkinson’s disease. Eur. J. Neurosci. 2009;29:855–860. doi: 10.1111/j.1460-9568.2009.06621.x. PubMed DOI

Beste C, et al. Mechanisms mediating parallel action monitoring in fronto-striatal circuits. NeuroImage. 2012;62:137–146. doi: 10.1016/j.neuroimage.2012.05.019. PubMed DOI

McKinlay A, Grace RC, Dalrymple-Alford JC, Roger D. Characteristics of executive function impairment in Parkinson’s disease patients without dementia. J. Int. Neuropsychol. Soc. JINS. 2010;16:268–277. doi: 10.1017/S1355617709991299. PubMed DOI

Willemssen R, Falkenstein M, Schwarz M, Müller T, Beste C. Effects of aging, Parkinson’s disease, and dopaminergic medication on response selection and control. Neurobiol. Aging. 2011;32:327–335. doi: 10.1016/j.neurobiolaging.2009.02.002. PubMed DOI

Cameron IGM, Watanabe M, Pari G, Munoz DP. Executive impairment in Parkinson’s disease: response automaticity and task switching. Neuropsychologia. 2010;48:1948–1957. doi: 10.1016/j.neuropsychologia.2010.03.015. PubMed DOI

Ravizza SM, Goudreau J, Delgado MR, Ruiz S. Executive function in Parkinson’s disease: contributions of the dorsal frontostriatal pathways to action and motivation. Cogn. Affect. Behav. Neurosci. 2012;12:193–206. doi: 10.3758/s13415-011-0066-6. PubMed DOI

Gohil K, Dippel G, Beste C. Questioning the role of the frontopolar cortex in multi-component behavior–a TMS/EEG study. Sci. Rep. 2016;6:22317. doi: 10.1038/srep22317. PubMed DOI PMC

Stock A-K, Gohil K, Beste C. Blocking effects in non-conditioned goal-directed behaviour. Brain Struct. Funct. 2017 PubMed

Buse J, Schoenefeld K, Münchau A, Roessner V. Neuromodulation in Tourette syndrome: dopamine and beyond. Neurosci. Biobehav. Rev. 2013;37:1069–1084. doi: 10.1016/j.neubiorev.2012.10.004. PubMed DOI

Ernst M, et al. High presynaptic dopaminergic activity in children with Tourette’s disorder. J. Am. Acad. Child Adolesc. Psychiatry. 1999;38:86–94. doi: 10.1097/00004583-199901000-00024. PubMed DOI

Wong DF, et al. Mechanisms of dopaminergic and serotonergic neurotransmission in Tourette syndrome: clues from an in vivo neurochemistry study with PET. Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 2008;33:1239–1251. doi: 10.1038/sj.npp.1301528. PubMed DOI PMC

Singer HS, Hahn IH, Moran TH. Abnormal dopamine uptake sites in postmortem striatum from patients with Tourette’s syndrome. Ann. Neurol. 1991;30:558–562. doi: 10.1002/ana.410300408. PubMed DOI

Singer HS, et al. Elevated intrasynaptic dopamine release in Tourette’s syndrome measured by PET. Am. J. Psychiatry. 2002;159:1329–1336. doi: 10.1176/appi.ajp.159.8.1329. PubMed DOI

Stock A-K, Ness V, Beste C. Complex sensorimotor transformation processes required for response selection are facilitated by the striatum. NeuroImage. 2015;123:33–41. doi: 10.1016/j.neuroimage.2015.08.036. PubMed DOI

Verleger R, Jaśkowski P, Wascher E. Evidence for an Integrative Role of P3b in Linking Reaction to Perception. J. Psychophysiol. 2005;19:165–181. doi: 10.1027/0269-8803.19.3.165. DOI

Chudasama Y, Robbins TW. Functions of frontostriatal systems in cognition: comparative neuropsychopharmacological studies in rats, monkeys and humans. Biol. Psychol. 2006;73:19–38. doi: 10.1016/j.biopsycho.2006.01.005. PubMed DOI

Redgrave P, Vautrelle N, Reynolds JNJ. Functional properties of the basal ganglia’s re-entrant loop architecture: selection and reinforcement. Neuroscience. 2011;198:138–151. doi: 10.1016/j.neuroscience.2011.07.060. PubMed DOI

Redgrave P, et al. Goal-directed and habitual control in the basal ganglia: implications for Parkinson’s disease. Nat. Rev. Neurosci. 2010;11:760–772. doi: 10.1038/nrn2915. PubMed DOI PMC

Ness V, Beste C. The role of the striatum in goal activation of cascaded actions. Neuropsychologia. 2013;51:2562–2571. doi: 10.1016/j.neuropsychologia.2013.09.032. PubMed DOI

Verleger R, Schroll H, Hamker FH. The unstable bridge from stimulus processing to correct responding in Parkinson’s disease. Neuropsychologia. 2013;51:2512–2525. doi: 10.1016/j.neuropsychologia.2013.09.017. PubMed DOI

Herrmann CS, Knight RT. Mechanisms of human attention: event-related potentials and oscillations. Neurosci. Biobehav. Rev. 2001;25:465–476. doi: 10.1016/S0149-7634(01)00027-6. PubMed DOI

Jackson GM, Mueller SC, Hambleton K, Hollis CP. Enhanced cognitive control in Tourette Syndrome during task uncertainty. Exp. Brain Res. 2007;182:357–364. doi: 10.1007/s00221-007-0999-8. PubMed DOI

Mueller SC, Jackson GM, Dhalla R, Datsopoulos S, Hollis CP. Enhanced cognitive control in young people with Tourette’s syndrome. Curr. Biol. CB. 2006;16:570–573. doi: 10.1016/j.cub.2006.01.064. PubMed DOI

Serrien DJ, Orth M, Evans AH, Lees AJ, Brown P. Motor inhibition in patients with Gilles de la Tourette syndrome: functional activation patterns as revealed by EEG coherence. Brain J. Neurol. 2005;128:116–125. doi: 10.1093/brain/awh318. PubMed DOI

Peterson BS, et al. A functional magnetic resonance imaging study of tic suppression in Tourette syndrome. Arch. Gen. Psychiatry. 1998;55:326–333. doi: 10.1001/archpsyc.55.4.326. PubMed DOI

Falup-Pecurariu, C., Ferreira, J., Martinez-Martin, P. & Chaudhuri, K. R. Movement disorders curricula (2017).

Dippel G, Beste C. A causal role of the right inferior frontal cortex in implementing strategies for multi-component behaviour. Nat. Commun. 2015;6:6587. doi: 10.1038/ncomms7587. PubMed DOI

Frank MJ, Doll BB, Oas-Terpstra J, Moreno F. Prefrontal and striatal dopaminergic genes predict individual differences in exploration and exploitation. Nat. Neurosci. 2009;12:1062–1068. doi: 10.1038/nn.2342. PubMed DOI PMC

Humphries MD, Stewart RD, Gurney KN. A physiologically plausible model of action selection and oscillatory activity in the basal ganglia. J. Neurosci. Off. J. Soc. Neurosci. 2006;26:12921–12942. doi: 10.1523/JNEUROSCI.3486-06.2006. PubMed DOI PMC

Meyer P, et al. Striatal presynaptic monoaminergic vesicles are not increased in Tourette’s syndrome. Neurology. 1999;53:371–374. doi: 10.1212/WNL.53.2.371. PubMed DOI

Albin RL, et al. Striatal [11C]dihydrotetrabenazine and [11C]methylphenidate binding in Tourette syndrome. Neurology. 2009;72:1390–1396. doi: 10.1212/WNL.0b013e3181a187dd. PubMed DOI PMC

Ben-Dor DH, et al. Reduced platelet vesicular monoamine transporter density in Tourette’s syndrome pediatric male patients. Eur. Neuropsychopharmacol. J. Eur. Coll. Neuropsychopharmacol. 2007;17:523–526. doi: 10.1016/j.euroneuro.2007.01.002. PubMed DOI

Müller-Vahl KR, et al. Dopamine D2 receptor imaging in Gilles de la Tourette syndrome. Acta Neurol. Scand. 2000;101:165–171. doi: 10.1034/j.1600-0404.2000.101003165.x. PubMed DOI

Müller-Vahl KR, et al. Dopamine transporter binding in Gilles de la Tourette syndrome. J. Neurol. 2000;247:514–520. doi: 10.1007/PL00007806. PubMed DOI

Roessner V, et al. European clinical guidelines for Tourette syndrome and other tic disorders. Part II: pharmacological treatment. Eur. Child Adolesc. Psychiatry. 2011;20:173–196. doi: 10.1007/s00787-011-0163-7. PubMed DOI PMC

Gilbert DL, Budman CL, Singer HS, Kurlan R, Chipkin RE. A D1 receptor antagonist, ecopipam, for treatment of tics in Tourette syndrome. Clin. Neuropharmacol. 2014;37:26–30. PubMed

Yoon DY, Gause CD, Leckman JF, Singer HS. Frontal dopaminergic abnormality in Tourette syndrome: a postmortem analysis. J. Neurol. Sci. 2007;255:50–56. doi: 10.1016/j.jns.2007.01.069. PubMed DOI

Leckman JF, et al. The Yale Global Tic Severity Scale: initial testing of a clinician-rated scale of tic severity. J. Am. Acad. Child Adolesc. Psychiatry. 1989;28:566–573. doi: 10.1097/00004583-198907000-00015. PubMed DOI

Rösler M, et al. Instrumente zur Diagnostik der Aufmerksamkeitsdefizit-/Hyperaktivitätsstörung (ADHS) im Erwachsenenalter: Selbstbeurteilungsskala (ADHS-SB) und Diagnosecheckliste (ADHS-DC) Nervenarzt. 2005;76:129–130. doi: 10.1007/s00115-004-1848-7. PubMed DOI

Foa EB, et al. The Obsessive-Compulsive Inventory: development and validation of a short version. Psychol. Assess. 2002;14:485–496. doi: 10.1037/1040-3590.14.4.485. PubMed DOI

Brandt VC, Beck C, Sajin V, Anders S, Münchau A. Convergent Validity of the PUTS. Front. Psychiatry. 2016;7:51. doi: 10.3389/fpsyt.2016.00051. PubMed DOI PMC

Woods DW, Piacentini J, Himle MB, Chang S. Premonitory Urge for Tics Scale (PUTS): initial psychometric results and examination of the premonitory urge phenomenon in youths with Tic disorders. J. Dev. Behav. Pediatr. JDBP. 2005;26:397–403. doi: 10.1097/00004703-200512000-00001. PubMed DOI

Gratton G, Coles MG, Donchin E. A new method for off-line removal of ocular artifact. Electroencephalogr. Clin. Neurophysiol. 1983;55:468–484. doi: 10.1016/0013-4694(83)90135-9. PubMed DOI

Perrin F, Pernier J, Bertrand O, Echallier JF. Spherical splines for scalp potential and current density mapping. Electroencephalogr. Clin. Neurophysiol. 1989;72:184–187. doi: 10.1016/0013-4694(89)90180-6. PubMed DOI

Beste C, et al. Functional 5-HT1a receptor polymorphism selectively modulates error-specific subprocesses of performance monitoring. Hum. Brain Mapp. 2010;31:621–630. PubMed PMC

Beste C, et al. The role of the BDNF Val66Met polymorphism for the synchronization of error-specific neural networks. J. Neurosci. Off. J. Soc. Neurosci. 2010;30:10727–10733. doi: 10.1523/JNEUROSCI.2493-10.2010. PubMed DOI PMC

Nunez PL, Pilgreen KL. The spline-Laplacian in clinical neurophysiology: a method to improve EEG spatial resolution. J. Clin. Neurophysiol. Off. Publ. Am. Electroencephalogr. Soc. 1991;8:397–413. PubMed