Site‐specific effects of mental practice combined with transcranial direct current stimulation on motor learning

Mental practice can induce significant neural plasticity and result in motor performance improvement if associated with motor imagery tasks. Given the effects of transcranial direct current stimulation (tDCS) on neuroplasticity, the current study tested whether tDCS, using different electrode montages, can increase the neuroplastic effects of mental imagery on motor learning. Eighteen healthy right‐handed adults underwent a randomised sham‐controlled crossover experiment to receive mental training combined with either sham or active anodal tDCS of the right primary motor cortex (M1), right supplementary motor area, right premotor area, right cerebellum or left dorsolateral prefrontal cortex (DLPFC). Motor performance was assessed by a blinded rater using: non‐dominant handwriting time and legibility, and mentally trained task at baseline (pre) and immediately after (post) mental practice combined with tDCS. Active tDCS significantly enhances the motor‐imagery‐induced improvement in motor function as compared with sham tDCS. There was a specific effect for the site of stimulation such that effects were only observed after M1 and DLPFC stimulation during mental practice. These findings provide new insights into motor imagery training and point out that two cortical targets (M1 and DLPFC) are significantly associated with the neuroplastic effects of mental imagery on motor learning. Further studies should explore a similar paradigm in patients with brain lesions.

[1]  N. Birbaumer,et al.  Enhancement of Planning Ability by Transcranial Direct Current Stimulation , 2009, The Journal of Neuroscience.

[2]  Sergio P. Rigonatti,et al.  Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory , 2005, Experimental Brain Research.

[3]  L Warner,et al.  Mental imagery and its potential for physical therapy. , 1988, Physical therapy.

[4]  Felipe Fregni,et al.  Differential modulatory effects of transcranial direct current stimulation on a facial expression go-no-go task in males and females , 2008, Neuroscience Letters.

[5]  T. Kasai,et al.  Evidence for facilitation of motor evoked potentials (MEPs) induced by motor imagery , 1997, Brain Research.

[6]  R. Passingham,et al.  The Time Course of Changes during Motor Sequence Learning: A Whole-Brain fMRI Study , 1998, NeuroImage.

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

[8]  S. Small,et al.  Fine modulation in network activation during motor execution and motor imagery. , 2004, Cerebral cortex.

[9]  S. Page,et al.  Effects of mental practice on affected limb use and function in chronic stroke. , 2005, Archives of physical medicine and rehabilitation.

[10]  Nicolas Schweighofer,et al.  Motor learning without doing: trial-by-trial improvement in motor performance during mental training. , 2010, Journal of neurophysiology.

[11]  Davis M. Glasser,et al.  Effects of Action Observation on Physical Training After Stroke , 2008, Stroke.

[12]  Stefan Geyer,et al.  Imagery of voluntary movement of fingers, toes, and tongue activates corresponding body-part-specific motor representations. , 2003, Journal of neurophysiology.

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

[14]  Julien Doyon,et al.  Training Mobility Tasks after Stroke with Combined Mental and Physical Practice: A Feasibility Study , 2004, Neurorehabilitation and neural repair.

[15]  S. Murphy,et al.  The effects of positive and negative imagery on motor skill performance , 1985, Cognitive Therapy and Research.

[16]  P. Roland,et al.  Supplementary motor area and other cortical areas in organization of voluntary movements in man. , 1980, Journal of neurophysiology.

[17]  Annie Vinter,et al.  The impact of spatio-temporal constraints on cursive letter handwriting in children , 2008 .

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

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

[20]  K. Feder,et al.  Handwriting development, competency, and intervention , 2007, Developmental medicine and child neurology.

[21]  J. Mazziotta,et al.  Mapping motor representations with positron emission tomography , 1994, Nature.

[22]  R. Passingham,et al.  Functional anatomy of the mental representation of upper extremity movements in healthy subjects. , 1995, Journal of neurophysiology.

[23]  J. G. Jones Motor Learning without Demonstration of Physical Practice, under Two Conditions of Mental Practice , 1965 .

[24]  Sara Marceglia,et al.  Cerebellar Transcranial Direct Current Stimulation Impairs the Practice-dependent Proficiency Increase in Working Memory , 2008, Journal of Cognitive Neuroscience.

[25]  M Hallett,et al.  Focal enhancement of motor cortex excitability during motor imagery: a transcranial magnetic stimulation study , 2002, Acta neurologica Scandinavica.

[26]  J Decety,et al.  Neural Representations for Action , 1996, Reviews in the neurosciences.

[27]  D. Ingvar,et al.  Distribution of cerebral blood flow in the dominant hemisphere during motor ideation and motor performance , 1977, Annals of neurology.

[28]  P. Matthews,et al.  Modulation of movement‐associated cortical activation by transcranial direct current stimulation , 2009, The European journal of neuroscience.

[29]  Giacomo Koch,et al.  Role of the cerebellum in externally paced rhythmic finger movements. , 2007, Journal of neurophysiology.

[30]  Alan C. Evans,et al.  Three-Dimensional MRI Atlas of the Human Cerebellum in Proportional Stereotaxic Space , 1999, NeuroImage.

[31]  Mary E. Morton,et al.  Does an education intervention improve physician signature legibility? Pilot study of a prospective chart review. , 2011, Perspectives in health information management.

[32]  Joseph Classen,et al.  Temporary occlusion of associative motor cortical plasticity by prior dynamic motor training. , 2006, Cerebral cortex.

[33]  M. Inase,et al.  Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. , 1991, Journal of neurophysiology.

[34]  Paul A. Pope,et al.  Task-specific facilitation of cognition by cathodal transcranial direct current stimulation of the cerebellum , 2012, Brain Stimulation.

[35]  Jessica A Turner,et al.  Cerebral and cerebellar sensorimotor plasticity following motor imagery-based mental practice of a sequential movement. , 2004, Journal of rehabilitation research and development.

[36]  C. Hall,et al.  Imagery effects on the performance of skilled and novice soccer players. , 1993, Journal of sports sciences.

[37]  Arno Villringer,et al.  Anodal transcranial direct current stimulation (tDCS) over supplementary motor area (SMA) but not pre-SMA promotes short-term visuomotor learning , 2013, Brain Stimulation.

[38]  Guinevere F. Eden,et al.  A combined fMRI study of typed spelling and reading , 2011, NeuroImage.

[39]  J. Thorne,et al.  Transcranial direct current stimulation of the prefrontal cortex modulates working memory performance: combined behavioural and electrophysiological evidence , 2011, BMC Neuroscience.

[40]  R. Iansek,et al.  Movement-related potentials associated with movement preparation and motor imagery , 1996, Experimental Brain Research.

[41]  M. Diamond,et al.  Primary Motor and Sensory Cortex Activation during Motor Performance and Motor Imagery: A Functional Magnetic Resonance Imaging Study , 1996, The Journal of Neuroscience.

[42]  E. Naito,et al.  Internally Simulated Movement Sensations during Motor Imagery Activate Cortical Motor Areas and the Cerebellum , 2002, The Journal of Neuroscience.

[43]  C. Collet,et al.  Imagery Quality Estimated by Autonomic Response Is Correlated to Sporting Performance Enhancement , 1999, Physiology & Behavior.

[44]  C. Richards,et al.  The Kinesthetic and Visual Imagery Questionnaire (KVIQ) for Assessing Motor Imagery in Persons with Physical Disabilities: A Reliability and Construct Validity Study , 2007, Journal of neurologic physical therapy : JNPT.

[45]  S. Kirker,et al.  Combined transcranial direct current stimulation and robot-assisted arm training in subacute stroke patients: a pilot study. , 2007, Restorative neurology and neuroscience.

[46]  R. Artuch,et al.  Combined Therapy with Idebenone and Deferiprone in Patients with Friedreich’s Ataxia , 2011, The Cerebellum.

[47]  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.

[48]  Jun Tanji,et al.  Role for supplementary motor area cells in planning several movements ahead , 1994, Nature.

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

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

[51]  Wouter Hulstijn,et al.  Learning new movement patterns: a study on good and poor writers comparing learning conditions emphasizing spatial, timing or abstract characteristics. , 2011, Human movement science.

[52]  R. Hanajima,et al.  Magnetic stimulation over the cerebellum in humans , 1995, Annals of neurology.

[53]  Julien Doyon,et al.  Functional neuroanatomical networks associated with expertise in motor imagery , 2008, NeuroImage.

[54]  Klaus Willmes,et al.  On the functional role of human parietal cortex in number processing: How gender mediates the impact of a ‘virtual lesion’ induced by rTMS , 2006, Neuropsychologia.

[55]  Jing Z. Liu,et al.  From mental power to muscle power—gaining strength by using the mind , 2004, Neuropsychologia.

[56]  A. Young,et al.  Human Cognitive Neuropsychology , 2013 .

[57]  D. Brooks,et al.  Motor sequence learning: a study with positron emission tomography , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  Alan C. Evans,et al.  Motor Learning Produces Parallel Dynamic Functional Changes during the Execution and Imagination of Sequential Foot Movements , 2002, NeuroImage.

[59]  M. Epstein,et al.  The Relationship of Mental Imagery and Mental Rehearsal to Performance of a Motor Task , 1980 .

[60]  P. Celnik,et al.  Modulation of Cerebellar Excitability by Polarity-Specific Noninvasive Direct Current Stimulation , 2009, The Journal of Neuroscience.

[61]  Chetwyn C. H. Chan,et al.  Mental imagery for promoting relearning for people after stroke: a randomized controlled trial. , 2004, Archives of physical medicine and rehabilitation.

[62]  M. Bonney Understanding and Assessing Handwriting Difficulty: Perspectives from the Literature , 2010 .

[63]  T. Pozzo,et al.  Improvement and generalization of arm motor performance through motor imagery practice , 2006, Neuroscience.

[64]  J. Decety,et al.  The cerebellum participates in mental activity: tomographic measurements of regional cerebral blood flow , 1990, Brain Research.

[65]  L. Cohen,et al.  Drivers of brain plasticity , 2005, Current opinion in neurology.

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

[67]  S. Page,et al.  Mental Practice in Chronic Stroke: Results of a Randomized, Placebo-Controlled Trial , 2007, Stroke.

[68]  F. P. de Lange,et al.  Motor imagery of gait: a quantitative approach , 2007, Experimental Brain Research.

[69]  H. Siebner,et al.  Effector‐independent representations of simple and complex imagined finger movements: a combined fMRI and TMS study , 2003, The European journal of neuroscience.

[70]  J. Oberdick,et al.  Cerebellar Zones: History, Development, and Function , 2011, The Cerebellum.

[71]  Peter Ford Dominey,et al.  Motor imagery in normal subjects and in asymmetrical Parkinson’s disease , 2000, Neurology.

[72]  M. Erb,et al.  Activation of Cortical and Cerebellar Motor Areas during Executed and Imagined Hand Movements: An fMRI Study , 1999, Journal of Cognitive Neuroscience.

[73]  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.

[74]  Robert L. Wilkes,et al.  Cognitions, mediating variables, and strength performance. , 1984 .

[75]  J. Kleim,et al.  Selective Synaptic Plasticity within the Cerebellar Cortex Following Complex Motor Skill Learning , 1998, Neurobiology of Learning and Memory.

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

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

[78]  R. Dickstein,et al.  Motor Imagery in Physical Therapist Practice , 2007, Physical Therapy.

[79]  S Rossi,et al.  Corticospinal excitability modulation to hand muscles during movement imagery. , 1999, Cerebral cortex.

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

[81]  Olga V. Demler,et al.  The World Health Organization adult ADHD self-report scale (ASRS): a short screening scale for use in the general population , 2005, Psychological Medicine.

[82]  O. Oscasson Functional organization of olivary projection to the cerebellar anterior lobe , 1980 .

[83]  M. Nitsche,et al.  Single-session tDCS-supported retraining does not improve fine motor control in musician's dystonia. , 2011, Restorative neurology and neuroscience.

[84]  G. V. Galen,et al.  The Acquisition of Skilled Handwriting: Discontinuous Trends in Kinematic Variables , 1988 .

[85]  J. Decety The neurophysiological basis of motor imagery , 1996, Behavioural Brain Research.

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

[87]  G. Grouios Mental practice: A review. , 1992 .

[88]  D. Reato,et al.  Gyri-precise head model of transcranial direct current stimulation: Improved spatial focality using a ring electrode versus conventional rectangular pad , 2009, Brain Stimulation.

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

[90]  Lambert Schomaker,et al.  Invariant properties between stroke features in handwriting. , 1993, Acta psychologica.