[en] 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.
Disciplines :
Neurology Radiology, nuclear medicine & imaging
Author, co-author :
Bohlhalter, Stephan; Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA
Goldfine, Andrew; Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA
Matteson, S.; Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA
Garraux, Gaëtan ; Université de Liège - ULiège & Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA
Hanakawa, Takashi; Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA
Kansaku, Kenji; Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA
Wurzman, Rachel; Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA
Hallett, Mark; Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA
Language :
English
Title :
Neural correlates of tic generation in Tourette syndrome: an event-related functional MRI study.
Adler CM, McDonough-Ryan P, Sax KW, Holland SK, Arndt S, Strakowski SM. fMRI of neuronal activation with symptom provocation in unmedicated patients with obsessive compulsive disorder. J Psychiatr Res 2000; 34: 317-24.
Amyes EW, Nielsen JM. Bilateral anterior cingulate gyrus lesions; report of case. Bull Los Angel Neuro Soc 1953; 18: 48-51.
Augustine JR. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 1996; 22: 229-44.
Aziz Q, Andersson JL, Valind S, Sundin A, Hamdy S, Jones AK, et al. Identification of human brain loci processing esophageal sensation using positron emission tomography. Gastroenterology 1997; 113: 50-9.
Ball T, Schreiber A, Feige B, Wagner M, Lucking CH, Kristeva-Feige R. The role of higher-order motor areas in voluntary movement as revealed by high-resolution EEG and fMRI. Neuroimage 1999; 10: 682-94.
Bancaud J, Talairach J, Geier S, Bonis A, Trottier S, Manrique M. Behavioral manifestations induced by electric stimulation of the anterior cingulate gyrus in man. Rev Neurol (Paris) 1976; 132: 705-24.
Barris RW, Schuman HR. Bilateral anterior cingulate gyrus lesions; syndrome of the anterior cingulate gyri. Neurology 1953; 3: 44-52.
Berardelli A, Curra A, Fabbrini G, Gilio F, Manfredi M. Pathophysiology of tics and Tourette syndrome. J Neurol 2003; 250: 781-7.
Biswal B, Ulmer J, Krippendorf R, Harsch H, Daniels D, Hyde J, et al. Abnormal cerebral activation associated with a motor task in Tourette syndrome. AJNR Am J Neuroradiol 1998; 19: 1509-12.
Braun AR, Stoetter B, Randolph C, Hsiao JK, Vladar K, Gernert J, et al. The functional neuroanatomy of Tourette's syndrome: an FDG-PET study. I. Regional changes in cerebral glucose metabolism differentiating patients and controls. Neuropsychopharmacology 1993; 9: 277-91.
Castellanos FX, Fine EJ, Kaysen D, Marsh WL, Rapoport JL, Hallett M. Sensorimotor gating in boys with Tourette's syndrome and ADHD: preliminary results. Biol Psychiatry 1996; 39: 33-41.
Cunnington R, Windischberger C, Deecke L, Moser E. The preparation and execution of self-initiated and externally-triggered movement: a study of event-related fMRI. Neuroimage 2002; 15: 373-85.
Cunnington R, Windischberger C, Deecke L, Moser E. The preparation and readiness for voluntary movement: a high-field event-related fMRI study of the Bereitschafts-BOLD response. Neuroimage 2003; 20: 404-12.
Deecke L, Kornhuber HH. An electrical sign of participation of the mesial 'supplementary' motor cortex in human voluntary finger movement. Brain Res 1978; 159: 473-6.
Deiber MP, Honda M, Ibanez V, Sadato N, Hallett M. Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate. J Neurophysiol 1999; 81: 3065-77.
Derbyshire SWG, Whalley MG, Stenger VA, Oakley DA. Cerebral activation during hypnotically induced and imagined pain. Neuroimage 2004; 23: 392-401.
Eidelberg D, Moeller J, Antonini A, Kazumata K, Dhawan V, Budman C, et al. The metabolic anatomy of Tourette's syndrome. Neurology 1997; 48: 927-34.
Freeman RD, Fast DK, Burd L, Kerbeshian J, Robertson MM, Sandor P. An international perspective on Tourette syndrome: selected findings from 3,500 individuals in 22 countries. Dev Med Child Neurol 2000; 42: 436-47.
Fried I, Katz A, McCarthy G, Sass KJ, Williamson P, Spencer S, et al. Functional organization of human supplementary motor cortex studied by electrical stimulation. J Neurosci 1991; 11: 3656-66.
Friston KJ, Holmes AP, Poline JB, Grasby PJ, Williams SC, Frackowiak RS, et al. Analysis of fMRI time-series revisited. Neuroimage 1995; 2: 45-53.
Genovese CR, Lazar NA, Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 2002; 15: 870-8.
Georgiou N, Bradshaw J, Phillips J, Bradshaw J, Chiu E. The Simon effect and attention deficits in Gilles de la Tourette's syndrome and Huntington's disease. Brain 1995a; 118: 1305-18.
Georgiou N, Bradshaw JL, Phillips JG, Bradshaw JA, Chiu E. Advance information and movement sequencing in Gilles de la Tourette's syndrome. J Neurol Neurosurg Psychiatry 1995b; 58: 184-91.
Gironell A, Rodriguez-Fornells A, Kulisevsky J, Pascual B, Riba J, Barbanoj M, et al. Abnormalities of the acoustic startle reflex and reaction time in Gilles de la Tourette syndrome. Clin Neurophysiol 2000; 111: 1366-71.
Hallett M. Neurophysiology of tics. In: Cohen DJ, Goetz CG, Jankovic J, editors. Tourette syndrome. Philadelphia: Lippincott, Williams and Wilkins; 2001. p. 237-44.
Hornse H, Banerjee S, Zeitlin H, Robertson M. The prevalence of Tourette syndrome in 13-14-year-olds in mainstream schools. J Child Psychol Psychiatry 2001; 42: 1035-9.
Hsieh JC, Hagermark O, Stahle-Backdahl M, Ericson K, Eriksson L, Stone-Elander S, et al. Urge to scratch represented in the human cerebral cortex during itch. J Neurophysiol 1994; 72: 3004-8.
Hulsmann E, Erb M, Grodd W. From will to action: sequential cerebellar contributions to voluntary movement. Neuroimage 2003; 20: 1485-92.
Ikeda A, Luders HO, Burgess RC, Shibasaki H. Movement-related potentials recorded from supplementary motor area and primary motor area. Role of supplementary motor area in voluntary movements. Brain 1992; 115: 1017-43.
Ikeda A, Yazawa S, Kunieda T, Ohara S, Terada K, Mikuni N, et al. Cognitive motor control in human pre-supplementary motor area studied by subdural recording of discrimination/selection-related potentials. Brain 1999; 122: 915-31.
Isnard J, Guenot M, Sindou M, Mauguiere F. Clinical manifestations of insular lobe seizures: a stereo-electroencephalographic study. Epilepsia 2004; 45: 1079-90.
Jahanshahi M, Jenkins I, Brown R, Marsden C, Passingham R, Brooks D. Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson's disease subjects. Brain 1995; 118: 913-33.
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.
Karp B, Porter S, Toro C, Hallett M. Simple motor tics may be preceded by a premotor potential. J Neurol Neurosurg Psychiatry 1996; 61: 103-6.
Kwan CL, Crawley AP, Mikulis DJ, Davis KD. An fMRI study of the anterior cingulate cortex and surrounding medial wall activations evoked by noxious cutaneous heat and cold stimuli. Pain 2000; 85: 359-74.
Laplane D, Degos JD, Baulac M, Gray F. Bilateral infarction of the anterior cingulate gyri and of the fornices. Report of a case. J Neurol Sci 1981; 51: 289-300.
Le Moal M, Simon H. Mesocorticolimbic dopaminergic network: functional and regulatory roles. Physiol Rev 1991; 71: 155-234.
Leuthold H, Jentzsch I. Neural correlates of advance movement preparation: a dipole source analysis approach. Brain Res Cogn Brain Res 2001; 12: 207-24.
Lim SH, Dinner DS, Pillay PK, Luders H, Morris HH, Klem G, et al. Functional anatomy of the human supplementary sensorimotor area: results of extraoperative electrical stimulation. Electroencephalogr Clin Neurophysiol 1994; 91: 179-93.
Lindvall O, Bjorklund A, Moore RY, Stenevi U. Mesencephalic dopamine neurons projecting to neocortex. Brain Res 1974; 81: 325-31.
Lu C-L, Wu Y-T, Yeh T-C, Chen L-F, Chang F-Y, Lee S-D, et al. Neuronal correlates of gastric pain induced by fundus distension: a 3T-fMRI study. Neurogastroenterol Motil 2004; 16: 575-87.
MacDonald PA, Paus T. The role of parietal cortex in awareness of self-generated movements: a transcranial magnetic stimulation study. Cereb Cortex 2003; 13: 962-7.
Mochizuki H, Tashiro M, Kano M, Sakurada Y, Itoh M, Yanai K. Imaging of central itch modulation in the human brain using positron emission tomography. Pain 2003; 105: 339-46.
Nemeth G, Hegedus K, Molnar L. Akinetic mutism associated with bicingular lesions: clinicopathological and functional anatomical correlates. Eur Arch Psychiatry Neurol Sci 1988; 237: 218-22.
Nowak DA, Rothwell J, Topka H, Robertson MM, Orth M. Grip force behavior in Gilles de la Tourette syndrome. Mov Disord 2005; 20: 217-23.
Obeso J, Rothwell J, Marsden C. Simple tics in Gilles de la Tourette's syndrome are not prefaced by a normal premovement EEG potential. J Neurol Neurosurg Psychiatry 1981; 44: 735-8.
Ostrowsky K, Magnin M, Ryvlin P, Isnard J, Guenot M, Mauguiere F. Representation of pain and somatic sensation in the human insula: a study of responses to direct electrical cortical stimulation. Cereb Cortex 2002; 12: 376-85.
Peterson BS, Skudlarski P, Anderson AW, Zhang H, Gatenby JC, Lacadie CM, et al. A functional magnetic resonance imaging study of tic suppression in Tourette syndrome. Arch Gen Psychiatry 1998; 55: 326-33.
Picard N, Strick PL. Imaging the premotor areas. Curr Opin Neurobiol 2001; 11: 663-72.
Rauch SL, Jenike MA, Alpert NM, Baer L, Breiter HC, Savage CR, et al. Regional cerebral blood flow measured during symptom provocation in obsessive-compulsive disorder using oxygen 15-labeled carbon dioxide and positron emission tomography. Arch Gen Psychiatry 1994; 51: 62-70.
Serrien DJ, Nirkko AC, Loher TJ, Lovblad K-O, Burgunder J-M, Wiesendanger M. Movement control of manipulative tasks in patients with Gilles de la Tourette syndrome. Brain 2002; 125: 290-300.
Shucard DW, Benedict RH, Tekok-Kilic A, Lichter DG. Slowed reaction time during a continuous performance test in children with Tourette's syndrome. Neuropsychology 1997; 11: 147-55.
Stern E, Silbersweig DA, Chee K-Y, Holmes A, Robertson MM, Trimble M, et al. A functional neuroanatomy of tics in Tourette syndrome. Arch Gen Psychiatry 2000; 57: 741-8.
Stern JS, Burza S, Robertson MM. Gilles de la Tourette's syndrome and its impact in the UK. Postgrad Med J 2005; 81: 12-19.
Swerdlow NR, Karban B, Ploum Y, Sharp R, Geyer MA, Eastvold A. Tactile prepuff inhibition of startle in children with Tourette's syndrome: in search of an 'fMRI-friendly' startle paradigm. Biol Psychiatry 2001; 50: 578-85.
Talairach J, Bancaud J, Geier S, Bordas-Ferrer M, Bonis A, Szikla G, et al. The cingulate gyrus and human behaviour. Electroencephalogr Clin Neurophysiol 1973; 34: 45-52.
Talairach J, Tournoux P. Co-planar stereotaxic atlas of the human brain. New York: Thieme Medical Publishers; 1988.
Tolle TR, Kaufmann T, Siessmeier T, Lautenbacher S, Berthele A, Munz F, et al. Region-specific encoding of sensory and affective components of pain in the human brain: a positron emission tomography correlation analysis. Ann Neurol 1999; 45: 40-7.
Toma K, Matsuoka T, Immisch I, Mima T, Waldvogel D, Koshy B, et al. Generators of movement-related cortical potentials: fMRI-constrained EEG dipole source analysis. Neuroimage 2002; 17: 161-73.
Weilke F, Spiegel S, Boecker H, von Einsiedel HG, Conrad B, Schwaiger M, et al. Time-resolved fMRI of activation patterns in M1 and SMA during complex voluntary movement. J Neurophysiol 2001; 85: 1858-63.
Winterer G, Adams CM, Jones DW, Knutson B. Volition to action - an event-related fMRI study. Neuroimage 2002; 17: 851-8.
Ziemann U, Paulus W, Rothenberger A. Decreased motor inhibition in Tourette's disorder: evidence from transcranial magnetic stimulation. Am J Psychiatry 1997; 154: 1277-84.