Modifying the Cortical Processing for Motor Preparation by Repetitive Transcranial Magnetic Stimulation

To investigate the effects of repetitive transcranial magnetic stimulation (rTMS) on the central processing of motor preparation, we had subjects perform a precued-choice reaction time (RT) task. They had to press one of two buttons as quickly as possible after a go signal specifying both the hand to be used and the button to press. A precue preceding this signal conveyed full, partial, or no advance information (hand and/or button), such that RT shortened with increasing amount of information. We applied 1200 to 2400 pulses of 1-Hz rTMS over various cortical areas and compared the subjects' performances at various times before and after this intervention. rTMS delayed RT at two distinct phases after stimulation, one within 10 min and another with a peak at 20 to 30 min and lasting for 60 to 90 min, with no significant effects on error rates or movement time. The effect was significantly larger on left- than on right-hand responses. RT was prominently delayed over the premotor and motor cortices with similar effects across different conditions of advance information, suggesting that preparatory processes relatively close to the formation of motor output were influenced by rTMS. In contrast, the effect of rTMS over the supplementary motor area and the anterior parietal cortex varied with the amount of advance information, indicating specific roles played by these areas in integrating target and effector information. The primary motor area, especially of the left hemisphere, may take over this processing, implementing motor output based on the information processed in other areas.

[1]  Andrea Brovelli,et al.  EEG dynamics of the frontoparietal network during reaching preparation in humans , 2007, NeuroImage.

[2]  Jonathan S. Cant,et al.  Effector-specific fields for motor preparation in the human frontal cortex , 2007, NeuroImage.

[3]  R. Verleger,et al.  A TMS study on non-consciously triggered response tendencies in the motor cortex , 2006, Experimental Brain Research.

[4]  Hartwig R. Siebner,et al.  BOLD MRI responses to repetitive TMS over human dorsal premotor cortex , 2005, NeuroImage.

[5]  Y. Terao,et al.  Interhemispheric transmission of visuomotor information for motor implementation. , 2005, Cerebral cortex.

[6]  Guido Nolte,et al.  Synchronization of parietal and premotor areas during preparation and execution of praxis hand movements , 2005, Clinical Neurophysiology.

[7]  G. Hammond,et al.  Electrophysiological evidence for lateralization of preparatory motor processes , 2005, Neuroreport.

[8]  Nobuyuki Nukina,et al.  Modulation of monoamine transporter expression and function by repetitive transcranial magnetic stimulation. , 2005, Biochemical and biophysical research communications.

[9]  J. Rothwell,et al.  Theta Burst Stimulation of the Human Motor Cortex , 2005, Neuron.

[10]  J. Rothwell,et al.  Increased corticospinal excitability after 5 Hz rTMS over the human supplementary motor area , 2005, Journal of Physiology.

[11]  Magdalena Sabaté,et al.  Brain lateralization of motor imagery: motor planning asymmetry as a cause of movement lateralization , 2004, Neuropsychologia.

[12]  Hartwig R. Siebner,et al.  Short-term modulation of regional excitability and blood flow in human motor cortex following rapid-rate transcranial magnetic stimulation , 2004, NeuroImage.

[13]  Sung Ho Jang,et al.  Facilitative effect of high frequency subthreshold repetitive transcranial magnetic stimulation on complex sequential motor learning in humans , 2004, Neuroscience Letters.

[14]  J. Tanji,et al.  Differential roles of neuronal activity in the supplementary and presupplementary motor areas: from information retrieval to motor planning and execution. , 2004, Journal of neurophysiology.

[15]  Yoshikazu Ugawa,et al.  Long‐term effect of motor cortical repetitive transcranial magnetic stimulation induces , 2004 .

[16]  J. Rothwell,et al.  Functional MRI of the immediate impact of transcranial magnetic stimulation on cortical and subcortical motor circuits , 2004, The European journal of neuroscience.

[17]  L. Cohen,et al.  Influence of interhemispheric interactions on motor function in chronic stroke , 2004, Annals of neurology.

[18]  Yoshikazu Ugawa,et al.  Endogenous dopamine release induced by repetitive transcranial magnetic stimulation over the primary motor cortex: an [11C]raclopride positron emission tomography study in anesthetized macaque monkeys , 2004, Biological Psychiatry.

[19]  U. Ziemann,et al.  Slowing fastest finger movements of the dominant hand with low-frequency rTMS of the hand area of the primary motor cortex , 2004, Experimental Brain Research.

[20]  Bob Abernethy.  Brain Imaging , 2003, Encyclopedia of Behavioral Medicine.

[21]  Wei-Hung Chen,et al.  Low-frequency rTMS over lateral premotor cortex induces lasting changes in regional activation and functional coupling of cortical motor areas , 2003, Clinical Neurophysiology.

[22]  Philippe A. Chouinard,et al.  Modulating neural networks with transcranial magnetic stimulation applied over the dorsal premotor and primary motor cortices. , 2003, Journal of neurophysiology.

[23]  John S. Duncan,et al.  Combined functional MRI and tractography to demonstrate the connectivity of the human primary motor cortex in vivo , 2003, NeuroImage.

[24]  J. Rothwell,et al.  Slow frequency repetitive transcranial magnetic stimulation affects reaction times, but not priming effects, in a masked prime task , 2003, Clinical Neurophysiology.

[25]  Karl J. Friston,et al.  Acute Remapping within the Motor System Induced by Low-Frequency Repetitive Transcranial Magnetic Stimulation , 2003, The Journal of Neuroscience.

[26]  Ichiro Kanazawa,et al.  0.2‐Hz repetitive transcranial magnetic stimulation has no add‐on effects as compared to a realistic sham stimulation in Parkinson's disease , 2003, Movement disorders : official journal of the Movement Disorder Society.

[27]  J. Adam,et al.  Rapid visuomotor preparation in the human brain: a functional MRI study. , 2003, Brain research. Cognitive brain research.

[28]  Harumasa Takano,et al.  Functional connectivity revealed by single-photon emission computed tomography (SPECT) during repetitive transcranial magnetic stimulation (rTMS) of the motor cortex , 2003, Clinical Neurophysiology.

[29]  P. Goldman-Rakic,et al.  Selective modulation of excitatory and inhibitory microcircuits by dopamine , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Borís Burle,et al.  Partial advance information, number of alternatives, and motor processes: an electromyographic study. , 2002, Acta psychologica.

[31]  Jun Tanji,et al.  Distribution of eye- and arm-movement-related neuronal activity in the SEF and in the SMA and Pre-SMA of monkeys. , 2002, Journal of neurophysiology.

[32]  J. Rothwell,et al.  Functional Connectivity of Human Premotor and Motor Cortex Explored with Repetitive Transcranial Magnetic Stimulation , 2002, The Journal of Neuroscience.

[33]  A. Foundas,et al.  Praxis Lateralization: Errors in Right and Left Hemisphere Stroke , 2001, Cortex.

[34]  John C. Rothwell,et al.  Transcranial Magnetic Stimulation Can Be Used to Test Connections to Primary Motor Areas from Frontal and Medial Cortex in Humans , 2001, NeuroImage.

[35]  Y. Ugawa,et al.  Decreased sensory cortical excitability after 1 Hz rTMS over the ipsilateral primary motor cortex , 2001, Clinical Neurophysiology.

[36]  J. Rothwell,et al.  Are the after-effects of low-frequency rTMS on motor cortex excitability due to changes in the efficacy of cortical synapses? , 2001, Clinical Neurophysiology.

[37]  Á. Pascual-Leone,et al.  The role of the dorsolateral prefrontal cortex during sequence learning is specific for spatial information. , 2001, Cerebral cortex.

[38]  J. Rothwell,et al.  Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex , 2001, NeuroImage.

[39]  D. Durstewitz,et al.  Bidirectional Dopamine Modulation of GABAergic Inhibition in Prefrontal Cortical Pyramidal Neurons , 2001, The Journal of Neuroscience.

[40]  H. Fukuzako,et al.  c-Fos expression in rat brain after repetitive transcranial magnetic stimulation , 2001, Neuroreport.

[41]  Jun Tanji,et al.  Integration of target and body-part information in the premotor cortex when planning action , 2000, Nature.

[42]  K M Heilman,et al.  Hemispheric asymmetries of limb-kinetic apraxia , 2000, Neurology.

[43]  Á. Pascual-Leone,et al.  Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability , 2000, Experimental Brain Research.

[44]  M. Hallett,et al.  Effects of low-frequency transcranial magnetic stimulation on motor excitability and basic motor behavior , 2000, Clinical Neurophysiology.

[45]  L. Cohen,et al.  Reduction of human visual cortex excitability using 1-Hz transcranial magnetic stimulation , 2000, Neurology.

[46]  H. Hinterhuber,et al.  Chronic repetitive transcranial magnetic stimulation enhances c-fos in the parietal cortex and hippocampus. , 2000, Brain research. Molecular brain research.

[47]  A. Riehle,et al.  Precise spike synchronization in monkey motor cortex involved in preparation for movement , 1999, Experimental Brain Research.

[48]  Á. Pascual-Leone,et al.  Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer’s cramp , 1999, Neurology.

[49]  Á. Pascual-Leone,et al.  Study and modulation of human cortical excitability with transcranial magnetic stimulation. , 1998, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[50]  R. Passingham,et al.  Temporary interference in human lateral premotor cortex suggests dominance for the selection of movements. A study using transcranial magnetic stimulation. , 1998, Brain : a journal of neurology.

[51]  J B Green,et al.  An electroencephalographic study of imagined movement. , 1997, Archives of physical medicine and rehabilitation.

[52]  M. Hallett,et al.  Depression of motor cortex excitability by low‐frequency transcranial magnetic stimulation , 1997, Neurology.

[53]  D. Harrington,et al.  Hemispheric asymmetry of movement , 1996, Current Opinion in Neurobiology.

[54]  G. Thickbroom,et al.  Transcranial magnetic stimulation mapping of the motor cortex in normal subjects The representation of two intrinsic hand muscles , 1993, Journal of the Neurological Sciences.

[55]  M. Hallett,et al.  Noninvasive mapping of muscle representations in human motor cortex. , 1992, Electroencephalography and clinical neurophysiology.

[56]  Karl J. Friston,et al.  Cortical areas and the selection of movement: a study with positron emission tomography , 1991, Experimental Brain Research.

[57]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  Jean Requin,et al.  A comparison of preparation-related neuronal activity changes in the prefrontal, premotor, primary motor and posterior parietal areas of the monkey cortex: preliminary results , 1990, Neuroscience Letters.

[59]  R. Nass,et al.  The assessment of aphasia and related disorders By Harold Goodglass and edith kaplan philadelphia, lea & febiger, 1983 illustrated, $27.50 (package) , 1984 .

[60]  E. Renzi,et al.  Modality-specific and supramodal mechanisms of apraxia. , 1982, Brain : a journal of neurology.

[61]  D. Rosenbaum.  Human movement initiation: specification of arm, direction, and extent. , 1980, Journal of experimental psychology. General.

[62]  David Goodman,et al.  Are movements prepared in parts? Not under compatible (naturalized) conditions. , 1980, Journal of experimental psychology. General.

[63]  I. T. Draper.  THE ASSESSMENT OF APHASIA AND RELATED DISORDERS , 1973 .

[64]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[65]  Lefaucheur Jp.  [Motor cortex stimulation for Parkinson's disease and dystonia: lessons from transcranial magnetic stimulation? A review of the literature]. , 2005 .

[66]  J. Lefaucheur.  [Motor cortex stimulation for Parkinson's disease and dystonia: lessons from transcranial magnetic stimulation? A review of the literature]. , 2005, Revue neurologique.

[67]  Alexa Riehle,et al.  Preparation for Action: one of the Key Functions of Motor Cortex , 2004 .

[68]  J. F. Kalaska,et al.  Neuronal activity in primate parietal cortex area 5 varies with intended movement direction during an instructed-delay period , 2004, Experimental Brain Research.

[69]  Paul B. Johnson,et al.  Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. , 1997, Annual review of neuroscience.

[70]  M. Hallett,et al.  Cerebral structures participating in motor preparation in humans: a positron emission tomography study. , 1996, Journal of neurophysiology.

[71]  R N Lemon,et al.  Preparation of visually cued arm movements in monkey. Involvement of inferior parietal cortex. , 1989, Brain, behavior and evolution.

[72]  D. Kimura,et al.  Motor functions of the left hemisphere. , 1974, Brain : a journal of neurology.