Cathodal transcranial direct current stimulation suppresses ipsilateral projections to presumed propriospinal neurons of the proximal upper limb.

This study investigated whether cathodal transcranial direct current stimulation (c-tDCS) of left primary motor cortex (M1) modulates excitability of ipsilateral propriospinal premotoneurons (PNs) in healthy humans. Transcranial magnetic stimulation (TMS) of the right motor cortex was used to obtain motor evoked potentials (MEPs) from the left biceps brachii (BB) while participants maintained contraction of the left BB. To examine presumed PN excitability, left BB MEPs were compared with those conditioned by median nerve stimulation (MNS) at the left elbow. Interstimulus intervals between TMS and MNS were set to produce summation at the C3-C4 level of the spinal cord. MNS facilitated BB MEPs elicited at TMS intensities near active motor threshold but inhibited BB MEPs at slightly higher intensities, indicative of putative PN modulation. c-tDCS suppressed the facilitatory and inhibitory effects of MNS. Sham tDCS did not alter either component. There was no effect of c-tDCS and sham tDCS on nonconditioned left BB MEPs or on the ipsilateral silent period of left BB. Right first dorsal interosseous MEPs were suppressed by c-tDCS. These results indicate that M1 c-tDCS can be used to modulate excitability of ipsilateral projections to presumed PNs controlling the proximal arm muscle BB. This technique may hold promise for promoting motor recovery of proximal upper limb function after stroke.

[1]  W. Byblow,et al.  Modulation of human cervical premotoneurons during bilateral voluntary contraction of upper‐limb muscles , 2004, Muscle & nerve.

[2]  Sergio P. Rigonatti,et al.  Transcranial direct current stimulation of the unaffected hemisphere in stroke patients , 2005, Neuroreport.

[3]  Gottfried Schlaug,et al.  Contralateral and ipsilateral motor effects after transcranial direct current stimulation , 2006, Neuroreport.

[4]  J. Rothwell,et al.  Level of action of cathodal DC polarisation induced inhibition of the human motor cortex , 2003, Clinical Neurophysiology.

[5]  Nikolaus Weiskopf,et al.  The Role of Contralesional Dorsal Premotor Cortex after Stroke as Studied with Concurrent TMS-fMRI , 2010, The Journal of Neuroscience.

[6]  E. Pierrot-Deseilligny,et al.  Convergence of descending and various peripheral inputs onto common propriospinal‐like neurones in man. , 1992, The Journal of physiology.

[7]  Integration in descending motor pathways controlling the forelimb in the cat , 2004, Experimental Brain Research.

[8]  Gottfried Schlaug,et al.  Transcranial direct current stimulation in stroke recovery. , 2008, Archives of neurology.

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

[10]  M. Nitsche,et al.  Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans , 2001, Neurology.

[11]  Richard S. J. Frackowiak,et al.  Neural correlates of outcome after stroke: a cross-sectional fMRI study. , 2003, Brain : a journal of neurology.

[12]  Marie-Hélène Boudrias,et al.  Output properties and organization of the forelimb representation of motor areas on the lateral aspect of the hemisphere in rhesus macaques. , 2010, Cerebral cortex.

[13]  H. Kuypers,et al.  Cells of origin of cortical projections to dorsal column nuclei, spinal cord and bulbar medial reticular formation in the rhesus monkey , 1976, Neuroscience Letters.

[14]  A. Lundberg,et al.  Integration in descending motor pathways controlling the forelimb in the cat , 2004, Experimental Brain Research.

[15]  S. Sasaki,et al.  Integration in descending motor pathways controlling the forelimb in the cat , 2004, Experimental Brain Research.

[16]  Richard S. J. Frackowiak,et al.  Motor system activation after subcortical stroke depends on corticospinal system integrity. , 2006, Brain : a journal of neurology.

[17]  Alan J Thompson,et al.  The relationship between brain activity and peak grip force is modulated by corticospinal system integrity after subcortical stroke , 2007, The European journal of neuroscience.

[18]  A. Lundberg,et al.  Integration in descending motor pathways controlling the forelimb in the cat , 1977, Experimental Brain Research.

[19]  L. Cohen,et al.  Memory formation in the motor cortex ipsilateral to a training hand. , 2008, Cerebral cortex.

[20]  J. Valls-Solé.  The circuitry of the human spinal cord: Its role in motor control and movement disorders Pierrot-Deseilligny E, Burke D, editors. Hardback. Cambridge University Press; 2005. 642 p. [ISBN: 13978052182581]. , 2008, Clinical Neurophysiology.

[21]  A. Lundberg,et al.  Integration in descending motor pathways controlling the forelimb in the cat , 1978, Experimental Brain Research.

[22]  Alvaro Pascual-Leone,et al.  Interhemispheric Modulation Induced by Cortical Stimulation and Motor Training , 2010, Physical Therapy.

[23]  Christian Gerloff,et al.  The Role of Multiple Contralesional Motor Areas for Complex Hand Movements after Internal Capsular Lesion , 2006, The Journal of Neuroscience.

[24]  Ulf Ziemann,et al.  Modulation of interhemispheric inhibition by volitional motor activity: an ipsilateral silent period study , 2009, The Journal of physiology.

[25]  H. Kuypers,et al.  THE DESCENDING PATHWAYS TO THE SPINAL CORD, THEIR ANATOMY AND FUNCTION. , 1964, Progress in brain research.

[26]  Julius P. A. Dewald,et al.  Ipsilateral versus contralateral cortical motor projections to a shoulder adductor in chronic hemiparetic stroke: implications for the expression of arm synergies , 2008, Experimental Brain Research.

[27]  B. Alstermark,et al.  Properties of propriospinal neurons in the C3-C4 segments mediating disynaptic pyramidal excitation to forelimb motoneurons in the macaque monkey. , 2006, Journal of neurophysiology.

[28]  E. Pierrot-Deseilligny,et al.  Task‐related changes in propriospinal excitation from hand muscles to human flexor carpi radialis motoneurones , 2007, The Journal of physiology.

[29]  R. Lemon.  Descending pathways in motor control. , 2008, Annual review of neuroscience.

[30]  Walter Paulus,et al.  Modulation of cortical excitability by weak direct current stimulation--technical, safety and functional aspects. , 2003, Supplements to Clinical neurophysiology.

[31]  J. Dewald,et al.  Shoulder abduction-induced reductions in reaching work area following hemiparetic stroke: neuroscientific implications , 2007, Experimental Brain Research.

[32]  E. Pierrot-Deseilligny,et al.  The Circuitry of the Human Spinal Cord: General Methodology , 2005 .

[33]  W. Byblow,et al.  Theta burst stimulation of human primary motor cortex degrades selective muscle activation in the ipsilateral arm. , 2010, Journal of neurophysiology.

[34]  D. Rom.  A sequentially rejective test procedure based on a modified Bonferroni inequality , 1990 .

[35]  J. Rothwell,et al.  A propriospinal-like contribution to electromyographic responses evoked in wrist extensor muscles by transcranial stimulation of the motor cortex in man , 1996, Experimental Brain Research.

[36]  Robert Chen,et al.  Interactions between inhibitory and excitatory circuits in the human motor cortex , 2003, Experimental Brain Research.

[37]  J. Dewald,et al.  Impact of gravity loading on post‐stroke reaching and its relationship to weakness , 2007, Muscle & nerve.

[38]  Robert Chen,et al.  The clinical diagnostic utility of transcranial magnetic stimulation: Report of an IFCN committee , 2008, Clinical Neurophysiology.

[39]  J. Lance,et al.  Corticoreticulospinal control of the tonic vibration reflex in the cat. , 1973, Journal of the neurological sciences.

[40]  D. Burke,et al.  Corticospinal excitation of presumed cervical propriospinal neurones and its reversal to inhibition in humans , 2001, The Journal of physiology.

[41]  M. Nitsche,et al.  Modulating parameters of excitability during and after transcranial direct current stimulation of the human motor cortex , 2005, Clinical Neurophysiology.

[42]  Jun Yao,et al.  Cortical overlap of joint representations contributes to the loss of independent joint control following stroke , 2009, NeuroImage.

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

[44]  E. Pierrot-Deseilligny,et al.  Transmission of the cortical command for human voluntary movement through cervical propriospinal premotoneurons , 1996, Progress in Neurobiology.

[45]  J. Rothwell,et al.  Intracortical circuits modulate transcallosal inhibition in humans , 2007, The Journal of physiology.

[46]  L. Cohen,et al.  Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation , 2006, Clinical Neurophysiology.

[47]  Leonardo G. Cohen,et al.  Mechanisms Underlying Functional Changes in the Primary Motor Cortex Ipsilateral to an Active Hand , 2008, The Journal of Neuroscience.

[48]  W. Byblow,et al.  Task-dependent modulation of inputs to proximal upper limb following transcranial direct current stimulation of primary motor cortex. , 2010, Journal of neurophysiology.

[49]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  M Davare,et al.  Role of the ipsilateral primary motor cortex in controlling the timing of hand muscle recruitment. , 2006, Cerebral cortex.

[51]  M Hallett,et al.  Changes in motor cortex excitability during ipsilateral hand muscle activation in humans , 2000, Clinical Neurophysiology.

[52]  W. Byblow,et al.  Task-dependent modulation of propriospinal inputs to human shoulder. , 2008, Journal of neurophysiology.

[53]  J. Tanji,et al.  Neuronal activity in cortical motor areas related to ipsilateral, contralateral, and bilateral digit movements of the monkey. , 1988, Journal of neurophysiology.

[54]  E. Pierrot-Deseilligny,et al.  Evidence for corticospinal excitation of presumed propriospinal neurones in man. , 1994, The Journal of physiology.

[55]  S. Sasaki,et al.  Integration in descending motor pathways controlling the forelimb in the cat , 2004, Experimental Brain Research.

[56]  Laura Avanzino,et al.  Suppression of the transcallosal motor output: a transcranial magnetic stimulation study in healthy subjects , 2004, Experimental Brain Research.

[57]  Sabine Meunier,et al.  Changes in propriospinally mediated excitation of upper limb motoneurons in stroke patients. , 2003, Brain : a journal of neurology.

[58]  Julius P. A. Dewald,et al.  Position-dependent torque coupling and associated muscle activation in the hemiparetic upper extremity , 2007, Experimental Brain Research.

[59]  Pattern of descending excitation of presumed propriospinal neurones at the onset of voluntary movement in humans. , 1994, Acta physiologica Scandinavica.

[60]  W. Paulus,et al.  Effects of transcranial direct current stimulation over the human motor cortex on corticospinal and transcallosal excitability , 2004, Experimental Brain Research.

[61]  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.

[62]  M. Nitsche,et al.  Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation , 2000, The Journal of physiology.

[63]  Sergio P. Rigonatti,et al.  Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients. , 2007, Restorative neurology and neuroscience.

[64]  W. Byblow,et al.  The Contribution of Cervical Propriospinal Premotoneurons in Recovering Hemiparetic Stroke Patients , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[65]  S. Sasaki,et al.  The C3–C4 propriospinal system in the cat and monkey: a spinal pre‐motoneuronal centre for voluntary motor control , 2007, Acta physiologica.