Different Current Intensities of Anodal Transcranial Direct Current Stimulation Do Not Differentially Modulate Motor Cortex Plasticity

Transcranial direct current stimulation (tDCS) is a noninvasive technique that modulates the excitability of neurons within the motor cortex (M1). Although the aftereffects of anodal tDCS on modulating cortical excitability have been described, there is limited data describing the outcomes of different tDCS intensities on intracortical circuits. To further elucidate the mechanisms underlying the aftereffects of M1 excitability following anodal tDCS, we used transcranial magnetic stimulation (TMS) to examine the effect of different intensities on cortical excitability and short-interval intracortical inhibition (SICI). Using a randomized, counterbalanced, crossover design, with a one-week wash-out period, 14 participants (6 females and 8 males, 22–45 years) were exposed to 10 minutes of anodal tDCS at 0.8, 1.0, and 1.2 mA. TMS was used to measure M1 excitability and SICI of the contralateral wrist extensor muscle at baseline, immediately after and 15 and 30 minutes following cessation of anodal tDCS. Cortical excitability increased, whilst SICI was reduced at all time points following anodal tDCS. Interestingly, there were no differences between the three intensities of anodal tDCS on modulating cortical excitability or SICI. These results suggest that the aftereffect of anodal tDCS on facilitating cortical excitability is due to the modulation of synaptic mechanisms associated with long-term potentiation and is not influenced by different tDCS intensities.

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

[2]  J. Rothwell,et al.  Reorganisation in human motor cortex. , 1995, Canadian journal of physiology and pharmacology.

[3]  Gary Kamen,et al.  Hemispheric differences in the relationship between corticomotor excitability changes following a fine-motor task and motor learning. , 2004, Journal of neurophysiology.

[4]  M. Zoghi,et al.  Progressive suppression of intracortical inhibition during graded isometric contraction of a hand muscle is not influenced by hand preference , 2007, Experimental Brain Research.

[5]  S. Jaberzadeh,et al.  Does anodal transcranial direct current stimulation enhance excitability of the motor cortex and motor function in healthy individuals and subjects with stroke: A systematic review and meta-analysis , 2012, Clinical Neurophysiology.

[6]  M. Nitsche,et al.  Physiological Basis of Transcranial Direct Current Stimulation , 2011, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[7]  M. Zoghi,et al.  Differential Modulation of Intracortical Inhibition in Human Motor Cortex during Selective Activation of an Intrinsic Hand Muscle , 2003, The Journal of physiology.

[8]  M. Nitsche,et al.  Serotonin Affects Transcranial Direct Current–Induced Neuroplasticity in Humans , 2009, Biological Psychiatry.

[9]  Walter Paulus,et al.  Gender-specific modulation of short-term neuroplasticity in the visual cortex induced by transcranial direct current stimulation , 2008, Visual Neuroscience.

[10]  K J Werhahn,et al.  Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans , 1999, The Journal of physiology.

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

[12]  Markus Zahn,et al.  Transcranial direct current stimulation: A computer-based human model study , 2007, NeuroImage.

[13]  Takashi Hanakawa,et al.  Enhancement of pinch force in the lower leg by anodal transcranial direct current stimulation , 2009, Experimental Brain Research.

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

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

[16]  P. Matthews,et al.  Polarity-Sensitive Modulation of Cortical Neurotransmitters by Transcranial Stimulation , 2009, The Journal of Neuroscience.

[17]  J. Sanes Neocortical mechanisms in motor learning , 2003, Current Opinion in Neurobiology.

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

[19]  Lei Zhang,et al.  Effects on decreasing upper-limb poststroke muscle tone using transcranial direct current stimulation: a randomized sham-controlled study. , 2013, Archives of physical medicine and rehabilitation.

[20]  Walter Paulus,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.

[21]  David Burke,et al.  The effects of alterations in conditioning stimulus intensity on short interval intracortical inhibition , 2009, Brain Research.

[22]  Robert Chen,et al.  Short-interval intracortical inhibition: A complex measure , 2008, Clinical Neurophysiology.

[23]  V. Di Lazzaro,et al.  The effects of prolonged cathodal direct current stimulation on the excitatory and inhibitory circuits of the ipsilateral and contralateral motor cortex , 2012, Journal of Neural Transmission.

[24]  Walter Paulus,et al.  The effect of lorazepam on the motor cortical excitability in man , 1996, Experimental Brain Research.

[25]  J C Rothwell,et al.  Releasing the brakes before pressing the gas pedal , 1999, Neurology.

[26]  Federico Ranieri,et al.  GABAA receptor subtype specific enhancement of inhibition in human motor cortex , 2006, The Journal of physiology.

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

[28]  M Hallett,et al.  Modulation of practice-dependent plasticity in human motor cortex. , 2001, Brain : a journal of neurology.

[29]  E. Wassermann,et al.  A safety screening questionnaire for transcranial magnetic stimulation , 2001, Clinical Neurophysiology.

[30]  M Hallett,et al.  Mechanisms of Cortical Reorganization in Lower-Limb Amputees , 1998, The Journal of Neuroscience.

[31]  L. Cohen,et al.  Mechanisms influencing stimulus-response properties of the human corticospinal system , 2001, Clinical Neurophysiology.

[32]  Monica A. Perez,et al.  Motor skill training induces changes in the excitability of the leg cortical area in healthy humans , 2004, Experimental Brain Research.

[33]  M. Hallett,et al.  Modeling the current distribution during transcranial direct current stimulation , 2006, Clinical Neurophysiology.

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

[35]  Rieko Osu,et al.  Single Session of Transcranial Direct Current Stimulation Transiently Increases Knee Extensor Force in Patients With Hemiparetic Stroke , 2011, Neurorehabilitation and neural repair.

[36]  M. Sale,et al.  Age-related differences in corticospinal control during functional isometric contractions in left and right hands. , 2005, Journal of applied physiology.

[37]  M. Hallett,et al.  Task-dependent changes of intracortical inhibition , 1997, Experimental Brain Research.

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

[39]  M. Ridding,et al.  Determinants of the induction of cortical plasticity by non‐invasive brain stimulation in healthy subjects , 2010, The Journal of physiology.

[40]  Janine Reis,et al.  Modulation of motor performance and motor learning by transcranial direct current stimulation. , 2011, Current opinion in neurology.

[41]  Nicolas Caesar Petersen,et al.  Probing the corticospinal link between the motor cortex and motoneurones: some neglected aspects of human motor cortical function , 2010, Acta physiologica.

[42]  M. Nitsche,et al.  Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. , 2002, Brain : a journal of neurology.

[43]  L. Cohen,et al.  Transcranial direct current stimulation: State of the art 2008 , 2008, Brain Stimulation.

[44]  M. Nitsche,et al.  Shaping the effects of transcranial direct current stimulation of the human motor cortex. , 2007, Journal of neurophysiology.

[45]  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.

[46]  W. Byblow,et al.  Cathodal transcranial direct current stimulation of the primary motor cortex improves selective muscle activation in the ipsilateral arm. , 2011, Journal of neurophysiology.

[47]  Sergio P. Rigonatti,et al.  Enhancement of non-dominant hand motor function by anodal transcranial direct current stimulation , 2006, Neuroscience Letters.

[48]  M. Koslowsky,et al.  tDCS polarity effects in motor and cognitive domains: a meta-analytical review , 2011, Experimental Brain Research.

[49]  J. Rothwell,et al.  Correlation between cortical plasticity, motor learning and BDNF genotype in healthy subjects , 2011, Experimental Brain Research.

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

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

[52]  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.

[53]  E. G. Jones,et al.  GABAergic neurons and their role in cortical plasticity in primates. , 1993, Cerebral cortex.

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

[55]  Ulf Ziemann,et al.  Inhibitory circuits and the nature of their interactions in the human motor cortex – a pharmacological TMS study , 2008, The Journal of physiology.

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

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

[58]  Charles Capaday,et al.  Task-dependent changes of motor cortical network excitability during precision grip compared to isolated finger contraction. , 2012, Journal of neurophysiology.

[59]  Antonio Oliviero,et al.  Transcranial direct current stimulation effects on I-wave activity in humans. , 2011, Journal of neurophysiology.

[60]  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.

[61]  W. Byblow,et al.  Role of intracortical inhibition in selective hand muscle activation. , 2003, Journal of neurophysiology.

[62]  Ethan R. Buch,et al.  Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation , 2009, Proceedings of the National Academy of Sciences.

[63]  Walter Paulus,et al.  Catecholaminergic consolidation of motor cortical neuroplasticity in humans. , 2004, Cerebral cortex.

[64]  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.

[65]  Kevin G Bath,et al.  Variant BDNF (Val66Met) impact on brain structure and function , 2006, Cognitive, affective & behavioral neuroscience.

[66]  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.

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

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