Background In Gilles de la Tourette syndrome (GTS) increased activation of the primary motor cortex (M1) before and during movement execution followed by increased inhibition after movement termination was reported. The present study aimed at investigating, whether this activation pattern is due to altered functional interaction between motor cortical areas. Methodology/Principal Findings 10 GTS-patients and 10 control subjects performed a self-paced finger movement task while neuromagnetic brain activity was recorded using Magnetoencephalography (MEG). Cerebro-cerebral coherence as a measure of functional interaction was calculated. During movement preparation and execution coherence between contralateral M1 and supplementary motor area (SMA) was significantly increased at beta-frequency in GTS-patients. After movement termination no significant differences between groups were evident. Conclusions/Significance The present data suggest that increased M1 activation in GTS-patients might be due to increased functional interaction between SMA and M1 most likely reflecting a pathophysiological marker of GTS. The data extend previous findings of motor-cortical alterations in GTS by showing that local activation changes are associated with alterations of functional networks between premotor and primary motor areas. Interestingly enough, alterations were evident during preparation and execution of voluntary movements, which implies a general theme of increased motor-cortical interaction in GTS.
References
[1]
Leckman JF, Riddle MA (2000) Tourette's syndrome: when habit-forming systems form habits of their own? Neuron 28: 349–354.
[2]
Paszek J, Pollok B, Biermann-Ruben K, Muller-Vahl K, Roessner V, et al. (2010) Is it a tic?–Twenty seconds to make a diagnosis. Mov Disord 25: 1106–1108.
[3]
Kwak C, Dat Vuong K, Jankovic J (2003) Premonitory sensory phenomenon in Tourette's syndrome. Mov Disord 18: 1530–1533.
[4]
Mink JW (2006) Neurobiology of basal ganglia and Tourette syndrome: basal ganglia circuits and thalamocortical outputs. Adv Neurol 99: 89–98.
[5]
Stern E, Silbersweig DA, Chee KY, Holmes A, Robertson MM, et al. (2000) A functional neuroanatomy of tics in Tourette syndrome. Arch Gen Psychiatry 57: 741–748.
[6]
Mink JW (2001) Basal ganglia dysfunction in Tourette's syndrome: a new hypothesis. Pediatr Neurol 25: 190–198.
[7]
Hampson M, Tokoglu F, King RA, Constable RT, Leckman JF (2009) Brain areas coactivating with motor cortex during chronic motor tics and intentional movements. Biol Psychiatry 65: 594–599.
[8]
Serrien DJ, Orth M, Evans AH, Lees AJ, Brown P (2005) Motor inhibition in patients with Gilles de la Tourette syndrome: functional activation patterns as revealed by EEG coherence. Brain 128: 116–125.
[9]
Bohlhalter S, Goldfine A, Matteson S, Garraux G, Hanakawa T, et al. (2006) Neural correlates of tic generation in Tourette syndrome: an event-related functional MRI study. Brain 129: 2029–2037.
[10]
Ziemann U, Paulus W, Rothenberger A (1997) Decreased motor inhibition in Tourette's disorder: evidence from transcranial magnetic stimulation. Am J Psychiatry 154: 1277–1284.
[11]
Orth M, Amann B, Robertson MM, Rothwell JC (2005) Excitability of motor cortex inhibitory circuits in Tourette syndrome before and after single dose nicotine. Brain 128: 1292–1300.
[12]
Moll GH, Wischer S, Heinrich H, Tergau F, Paulus W, et al. (1999) Deficient motor control in children with tic disorder: evidence from transcranial magnetic stimulation. Neurosci Lett 272: 37–40.
[13]
Gilbert DL, Bansal AS, Sethuraman G, Sallee FR, Zhang J, et al. (2004) Association of cortical disinhibition with tic, ADHD, and OCD severity in Tourette syndrome. Mov Disord 19: 416–425.
[14]
Orth M, Munchau A, Rothwell JC (2008) Corticospinal system excitability at rest is associated with tic severity in tourette syndrome. Biol Psychiatry 64: 248–251.
[15]
Franzkowiak S, Pollok B, Biermann-Ruben K, Sudmeyer M, Paszek J, et al. (2010) Altered pattern of motor cortical activation-inhibition during voluntary movements in Tourette syndrome. Mov Disord 25: 1960–1966.
[16]
Biswal B, Ulmer JL, Krippendorf RL, Harsch HH, Daniels DL, et al. (1998) Abnormal cerebral activation associated with a motor task in Tourette syndrome. AJNR Am J Neuroradiol 19: 1509–1512.
[17]
Fattapposta F, Restuccia R, Colonnese C, Labruna L, Garreffa G, et al. (2005) Gilles de la Tourette syndrome and voluntary movement: a functional MRI study. Psychiatry Res 138: 269–272.
[18]
Gross J, Kujala J, Hamalainen M, Timmermann L, Schnitzler A, et al. (2001) Dynamic imaging of coherent sources: Studying neural interactions in the human brain. Proc Natl Acad Sci U S A 98: 694–699.
[19]
Schnitzler A, Gross J (2005) Normal and pathological oscillatory communication in the brain. Nat Rev Neurosci 6: 285–296.
[20]
Robertson MM, Banerjee S, Kurlan R, Cohen DJ, Leckman JF, et al. (1999) The Tourette syndrome diagnostic confidence index: development and clinical associations. Neurology 53: 2108–2112.
[21]
Leckman JF, Riddle MA, Hardin MT, Ort SI, Swartz KL, et al. (1989) The Yale Global Tic Severity Scale: initial testing of a clinician-rated scale of tic severity. J Am Acad Child Adolesc Psychiatry 28: 566–573.
[22]
Goetz CG, Pappert EJ, Louis ED, Raman R, Leurgans S (1999) Advantages of a modified scoring method for the Rush Video-Based Tic Rating Scale. Mov Disord 14: 502–506.
[23]
Adler L, Kessler R, Spencer T (2003) Adult ADHD Self-Report Scale-v1.1 (ASRS-v1.1) Symptom Checklist. New York, NY: World Health Organization.
[24]
Retz-Junginger P, Retz W, Blocher D, Weijers HG, Trott GE, et al. (2002) [Wender Utah rating scale. The short-version for the assessment of the attention-deficit hyperactivity disorder in adults]. Nervenarzt 73: 830–838.
[25]
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9: 97–113.
[26]
Jurkiewicz MT, Gaetz WC, Bostan AC, Cheyne D (2006) Post-movement beta rebound is generated in motor cortex: evidence from neuromagnetic recordings. Neuroimage 32: 1281–1289.
[27]
Chen R, Yaseen Z, Cohen LG, Hallett M (1998) Time course of corticospinal excitability in reaction time and self-paced movements. Ann Neurol 44: 317–325.
[28]
Holm S (1979) A Simple Sequentially Rejective Multiple Test Procedure. Scand J Statist 6: 65–70.
[29]
Rosenblum MG, Pikovsky AS (2001) Detecting direction of coupling in interacting oscillators. Phys Rev E Stat Nonlin Soft Matter Phys 64: 045202.
[30]
Salmelin R, Hamalainen M, Kajola M, Hari R (1995) Functional segregation of movement-related rhythmic activity in the human brain. Neuroimage 2: 237–243.
[31]
Ritter P, Moosmann M, Villringer A (2009) Rolandic alpha and beta EEG rhythms' strengths are inversely related to fMRI-BOLD signal in primary somatosensory and motor cortex. Hum Brain Mapp 30: 1168–1187.
[32]
Deecke L, Weinberg H, Brickett P (1982) Magnetic fields of the human brain accompanying voluntary movement: Bereitschaftsmagnetfeld. Exp Brain Res 48: 144–148.
[33]
Praamstra P, Stegeman DF, Horstink MW, Cools AR (1996) Dipole source analysis suggests selective modulation of the supplementary motor area contribution to the readiness potential. Electroencephalogr Clin Neurophysiol 98: 468–477.
[34]
Gerloff C, Richard J, Hadley J, Schulman AE, Honda M, et al. (1998) Functional coupling and regional activation of human cortical motor areas during simple, internally paced and externally paced finger movements. Brain 121: 1513–1531.
[35]
Ohara S, Mima T, Baba K, Ikeda A, Kunieda T, et al. (2001) Increased synchronization of cortical oscillatory activities between human supplementary motor and primary sensorimotor areas during voluntary movements. J Neurosci 21: 9377–9386.
[36]
Myers LJ, Mackinnon CD (2004) The time course of functional coupling between human cortical motor areas during internally driven vs. externally cued movements. Conf Proc IEEE Eng Med Biol Soc 6: 4669–4672.
[37]
Serrien DJ, Nirkko AC, Loher TJ, Lovblad KO, Burgunder JM, et al. (2002) Movement control of manipulative tasks in patients with Gilles de la Tourette syndrome. Brain 125: 290–300.
[38]
Mantovani A, Leckman JF, Grantz H, King RA, Sporn AL, et al. (2007) Repetitive Transcranial Magnetic Stimulation of the Supplementary Motor Area in the treatment of Tourette Syndrome: report of two cases. Clin Neurophysiol 118: 2314–2315.
[39]
Mantovani A, Lisanby SH, Pieraccini F, Ulivelli M, Castrogiovanni P, et al. (2006) Repetitive transcranial magnetic stimulation (rTMS) in the treatment of obsessive-compulsive disorder (OCD) and Tourette's syndrome (TS). Int J Neuropsychopharmacol 9: 95–100.
[40]
Heise KF, Steven B, Liuzzi G, Thomalla G, Jonas M, et al. (2010) Altered modulation of intracortical excitability during movement preparation in Gilles de la Tourette syndrome. Brain 133: 580–590.
[41]
Hall SD, Stanford IM, Yamawaki N, McAllister CJ, Ronnqvist KC, et al. (2011) The role of GABAergic modulation in motor function related neuronal network activity. Neuroimage 56: 1506–1510.
[42]
Thomalla G, Siebner HR, Jonas M, Baumer T, Biermann-Ruben K, et al. (2009) Structural changes in the somatosensory system correlate with tic severity in Gilles de la Tourette syndrome. Brain 132: 765–777.
[43]
Sowell ER, Kan E, Yoshii J, Thompson PM, Bansal R, et al. (2008) Thinning of sensorimotor cortices in children with Tourette syndrome. Nat Neurosci 11: 637–639.
[44]
Mink JW (2003) The Basal Ganglia and involuntary movements: impaired inhibition of competing motor patterns. Arch Neurol 60: 1365–1368.
[45]
Peterson BS, Thomas P, Kane MJ, Scahill L, Zhang H, et al. (2003) Basal Ganglia volumes in patients with Gilles de la Tourette syndrome. Arch Gen Psychiatry 60: 415–424.
[46]
Peterson B, Riddle MA, Cohen DJ, Katz LD, Smith JC, et al. (1993) Reduced basal ganglia volumes in Tourette's syndrome using three-dimensional reconstruction techniques from magnetic resonance images. Neurology 43: 941–949.
[47]
Leckman JF, Bloch MH, Smith ME, Larabi D, Hampson M (2010) Neurobiological substrates of Tourette's disorder. J Child Adolesc Psychopharmacol 20: 237–247.
DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13: 281–285.
[50]
Malison RT, McDougle CJ, van Dyck CH, Scahill L, Baldwin RM, et al. (1995) [123I]beta-CIT SPECT imaging of striatal dopamine transporter binding in Tourette's disorder. Am J Psychiatry 152: 1359–1361.
[51]
Singer HS, Szymanski S, Giuliano J, Yokoi F, Dogan AS, et al. (2002) Elevated intrasynaptic dopamine release in Tourette's syndrome measured by PET. Am J Psychiatry 159: 1329–1336.
[52]
Singer HS (1994) Neurobiological issues in Tourette syndrome. Brain Dev 16: 353–364.
[53]
Akkal D, Dum RP, Strick PL (2007) Supplementary motor area and presupplementary motor area: targets of basal ganglia and cerebellar output. J Neurosci 27: 10659–10673.
[54]
Steeves TD, Ko JH, Kideckel DM, Rusjan P, Houle S, et al. (2010) Extrastriatal dopaminergic dysfunction in tourette syndrome. Ann Neurol 67: 170–181.
[55]
Gilbert DL, Christian BT, Gelfand MJ, Shi B, Mantil J, et al. (2006) Altered mesolimbocortical and thalamic dopamine in Tourette syndrome. Neurology 67: 1695–1697.
Minzer K, Lee O, Hong JJ, Singer HS (2004) Increased prefrontal D2 protein in Tourette syndrome: a postmortem analysis of frontal cortex and striatum. J Neurol Sci 219: 55–61.
[58]
Mueller SC, Jackson GM, Dhalla R, Datsopoulos S, Hollis CP (2006) Enhanced cognitive control in young people with Tourette's syndrome. Curr Biol 16: 570–573.
[59]
Jackson GM, Mueller SC, Hambleton K, Hollis CP (2007) Enhanced cognitive control in Tourette Syndrome during task uncertainty. Exp Brain Res 182: 357–364.
[60]
Georgiou N, Bradshaw JL, Phillips JG, Bradshaw JA, Chiu E (1995) Advance information and movement sequencing in Gilles de la Tourette's syndrome. J Neurol Neurosurg Psychiatry 58: 184–191.
