Mechanisms underlying mirror movements in Parkinson's disease: A transcranial magnetic stimulation study

The neural mechanisms underlying unintended mirror movements (MMs) of one hand during unimanual movements of the other hand in patients with Parkinson's disease (PD) are largely unexplored. Here we used surface electromyographic (EMG) analysis and focal transcranial magnetic stimulation (TMS) to investigate the pathophysiological substrate of MMs in four PD patients. Surface EMG was recorded from both abductor pollicis brevis (APB) and first dorsal interosseous (FDI) muscles. Cross‐correlation EMG analysis revealed no common motor drive to the two APBs during intended unimanual tasks. Focal TMS of either primary motor cortex (M1) elicited normal motor‐evoked potentials (MEPs) in the contralateral APB, whereas MEPs were not seen in the ipsilateral hand. During either mirror or voluntary APB contraction, focal TMS of the contralateral M1 produced a long‐lasting silent period (SP), whereas stimulation of the ipsilateral M1 produced a short‐lasting SP. During either mirror or voluntary finger tapping, 5 Hz repetitive TMS (rTMS) of the contralateral M1 disrupted EMG activity in the target FDI, whereas the effects of rTMS of the ipsilateral M1 were by far slighter. During either mirror or voluntary APB contraction, paired‐pulse TMS showed a reduction of short‐interval intracortical inhibition in the contralateral M1. These findings provide converging evidence that, in PD, MMs do not depend on unmasking of ipsilateral projections but are explained by motor output along the crossed corticospinal projection from the mirror M1. © 2006 Movement Disorder Society

[1]  G. Schott,et al.  Congenital mirror movements. , 1981, Journal of neurology, neurosurgery, and psychiatry.

[2]  C. Brinkman.  Supplementary motor area of the monkey's cerebral cortex: short- and long-term deficits after unilateral ablation and the effects of subsequent callosal section , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  H. Shibasaki,et al.  Mirror movement: Application of movement‐related cortical potentials , 1984, Annals of neurology.

[4]  S. Fahn.  Members of the UPDRS Development Committee. Unified Parkinson's Disease Rating Scale , 1987 .

[5]  Z. Jelić-Ivanović,et al.  Esterase D polymorphism in Serbia (Yugoslavia). , 1988, Human heredity.

[6]  E. Ross,et al.  Left‐handed mirror writing following right anterior cerebral artery infarction , 1988, Neurology.

[7]  J. Stephens,et al.  Mirror movements studied in a patient with Klippel‐Feil syndrome. , 1990, The Journal of physiology.

[8]  M. Hallett,et al.  Congenital mirror movements. Abnormal organization of motor pathways in two patients. , 1991, Brain : a journal of neurology.

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

[10]  Karl J. Friston,et al.  Individual patterns of functional reorganization in the human cerebral cortex after capsular infraction , 1993, Annals of neurology.

[11]  L M Harrison,et al.  Patterns of central motor reorganization in hemiplegic cerebral palsy. , 1993, Brain : a journal of neurology.

[12]  J L Bradshaw,et al.  Mirror movements in normal adult subjects. , 1994, Journal of clinical and experimental neuropsychology.

[13]  N Accornero,et al.  Motor cortical inhibition and the dopaminergic system. Pharmacological changes in the silent period after transcranial brain stimulation in normal subjects, patients with Parkinson's disease and drug-induced parkinsonism. , 1994, Brain : a journal of neurology.

[14]  J. L. Taylor,et al.  The effect of voluntary contraction on cortico‐cortical inhibition in human motor cortex. , 1995, The Journal of physiology.

[15]  K. Bötzel,et al.  Movement-related cortical potentials in persistent mirror movements. , 1995, Electroencephalography and clinical neurophysiology.

[16]  B. Meyer,et al.  Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. , 1995, Brain : a journal of neurology.

[17]  M Hallett,et al.  Transcranial magnetic stimulation. Negative effects. , 1995, Advances in neurology.

[18]  P. Gangemi,et al.  Hand motor cortex activation in a patient with congenital mirror movements: a study of the silent period following focal transcranial magnetic stimulation. , 1996, Electroencephalography and clinical neurophysiology.

[19]  L. Harrison,et al.  Mirror movements in X-linked Kallmann's syndrome. I. A neurophysiological study. , 1997, Brain : a journal of neurology.

[20]  R. Dolan,et al.  Mirror movements in X-linked Kallmann's syndrome. II. A PET study. , 1997, Brain : a journal of neurology.

[21]  N. Sadato,et al.  Role of the Supplementary Motor Area and the Right Premotor Cortex in the Coordination of Bimanual Finger Movements , 1997, The Journal of Neuroscience.

[22]  A. Danek,et al.  Persistent mirror movements: functional MR imaging of the hand motor cortex. , 1997, Radiology.

[23]  K. Müller,et al.  Differences between `congenital mirror movements' and `associated movements' in normal children: a neurophysiological case study , 1998, Neuroscience Letters.

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

[25]  J. Stephens,et al.  A neurophysiological study of mirror movements in adults and children , 1999, Annals of neurology.

[26]  P. Beek,et al.  Coordination disorders in patients with Parkinson's disease: a study of paced rhythmic forearm movements , 2000, Experimental Brain Research.

[27]  A. Bonnet.  [The Unified Parkinson's Disease Rating Scale]. , 2000, Revue neurologique.

[28]  G Zaccara,et al.  Reorganization of the motor cortex in a patient with congenital hemiparesis and mirror movements , 2000, Neurology.

[29]  P. Balbi,et al.  Patterns of motor control reorganization in a patient with mirror movements , 2000, Clinical Neurophysiology.

[30]  M. Hallett,et al.  Pathophysiology of bradykinesia in Parkinson's disease. , 2001, Brain : a journal of neurology.

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

[32]  L. Cohen,et al.  Transitions between dynamical states of differing stability in the human brain , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[33]  G. Zaccara,et al.  Bilateral motor cortex output with intended unimanual contraction in congenital mirror movements , 2002, Neurology.

[34]  T. Amisaki,et al.  Congenital mirror movement: a study of functional MRI and transcranial magnetic stimulation. , 2002, Developmental medicine and child neurology.

[35]  G. Zeloni,et al.  Separate ipsilateral and contralateral corticospinal projections in congenital mirror movements: Neurophysiological evidence and significance for motor rehabilitation , 2003, Movement disorders : official journal of the Movement Disorder Society.

[36]  M. Vidailhet,et al.  Mirror movements of the non-affected hand in hemiparkinsonian patients: a reflection of ipsilateral motor overactivity? , 2003, Journal of neurology, neurosurgery, and psychiatry.

[37]  G. Zaccara,et al.  Motor control in mirror movements: studies with transcranial magnetic stimulation. , 2003, Supplements to Clinical neurophysiology.

[38]  S. Rossi,et al.  Involvement of the human dorsal premotor cortex in unimanual motor control: an interference approach using transcranial magnetic stimulation , 2004, Neuroscience Letters.

[39]  John L. Bradshaw,et al.  Investigating the cortical origins of motor overflow , 2004, Brain Research Reviews.

[40]  R. Carson.  Neural pathways mediating bilateral interactions between the upper limbs , 2005, Brain Research Reviews.

[41]  A. Lang,et al.  Mirror movements in parkinsonism: evaluation of a new clinical sign , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[42]  Mark Hallett,et al.  Effect of transcranial magnetic stimulation on bimanual movements. , 2005, Journal of neurophysiology.

[43]  R. Sinke,et al.  Novel PRKCG/SCA14 mutation in a Dutch spinocerebellar ataxia family: Expanding the phenotype , 2006, Movement disorders : official journal of the Movement Disorder Society.