Effects of the motor cortical quadripulse transcranial magnetic stimulation (QPS) on the contralateral motor cortex and interhemispheric interactions.

Corpus callosum connects the bilateral primary motor cortices (M1s) and plays an important role in motor control. Using the paired-pulse transcranial magnetic stimulation (TMS) paradigm, we can measure interhemispheric inhibition (IHI) and interhemispheric facilitation (IHF) as indexes of the interhemispheric interactions in humans. We investigated how quadripulse transcranial magnetic stimulation (QPS), one form of repetitive TMS (rTMS), on M1 affects the contralateral M1 and the interhemispheric interactions. QPS is able to induce bidirectional plastic changes in M1 depending on the interstimulus intervals (ISIs) of TMS pulses: long-term potentiation (LTP)-like effect by QPS-5 protocol, and long-term depression-like effect by QPS-50, whose numbers indicate the ISI (ms). Twelve healthy subjects were enrolled. We applied QPS over the left M1 and recorded several parameters before and 30 min after QPS. QPS-5, which increased motor-evoked potentials (MEPs) induced by left M1 activation, also increased MEPs induced by right M1 activation. Meanwhile, QPS-50, which decreased MEPs elicited by left M1 activation, did not induce any significant changes in MEPs elicited by right M1 activation. None of the resting motor threshold, active motor threshold, short-interval intracortical inhibition, long-interval intracortical inhibition, intracortical facilitation, and short-interval intracortical inhibition in right M1 were affected by QPS. IHI and IHF from left to right M1 significantly increased after left M1 QPS-5. The degree of left first dorsal interosseous MEP amplitude change by QPS-5 significantly correlated with the degree of IHF change. We suppose that the LTP-like effect on the contralateral M1 may be produced by some interhemispheric interactions through the corpus callosum.

[1]  J. Rothwell,et al.  Practice‐related reduction of electromyographic mirroring activity depends on basal levels of interhemispheric inhibition , 2012, The European journal of neuroscience.

[2]  J. Rothwell,et al.  The physiological basis of the effects of intermittent theta burst stimulation of the human motor cortex , 2008, The Journal of physiology.

[3]  Christian Gerloff,et al.  Disinhibition of the contralateral motor cortex by low-frequency rTMS , 2003, Neuroreport.

[4]  Daniel Zeller,et al.  Theta-burst stimulation: Remote physiological and local behavioral after-effects , 2008, NeuroImage.

[5]  J. Rothwell,et al.  Consensus: Motor cortex plasticity protocols , 2008, Brain Stimulation.

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

[7]  Tohru Ozaki,et al.  Asymmetric control mechanisms of bimanual coordination: An application of directed connectivity analysis to kinematic and functional MRI data , 2008, NeuroImage.

[8]  J. Rothwell,et al.  Effects on the right motor hand‐area excitability produced by low‐frequency rTMS over human contralateral homologous cortex , 2003, The Journal of physiology.

[9]  M Hallett,et al.  Inhibitory influence of the ipsilateral motor cortex on responses to stimulation of the human cortex and pyramidal tract , 1998, The Journal of physiology.

[10]  P. Rossini,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. , 1994, Electroencephalography and clinical neurophysiology.

[11]  Carolynn Patten,et al.  Repetitive Transcranial Magnetic Stimulation of Motor Cortex after Stroke: A Focused Review , 2012, American journal of physical medicine & rehabilitation.

[12]  Paolo Maria Rossini,et al.  Callosal effects of transcranial magnetic stimulation (TMS): the influence of gender and stimulus parameters , 2004, Neuroscience Research.

[13]  Giacomo Koch,et al.  A common polymorphism in the brain‐derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS , 2008, The Journal of physiology.

[14]  L. Cohen,et al.  Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke? , 2006, The Lancet Neurology.

[15]  B. Schofield,et al.  Dendritic morphology and axon collaterals of corticotectal, corticopontine, and callosal neurons in layer V of primary visual cortex of the hooded rat , 1988, The Journal of comparative neurology.

[16]  A. Avenanti,et al.  Low-frequency rTMS promotes use-dependent motor plasticity in chronic stroke , 2012, Neurology.

[17]  Robert Chen,et al.  The effects of inhibitory and facilitatory intracortical circuits on interhemispheric inhibition in the human motor cortex , 2007, The Journal of physiology.

[18]  Y. Sohn,et al.  Interhemispheric transfer of paired associative stimulation-induced plasticity in the human motor cortex , 2011, Neuroreport.

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

[20]  M. Hallett,et al.  Responses to paired transcranial magnetic stimuli in resting, active, and recently activated muscles , 1996, Experimental Brain Research.

[21]  B. Day,et al.  Interhemispheric inhibition of the human motor cortex. , 1992, The Journal of physiology.

[22]  U. Ziemann,et al.  Hemispheric asymmetry of transcallosalinhibition in man , 2004, Experimental Brain Research.

[23]  C. Blakemore,et al.  Pyramidal neurons in layer 5 of the rat visual cortex. III. Differential maturation of axon targeting, dendritic morphology, and electrophysiological properties , 1994, The Journal of comparative neurology.

[24]  J. Liepert,et al.  Interhemispheric effects of high and low frequency rTMS in healthy humans , 2003, Clinical Neurophysiology.

[25]  P. Pasqualetti,et al.  Modulation of motor cortex neuronal networks by rTMS: comparison of local and remote effects of six different protocols of stimulation. , 2011, Journal of neurophysiology.

[26]  Robert Chen,et al.  Organization of ipsilateral excitatory and inhibitory pathways in the human motor cortex. , 2003, Journal of neurophysiology.

[27]  Alexander Münchau,et al.  Magnetic stimulation of human premotor or motor cortex produces interhemispheric facilitation through distinct pathways , 2006, The Journal of physiology.

[28]  D. Matsuzawa,et al.  Quadri-pulse stimulation (QPS) induced LTP/LTD was not affected by Val66Met polymorphism in the brain-derived neurotrophic factor (BDNF) gene , 2011, Neuroscience Letters.

[29]  R. Hanajima,et al.  Quadro-pulse stimulation is more effective than paired-pulse stimulation for plasticity induction of the human motor cortex , 2007, Clinical Neurophysiology.

[30]  John C. Rothwell,et al.  Effect of theta burst stimulation over the human sensorimotor cortex on motor and somatosensory evoked potentials , 2007, Clinical Neurophysiology.

[31]  Babak Boroojerdi,et al.  Transcallosal inhibition in cortical and subcortical cerebral vascular lesions , 1996, Journal of the Neurological Sciences.

[32]  Sergio P. Rigonatti,et al.  A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients , 2005, Neurology.

[33]  U. Ziemann,et al.  Hemispheric asymmetry of transcallosal inhibition in man. , 1995, Experimental brain research.

[34]  Walter Paulus,et al.  Demonstration of facilitatory I wave interaction in the human motor cortex by paired transcranial magnetic stimulation , 1998, The Journal of physiology.

[35]  E. Vaadia,et al.  Timing of bimanual movements in human and non-human primates in relation to neuronal activity in primary motor cortex and supplementary motor area , 2002, Experimental Brain Research.

[36]  A. Salerno,et al.  Interhemispheric facilitation and inhibition studied in man with double magnetic stimulation. , 1996, Electroencephalography and clinical neurophysiology.

[37]  J C Rothwell,et al.  Short latency facilitation between pairs of threshold magnetic stimuli applied to human motor cortex. , 1996, Electroencephalography and clinical neurophysiology.

[38]  Ichiro Kanazawa,et al.  Interhemispheric facilitation of the hand area of the human motor cortex , 1993, Neuroscience Letters.

[39]  M. Hallett,et al.  Human motor evoked responses to paired transcranial magnetic stimuli. , 1992, Electroencephalography and clinical neurophysiology.

[40]  Ichiro Kanazawa,et al.  Mechanisms of intracortical I‐wave facilitation elicited with paired‐pulse magnetic stimulation in humans , 2002, The Journal of physiology.

[41]  B W Fling,et al.  Fundamental differences in callosal structure, neurophysiologic function, and bimanual control in young and older adults. , 2012, Cerebral cortex.

[42]  J. Rothwell,et al.  Theta burst stimulation induces after‐effects on contralateral primary motor cortex excitability in humans , 2008, The Journal of physiology.

[43]  O. Witte,et al.  Physiology of modulation of motor cortex excitability by low-frequency suprathreshold repetitive transcranial magnetic stimulation , 2006, Experimental Brain Research.

[44]  R. Hanajima,et al.  Bidirectional long‐term motor cortical plasticity and metaplasticity induced by quadripulse transcranial magnetic stimulation , 2008, The Journal of physiology.

[45]  E. Vaadia,et al.  Primary motor cortex is involved in bimanual coordination , 1998, Nature.

[46]  A. Münchau,et al.  Laterality of interhemispheric inhibition depends on handedness , 2007, Experimental Brain Research.

[47]  Heidi M. Schambra,et al.  Modulation of excitability of human motor cortex (M1) by 1 Hz transcranial magnetic stimulation of the contralateral M1 , 2003, Clinical Neurophysiology.

[48]  Z. Molnár,et al.  Towards the classification of subpopulations of layer V pyramidal projection neurons , 2006, Neuroscience Research.

[49]  I. Kanazawa,et al.  Interhemispheric facilitation of the hand motor area in humans , 2001, The Journal of physiology.

[50]  鯨井 隆 Corticocortical inhibition in human motor cortex , 1994 .

[51]  J. Rothwell,et al.  The role of interneuron networks in driving human motor cortical plasticity. , 2013, Cerebral cortex.

[52]  Aimee J Nelson,et al.  Bi-directional interhemispheric inhibition during unimanual sustained contractions , 2009, BMC Neuroscience.

[53]  M. George,et al.  Crossed reduction of human motor cortex excitability by 1-Hz transcranial magnetic stimulation 1 These data were previously published in abstract form in: Wassermann, E.M., Wedegaertner, F.R., George, M.S. and Chen, R., Electroenceph. clin. Neurophysiol., 103 (1997) 151. 1 , 1998, Neuroscience Letters.

[54]  Christian Gerloff,et al.  Coordination of Uncoupled Bimanual Movements by Strictly Timed Interhemispheric Connectivity , 2011, The Journal of Neuroscience.

[55]  S. Rossi,et al.  Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research , 2009, Clinical Neurophysiology.

[56]  Francesca Morgante,et al.  Effect of low-frequency repetitive transcranial magnetic stimulation on interhemispheric inhibition. , 2005, Journal of neurophysiology.

[57]  Robert Chen,et al.  Cortical excitability and interhemispheric inhibition after subcortical pediatric stroke: Plastic organization and effects of rTMS , 2010, Clinical Neurophysiology.

[58]  S. Weis,et al.  Sex Hormones: Modulators of Interhemispheric Inhibition in the Human Brain , 2010, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[59]  Robert Chen,et al.  Contralesional repetitive transcranial magnetic stimulation for chronic hemiparesis in subcortical paediatric stroke: a randomised trial , 2008, The Lancet Neurology.

[60]  S. A. Brandt,et al.  Effects of GABAA and GABAB agonists on interhemispheric inhibition in man , 2007, Clinical Neurophysiology.

[61]  P. Mazzone,et al.  Direct demonstration of interhemispheric inhibition of the human motor cortex produced by transcranial magnetic stimulation , 1999, Experimental Brain Research.

[62]  Daniel T Willingham,et al.  Neurophysiological Mechanisms Involved in Transfer of Procedural Knowledge , 2007, The Journal of Neuroscience.