Association of cortical disinhibition with tic, ADHD, and OCD severity in Tourette syndrome

Hyperkinetic disorders may involve excess excitatory output from thalamus to cerebral cortex. Case–control, neurophysiological studies in persons with Tourette Syndrome (TS), Attention Deficit Hyperactivity Disorder (ADHD), and Obsessive‐Compulsive Disorder (OCD) support this model. To compare the strength of association between motor cortex inhibition and tic, ADHD, and OCD severity in TS, we used transcranial magnetic stimulation to measure motor cortex inhibition in 36 children and adults with TS. Current symptom severity was assessed with standard clinical rating scales and compared with neurophysiological measures using correlational and multivariate regression analyses. Severity of ADHD symptoms and motor tics were associated significantly and independently with short interval intracortical inhibition (SICI) (r2 = 0.50; F[2,27] = 13.7; P < 0.001), particularly in subjects not taking neuroleptics (r2 = 0.68; F[2,17] = 17.8; P < 0.0001). The correlation of cortical disinhibition was greater with ADHD symptoms severity (r = 0.53; P = 0.003) than with tic severity (r = 0.42; P = 0.02), suggesting that in TS, the association between SICI and ADHD symptoms may be more consistent or direct than the association between SICI and tics. © 2004 Movement Disorder Society

[1]  J. Rothwell,et al.  Changes in the balance between motor cortical excitation and inhibition in focal, task specific dystonia. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[2]  A. Anderson,et al.  A functional magnetic resonance imaging study of tic suppression in Tourette syndrome. , 1998, Archives of general psychiatry.

[3]  N. Swerdlow,et al.  Toward Understanding the Biology of a Complex Phenotype: Rat Strain and Substrain Differences in the Sensorimotor Gating-Disruptive Effects of Dopamine Agonists , 2000, The Journal of Neuroscience.

[4]  D. Cohen,et al.  The Yale Global Tic Severity Scale: initial testing of a clinician-rated scale of tic severity. , 1989, Journal of the American Academy of Child and Adolescent Psychiatry.

[5]  J. Penney,et al.  Speculations on the functional anatomy of basal ganglia disorders. , 1983, Annual review of neuroscience.

[6]  Neal R. Swerdlow,et al.  Tactile prepuff inhibition of startle in children with Tourette’s syndrome: in search of an “fMRI-friendly” startle paradigm , 2001, Biological Psychiatry.

[7]  J. Rothwell,et al.  Magnetic transcranial stimulation at intensities below active motor threshold activates intracortical inhibitory circuits , 1998, Experimental Brain Research.

[8]  Bradley S. Peterson,et al.  The temporal dynamics of tics in Gilles de la Tourette syndrome , 1998, Biological Psychiatry.

[9]  W Paulus,et al.  Changes in human motor cortex excitability induced by dopaminergic and anti-dopaminergic drugs. , 1997, Electroencephalography and clinical neurophysiology.

[10]  H. Tsuji,et al.  Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. , 1997, The Journal of physiology.

[11]  V. Hömberg,et al.  Magnetoelectrical stimulation of motor cortex in children with motor disturbances. , 1992, Electroencephalography and clinical neurophysiology.

[12]  S. Lorente,et al.  Neurophysiological methods testing the psychoneural basis of attention deficit hyperactivity disorder , 1996, Child's Nervous System.

[13]  D. Cohen,et al.  Familial relationship between Gilles de la Tourette's syndrome, attention deficit disorder, learning disabilities, speech disorders, and stuttering. , 1993, Journal of the American Academy of Child and Adolescent Psychiatry.

[14]  A L Reiss,et al.  Corpus callosum morphology in children with Tourette syndrome and attention deficit hyperactivity disorder , 1996, Neurology.

[15]  W. Goodman,et al.  Children's Yale-Brown Obsessive Compulsive Scale: reliability and validity. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[16]  J. McClellan,et al.  Practice parameter for the use of stimulant medications in the treatment of children, adolescents, and adults. , 2004, Journal of the American Academy of Child and Adolescent Psychiatry.

[17]  V. Hömberg,et al.  Magnetic stimulation of motor cortex and nerve roots in children. Maturation of cortico-motoneuronal projections. , 1991, Electroencephalography and clinical neurophysiology.

[18]  R. Inzelberg,et al.  Changes in excitability of motor cortical circuitry in patients with parkinson's disease , 1995, Annals of neurology.

[19]  N. Swerdlow,et al.  Seroquel restores sensorimotor gating in phencyclidine-treated rats. , 1996, The Journal of pharmacology and experimental therapeutics.

[20]  H. Heinrich,et al.  Deficient intracortical inhibition in drug-naive children with attention-deficit hyperactivity disorder is enhanced by methylphenidate , 2000, Neuroscience Letters.

[21]  E Stern,et al.  A functional neuroanatomy of tics in Tourette syndrome. , 2000, Archives of general psychiatry.

[22]  W. Paulus,et al.  Motor system excitability in healthy children: developmental aspects from transcranial magnetic stimulation. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[23]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[24]  S. Miller,et al.  Evidence of activity-dependent withdrawal of corticospinal projections during human development , 2001, Neurology.

[25]  Yun Zhou,et al.  Elevated intrasynaptic dopamine release in Tourette's syndrome measured by PET. , 2002, The American journal of psychiatry.

[26]  C. Marsden,et al.  Corticocortical inhibition in human motor cortex. , 1993, The Journal of physiology.

[27]  Andreas Heinz,et al.  Tourette's syndrome , 1998, Neurology.

[28]  H. Singer.  Current issues in Tourette syndrome , 2000, Movement disorders : official journal of the Movement Disorder Society.

[29]  W. Paulus,et al.  Deficient motor control in children with tic disorder: evidence from transcranial magnetic stimulation , 1999, Neuroscience Letters.

[30]  J. Mink.  Basal ganglia dysfunction in Tourette's syndrome: a new hypothesis. , 2001, Pediatric neurology.

[31]  E. Wassermann.  Variation in the response to transcranial magnetic brain stimulation in the general population , 2002, Clinical Neurophysiology.

[32]  J C Rothwell,et al.  Abnormalities of the balance between inhibition and excitation in the motor cortex of patients with cortical myoclonus. , 1996, Brain : a journal of neurology.

[33]  C. McDougle,et al.  [123I]beta-CIT SPECT imaging of striatal dopamine transporter binding in Tourette's disorder. , 1995, The American journal of psychiatry.

[34]  G. E. Alexander,et al.  Microstimulation of the primate neostriatum. II. Somatotopic organization of striatal microexcitable zones and their relation to neuronal response properties. , 1985, Journal of neurophysiology.

[35]  S. Zorn,et al.  Blockade of drug-induced deficits in prepulse inhibition of acoustic startle by ziprasidone , 2001, Pharmacology Biochemistry and Behavior.

[36]  K J Werhahn,et al.  Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans , 1999, The Journal of physiology.

[37]  P. Fitzgerald,et al.  A transcranial magnetic stimulation study of the effects of olanzapine and risperidone on motor cortical excitability in patients with schizophrenia , 2002, Psychopharmacology.

[38]  Godfrey D Pearlson,et al.  MRI parcellation of the frontal lobe in boys with attention deficit hyperactivity disorder or Tourette syndrome , 2002, Psychiatry Research: Neuroimaging.

[39]  D. Sackett,et al.  The Ends of Human Life: Medical Ethics in a Liberal Polity , 1992, Annals of Internal Medicine.

[40]  K. Mills,et al.  Corticomotor threshold to magnetic stimulation: Normal values and repeatability , 1997, Muscle & nerve.

[41]  R. Coppola,et al.  Tourette Syndrome: Prediction of Phenotypic Variation in Monozygotic Twins by Caudate Nucleus D2 Receptor Binding , 1996, Science.

[42]  A. O. Hughes,et al.  Clinical epidemiology a basic science for clinical medicine (2nd edition). David L. Sackett, R. Brian Haynes, Gordon H. Guyatt, Peter Tugwell, Little Brown and company, Bosten, 1991. no. of pages: xvii+441. price: £23.95, $32.50. ISBn: 0316‐76599‐6 , 1993 .

[43]  J. Bartko,et al.  New graphical method to measure silent periods evoked by transcranial magnetic stimulation , 2001, Clinical Neurophysiology.

[44]  Mark Hallett,et al.  Sensorimotor gating in boys with Tourette's syndrome and ADHD: Preliminary results , 1996, Biological Psychiatry.

[45]  H. Heinrich,et al.  Children with comorbid attention‐deficit‐hyperactivity disorder and tic disorder: Evidence for additive inhibitory deficits within the motor system , 2001, Annals of neurology.

[46]  W. Paulus,et al.  Pharmacological control of facilitatory I-wave interaction in the human motor cortex. A paired transcranial magnetic stimulation study. , 1998, Electroencephalography and clinical neurophysiology.

[47]  M. Robertson,et al.  Tourette syndrome, associated conditions and the complexities of treatment. , 2000, Brain : a journal of neurology.

[48]  A Rothenberger,et al.  Decreased motor inhibition in Tourette's disorder: evidence from transcranial magnetic stimulation. , 1997, The American journal of psychiatry.

[49]  A. Barker,et al.  NON-INVASIVE MAGNETIC STIMULATION OF HUMAN MOTOR CORTEX , 1985, The Lancet.

[50]  B. Greenberg,et al.  Altered cortical excitability in obsessive–compulsive disorder , 2000, Neurology.

[51]  D. Benson,et al.  Obsessions and compulsions in Gilles de la Tourette's syndrome , 1986, Neurology.

[52]  Danielle N. Pappas.  ADHD Rating Scale-IV: Checklists, Norms, and Clinical Interpretation , 2006 .

[53]  F. Castellanos,et al.  Neuroscience of attention-deficit/hyperactivity disorder: the search for endophenotypes , 2002, Nature Reviews Neuroscience.

[54]  Thomas E. Nichols,et al.  Increased ventral striatal monoaminergic innervation in Tourette syndrome , 2003, Neurology.

[55]  D. Weinberger,et al.  Tourette's syndrome: [I-123]beta-CIT SPECT correlates of vocal tic severity. , 1998, Neurology.