Brain polarization enhances the formation and retention of motor memories.

One of the first steps in the acquisition of a new motor skill is the formation of motor memories. Here we tested the capacity of transcranial DC stimulation (tDCS) applied over the motor cortex during motor practice to increase motor memory formation and retention. Nine healthy individuals underwent a crossover transcranial magnetic stimulation (TMS) study designed to test motor memory formation resulting from training. Anodal tDCS elicited an increase in the magnitude and duration of motor memories in a polarity-specific manner, as reflected by changes in the kinematic characteristics of TMS-evoked movements after anodal, but not cathodal or sham stimulation. This effect was present only when training and stimulation were associated and mediated by a differential modulation of corticomotor excitability of the involved muscles. These results indicate that anodal brain polarization can enhance the initial formation and retention of a new motor memory resulting from training. These processes may be the underlying mechanisms by which tDCS enhances motor learning.

[1]  Daniel Zeller,et al.  Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. , 2008, Cerebral cortex.

[2]  Alfredo Berardelli,et al.  Phasic voluntary movements reverse the aftereffects of subsequent theta-burst stimulation in humans. , 2008, Journal of neurophysiology.

[3]  Stefan Knecht,et al.  Noninvasive Brain Stimulation Improves Language Learning , 2008, Journal of Cognitive Neuroscience.

[4]  Andreas R. Luft,et al.  Motor learning transiently changes cortical somatotopy , 2008, NeuroImage.

[5]  John C Rothwell,et al.  Effect of physiological activity on an NMDA-dependent form of cortical plasticity in human. , 2008, Cerebral cortex.

[6]  L. Cohen,et al.  Concurrent action observation modulates practice‐induced motor memory formation , 2008, The European journal of neuroscience.

[7]  Reza Shadmehr,et al.  Impairment of Retention But Not Acquisition of a Visuomotor Skill Through Time-Dependent Disruption of Primary Motor Cortex , 2007, The Journal of Neuroscience.

[8]  John C Rothwell,et al.  Differential Modulation of Motor Cortical Plasticity and Excitability in Early and Late Phases of Human Motor Learning , 2007, The Journal of Neuroscience.

[9]  A. Berardelli,et al.  Effects of 5 Hz subthreshold magnetic stimulation of primary motor cortex on fast finger movements in normal subjects , 2007, Experimental Brain Research.

[10]  Sergio P. Rigonatti,et al.  Hand function improvement with low-frequency repetitive transcranial magnetic stimulation of the unaffected hemisphere in a severe case of stroke. , 2006, American journal of physical medicine & rehabilitation.

[11]  G. Davis.  Homeostatic control of neural activity: from phenomenology to molecular design. , 2006, Annual review of neuroscience.

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

[13]  Julie Duque,et al.  Encoding a motor memory in the older adult by action observation , 2006, NeuroImage.

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

[15]  Marie-H Monfils,et al.  In Search of the Motor Engram: Motor Map Plasticity as a Mechanism for Encoding Motor Experience , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[16]  S. Knecht,et al.  Dopaminergic effects on encoding of a motor memory in chronic stroke , 2005, Neurology.

[17]  L. Cohen,et al.  Dopaminergic influences on formation of a motor memory , 2005, Annals of neurology.

[18]  Y. Z. Huang,et al.  Theta‐burst repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex , 2005, The Journal of physiology.

[19]  L. Cohen,et al.  Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. , 2005, Brain : a journal of neurology.

[20]  L. Cohen,et al.  Role of voluntary drive in encoding an elementary motor memory. , 2005, Journal of neurophysiology.

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

[22]  Walter Paulus,et al.  Facilitation of probabilistic classification learning by transcranial direct current stimulation of the prefrontal cortex in the human , 2004, Neuropsychologia.

[23]  D. Liebetanz,et al.  MRI study of human brain exposed to weak direct current stimulation of the frontal cortex , 2004, Clinical Neurophysiology.

[24]  Manuel Rodrı́guez,et al.  Hand movement distribution in the motor cortex: the influence of a concurrent task and motor imagery , 2004, NeuroImage.

[25]  L. Cohen,et al.  Enhancing encoding of a motor memory in the primary motor cortex by cortical stimulation. , 2004, Journal of neurophysiology.

[26]  K. Hoffmann,et al.  Facilitation of visuo‐motor learning by transcranial direct current stimulation of the motor and extrastriate visual areas in humans , 2004, The European journal of neuroscience.

[27]  J. Rothwell,et al.  Preconditioning of Low-Frequency Repetitive Transcranial Magnetic Stimulation with Transcranial Direct Current Stimulation: Evidence for Homeostatic Plasticity in the Human Motor Cortex , 2004, The Journal of Neuroscience.

[28]  D. Ruge,et al.  Learning Modifies Subsequent Induction of Long-Term Potentiation-Like and Long-Term Depression-Like Plasticity in Human Motor Cortex , 2004, The Journal of Neuroscience.

[29]  S. Nelson,et al.  Homeostatic plasticity in the developing nervous system , 2004, Nature Reviews Neuroscience.

[30]  J. Kleim,et al.  Cortical Synaptogenesis and Motor Map Reorganization Occur during Late, But Not Early, Phase of Motor Skill Learning , 2004, The Journal of Neuroscience.

[31]  M. Nitsche,et al.  Safety criteria for transcranial direct current stimulation (tDCS) in humans , 2003, Clinical Neurophysiology.

[32]  M. Nitsche,et al.  Pharmacological Modulation of Cortical Excitability Shifts Induced by Transcranial Direct Current Stimulation in Humans , 2003, The Journal of physiology.

[33]  H. Dinse,et al.  Pharmacological Modulation of Perceptual Learning and Associated Cortical Reorganization , 2003, Science.

[34]  M. Nitsche,et al.  Facilitation of Implicit Motor Learning by Weak Transcranial Direct Current Stimulation of the Primary Motor Cortex in the Human , 2003, Journal of Cognitive Neuroscience.

[35]  L. Cohen,et al.  A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. , 2003, Journal of neurophysiology.

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

[37]  C. Braun,et al.  Motor learning elicited by voluntary drive. , 2003, Brain : a journal of neurology.

[38]  L. G. Cohen,et al.  Effect of an α1-adrenergic blocker on plasticity elicited by motor training , 2003, Experimental Brain Research.

[39]  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.

[40]  L. Cohen,et al.  Enhancement of use-dependent plasticity by d-amphetamine , 2002, Neurology.

[41]  B. Christensen,et al.  The mechanisms of interhemispheric inhibition in the human motor cortex , 2002, The Journal of physiology.

[42]  L. Cohen,et al.  Cortical excitability changes induced by deafferentation of the contralateral hemisphere. , 2002, Brain : a journal of neurology.

[43]  M. Hallett,et al.  Early consolidation in human primary motor cortex , 2002, Nature.

[44]  L. Cohen,et al.  Modulation of use‐dependent plasticity by d‐amphetamine , 2002, Supplements to Clinical neurophysiology.

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

[46]  L. Cohen,et al.  Enhancing analogic reasoning with rTMS over the left prefrontal cortex , 2001, Neurology.

[47]  M. Hallett,et al.  Role of the human motor cortex in rapid motor learning , 2001, Experimental Brain Research.

[48]  Walter Paulus,et al.  Diminution of training-induced transient motor cortex plasticity by weak transcranial direct current stimulation in the human , 2000, Neuroscience Letters.

[49]  P M Matthews,et al.  Evidence for adaptive functional changes in the cerebral cortex with axonal injury from multiple sclerosis. , 2000, Brain : a journal of neurology.

[50]  L. Abbott,et al.  Synaptic plasticity: taming the beast , 2000, Nature Neuroscience.

[51]  J. Donoghue,et al.  Learning-induced LTP in neocortex. , 2000, Science.

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

[53]  J. Kalaska,et al.  Prior information in motor and premotor cortex: activity during the delay period and effect on pre-movement activity. , 2000, Journal of neurophysiology.

[54]  M. Hallett.  Transcranial magnetic stimulation and the human brain , 2000, Nature.

[55]  J. Liepert,et al.  Treatment-induced cortical reorganization after stroke in humans. , 2000, Stroke.

[56]  S. Wise,et al.  Mechanisms of use-dependent plasticity in the human motor cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[57]  L. Cohen,et al.  Induction of plasticity in the human motor cortex by paired associative stimulation. , 2000, Brain : a journal of neurology.

[58]  M. Mesulam,et al.  Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[60]  Mark Hallett,et al.  Mechanisms of Deafferentation-Induced Plasticity in Human Motor Cortex , 1998, The Journal of Neuroscience.

[61]  J. Donoghue,et al.  Strengthening of horizontal cortical connections following skill learning , 1998, Nature Neuroscience.

[62]  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.

[63]  J. Liepert,et al.  Motor cortex plasticity during constraint-induced movement therapy in stroke patients , 1998, Neuroscience Letters.

[64]  M. Hallett,et al.  Rapid plasticity of human cortical movement representation induced by practice. , 1998, Journal of neurophysiology.

[65]  L. Cohen,et al.  Modulation of Plasticity in Human Motor Cortex after Forearm Ischemic Nerve Block , 1998, The Journal of Neuroscience.

[66]  M Hallett,et al.  Linguistic processing during repetitive transcranial magnetic stimulation , 1998, Neurology.

[67]  M. Ridding,et al.  Stimulus/response curves as a method of measuring motor cortical excitability in man. , 1997, Electroencephalography and clinical neurophysiology.

[68]  W. Abraham,et al.  Metaplasticity: A new vista across the field of synaptic plasticity , 1997, Progress in Neurobiology.

[69]  J. Rothwell,et al.  Techniques and mechanisms of action of transcranial stimulation of the human motor cortex , 1997, Journal of Neuroscience Methods.

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

[71]  T. Brashers-Krug,et al.  Functional Stages in the Formation of Human Long-Term Motor Memory , 1997, The Journal of Neuroscience.

[72]  A. Schnitzler,et al.  Transcallosally mediated inhibition of interneurons within human primary motor cortex , 1996, Experimental Brain Research.

[73]  K Kaneko,et al.  The effect of current direction induced by transcranial magnetic stimulation on the corticospinal excitability in human brain. , 1996, Electroencephalography and clinical neurophysiology.

[74]  R. Nudo,et al.  Neural Substrates for the Effects of Rehabilitative Training on Motor Recovery After Ischemic Infarct , 1996, Science.

[75]  R. Nudo,et al.  Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. , 1996, Journal of neurophysiology.

[76]  J. Donoghue,et al.  Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex. , 1996, Journal of neurophysiology.

[77]  M. Bear,et al.  Metaplasticity: the plasticity of synaptic plasticity , 1996, Trends in Neurosciences.

[78]  H Scheich,et al.  LTD and LTP induced by transcranial magnetic stimulation in auditory cortex , 1996, Neuroreport.

[79]  M. Merzenich,et al.  Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[80]  Leslie G. Ungerleider,et al.  Functional MRI evidence for adult motor cortex plasticity during motor skill learning , 1995, Nature.

[81]  M. Hallett,et al.  Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. , 1995, Journal of neurophysiology.

[82]  J. Donoghue,et al.  Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[83]  K. Mauritz,et al.  Repetitive training of isolated movements improves the outcome of motor rehabilitation of the centrally paretic hand , 1995, Journal of the Neurological Sciences.

[84]  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.

[85]  M. Hallett,et al.  Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. , 1994, Brain : a journal of neurology.

[86]  J. Donoghue,et al.  Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps. , 1994, Journal of neurophysiology.

[87]  B. Day,et al.  The effect of magnetic coil orientation on the latency of surface EMG and single motor unit responses in the first dorsal interosseous muscle. , 1994, Electroencephalography and clinical neurophysiology.

[88]  M. Hallett,et al.  Modulation of cortical motor output maps during development of implicit and explicit knowledge. , 1994, Science.

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

[90]  G. Recanzone,et al.  Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task. , 1992, Journal of neurophysiology.

[91]  C. Woody,et al.  Properties of associative long-lasting potentiation induced by cellular conditioning in the motor cortex of conscious cats , 1991, Neuroscience.

[92]  A. Keller,et al.  Long-term potentiation in the motor cortex. , 1989, Science.

[93]  A. Baranyi,et al.  Long-lasting potentiation of synaptic transmission requires postnaptic modifications in the neocortex , 1987, Brain Research.

[94]  Brian L. Day,et al.  Different sites of action of electrical and magnetic stimulation of the human brain , 1987, Neuroscience Letters.

[95]  D. M. Feeney,et al.  Amphetamine, haloperidol, and experience interact to affect rate of recovery after motor cortex injury. , 1982, Science.

[96]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[97]  A. Baranyi,et al.  Synaptic facilitation requires paired activation of convergent pathways in the neocortex , 1981, Nature.

[98]  A. Ryszka,et al.  Afferent connections of the laterodorsal thalamic nucleus in the rat , 1979, Neuroscience Letters.

[99]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[100]  E. Evarts.  Activity of pyramidal tract neurons during postural fixation. , 1969, Journal of neurophysiology.

[101]  A. Wu.  Functional neuroimaging and repetitive transcranial magnetic stimulation in Parkinson's disease. , 2007, Reviews in neurological diseases.

[102]  Joseph Classen,et al.  Cerebral Cortex doi:10.1093/cercor/bhi116 Temporary Occlusion of Associative Motor Cortical Plasticity by Prior Dynamic Motor Training , 2005 .

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

[104]  L. Cohen,et al.  Effect of an alpha(1)-adrenergic blocker on plasticity elicited by motor training. , 2003, Experimental brain research.

[105]  L. Cohen,et al.  Cholinergic influences on use-dependent plasticity. , 2002, Journal of neurophysiology.

[106]  J. Donoghue,et al.  Long-term potentiation and long-term depression of horizontal connections in rat motor cortex. , 1996, Acta neurobiologiae experimentalis.

[107]  M. Merzenich,et al.  Repetitive microstimulation alters the cortical representation of movements in adult rats. , 1990, Somatosensory & motor research.

[108]  D. Purpura,et al.  INTRACELLULAR ACTIVITIES AND EVOKED POTENTIAL CHANGES DURING POLARIZATION OF MOTOR CORTEX. , 1965, Journal of neurophysiology.

[109]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .