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Electrifying the motor engram: effects of tDCS on motor learning and control

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Abstract

Learning to control our movements is accompanied by neuroplasticity of motor areas of the brain. The mechanisms of neuroplasticity are diverse and produce what is referred to as the motor engram, i.e., the neural trace of the motor memory. Transcranial direct current stimulation (tDCS) alters the neural and behavioral correlates of motor learning, but its precise influence on the motor engram is unknown. In this review, we summarize the effects of tDCS on neural activity and suggest a few key principles: (1) Firing rates are increased by anodal polarization and decreased by cathodal polarization, (2) anodal polarization strengthens newly formed associations, and (3) polarization modulates the memory of new/preferred firing patterns. With these principles in mind, we review the effects of tDCS on motor control, motor learning, and clinical applications. The increased spontaneous and evoked firing rates may account for the modulation of dexterity in non-learning tasks by tDCS. The facilitation of new association may account for the effect of tDCS on learning in sequence tasks while the ability of tDCS to strengthen memories of new firing patterns may underlie the effect of tDCS on consolidation of skills. We then describe the mechanisms of neuroplasticity of motor cortical areas and how they might be influenced by tDCS. We end with current challenges for the fields of brain stimulation and motor learning.

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References

  • Albert DJ (1966) The effects of polarizing currents on the consolidation of learning. Neuropsychologia 4:65–77

    Article  Google Scholar 

  • Allen EA, Pasley BN, Duong T, Freeman RD (2007) Transcranial magnetic stimulation elicits coupled neural and hemodynamic consequences. Science 317(80):1918–1921

  • Antal A, Nitsche MA, Kincses TZ, Kruse W, Hoffmann K-P, Paulus W (2004) Facilitation of visuo-motor learning by transcranial direct current stimulation of the motor and extrastriate visual areas in humans. Eur J Neurosci 19:2888–2892

    Article  PubMed  Google Scholar 

  • Arce F, Novick I, Mandelblat-Cerf Y, Israel Z, Ghez C, Vaadia E (2010a) Combined adaptiveness of specific motor cortical ensembles underlies learning. J Neurosci 30:5415–5425

    Article  PubMed  CAS  Google Scholar 

  • Arce F, Novick I, Mandelblat-Cerf Y, Vaadia E (2010b) Neuronal correlates of memory formation in motor cortex after adaptation to force field. J Neurosci 30:9189–9198

    Article  PubMed  CAS  Google Scholar 

  • Aydin-Abidin S, Moliadze V, Eysel UT, Funke K (2006) Effects of repetitive TMS on visually evoked potentials and EEG in the anaesthetized cat: dependence on stimulus frequency and train duration. J Physiol 574:443–455

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bastani A, Jaberzadeh S (2012) 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. Clin Neurophysiol 123:644–657

  • Bastani A, Jaberzadeh S (2014) Within-session repeated a-tDCS: The effects of repetition rate and inter-stimulus interval on corticospinal excitability and motor performance. Clin Neurophysiol doi:10.1016/j.clinph.2014.01.010

  • Bennett C, Baird A, Miller MB, Wolford GL (2011) Neural correlates of interspecies perspective taking in the post-mortem atlantic salmon: an argument for proper multiple comparisons correction. J Serendipitous 1:1–5

  • Benninger DH, Lomarev MP, Lopez G, Wassermann EM, Li X, Considine E, Hallett M (2010) Transcranial direct current stimulation for the treatment of Parkinson’s disease. J Neurol Neurosurg Psychiatry 81:1105–1111

    Article  PubMed  PubMed Central  Google Scholar 

  • Benninger DH, Lomarev M, Lopez G, Pal N, Luckenbaugh DA, Hallett M (2011) Transcranial direct current stimulation for the treatment of focal hand dystonia. Mov Disord 26:1698–1702

  • Bikson M, Inoue M, Akiyama H, Deans JK, Fox JE, Miyakawa H, Jefferys JGR (2004) Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro. J Physiol 557:175–190

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bikson M, Datta A, Rahman A, Scaturro J (2010) Electrode montages for tDCS and weak transcranial electrical stimulation: role of “return” electrode’s position and size. Clin Neurophysiol 121:1976–1978

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bindman LJ, Lippold OCJ, Redfearn JWT (1962) Long-lasting changes in the level of the electrical activity of the cerebral cortex produced by polarizing currents. Nature 196:584–585

    Article  PubMed  CAS  Google Scholar 

  • Bindman LJ, Lippold OCJ, Redfearn JWT (1964) The action of brief polarizing currents on the cerebral cortex of the rat (1) during current flow and (2) in the production of long-lasting after-effects. J Physiol 172:369–382

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bishop GH, O’Leary JL (1950) The effects of polarizing currents on cell potentials and their significance in the interpretation of central nervous system activity. Electroencephalogr Clin Neurophysiol 2:401–416

    Article  PubMed  CAS  Google Scholar 

  • Boggio PS, Castro LO, Savagim EA, Braite R, Cruz VC, Rocha RR, Rigonatti SP, Silva MTA, Fregni F (2006) Enhancement of non-dominant hand motor function by anodal transcranial direct current stimulation. Neurosci Lett 404:232–236

  • Brazovskaya F, Malikova A, Pavlygina R (1972) After-effects of anodal polarization in the cat cerebral cortex. Neurophysiology 4:194–199

    Article  Google Scholar 

  • Buitrago MM, Ringer T, Schulz JB, Dichgans J, Luft AR (2004) Characterization of motor skill and instrumental learning time scales in a skilled reaching task in rat. Behav Brain Res 155:249–256

    Article  PubMed  Google Scholar 

  • Butler AJ, Shuster M, O’Hara E, Hurley K, Middlebrooks D, Guilkey K (2013) A meta-analysis of the efficacy of anodal transcranial direct current stimulation for upper limb motor recovery in stroke survivors. J Hand Ther 26:162–171

    Article  PubMed  Google Scholar 

  • Buttkus F, Weidenmüller M, Schneider S, Jabusch H-C, Nitsche MA, Paulus W, Altenmüller E (2010) Failure of cathodal direct current stimulation to improve fine motor control in musician’s dystonia. Mov Disord 25:389–394

    Article  PubMed  Google Scholar 

  • Button KS, Ioannidis JPA, Mokrysz C, Nosek BA, Flint J, Robinson ESJ, Munafò MR (2013) Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci 14:365–376

  • Cantarero G, Lloyd A, Celnik PA (2013a) Reversal of long-term potentiation-like plasticity processes after motor learning disrupts skill retention. J Neurosci 33:12862–12869

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cantarero G, Tang B, O’Malley R, Salas R, Celnik PA (2013b) Motor learning interference is proportional to occlusion of LTP-like plasticity. J Neurosci 33:4634–4641

  • Caparelli-Daquer EM, Zimmermann TJ, Mooshagian E, Parra LC, Rice JK, Datta A, Bikson M, Wassermann EM (2012) A pilot study on effects of 4 × 1 high-definition tDCS on motor cortex excitability. In: Conference on proceedings of IEEE engineering in medicine and biology society, pp 735–738

  • Carmeli E, Patish H, Coleman R (2003) The aging hand. J Gerontol A Biol Sci Med Sci 58:146–152

    Article  PubMed  Google Scholar 

  • Castro-Alamancos MA, Borrell J (1993) Motor activity induced by disinhibition of the primary motor cortex of the rat is blocked by a non-NMDA glutamate receptor antagonist. Neurosci Lett 150:183–186

  • Censor N, Dimyan MA, Cohen LG (2010) Modification of existing human motor memories is enabled by primary cortical processing during memory reactivation. Curr Biol 20:1545–1549

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chan CY, Nicholson C (1986) Modulation by applied electric fields of Purkinje and stellate cell activity in the isolated turtle cerebellum. J Physiol 371:89–114

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chan CY, Hounsgaard J, Nicholson C (1988) Effects of electric fields on transmembrane potential and excitability of turtle cerebellar Purkinje cells in vitro. J Physiol 402:751–771

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chen H, Hua SE, Smith MA, Lenz FA, Shadmehr R (2006) Effects of human cerebellar thalamus disruption on adaptive control of reaching. Cereb Cortex 16:1462–1473

  • Churchland MM, Cunningham JP, Kaufman MT, Ryu SI, Shenoy KV (2010) Cortical preparatory activity: representation of movement or first cog in a dynamical machine? Neuron 68:387–400

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Churchland MM, Cunningham JP, Kaufman MT, Foster JD, Nuyujukian P, Ryu SI, Shenoy KV (2012) Neural population dynamics during reaching. Nature 487:51–56

    PubMed  CAS  PubMed Central  Google Scholar 

  • Clarkson AN, Huang BS, MacIsaac SE, Mody I, Carmichael ST (2010) Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature 468:305–309

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Coderre AM, Zeid AA, Dukelow SP, Demmer MJ, Moore KD, Demers MJ, Bretzke H, Herter TM, Glasgow JI, Norman KE, Bagg SD, Scott SH (2010) Assessment of upper-limb sensorimotor function of subacute stroke patients using visually guided reaching. Neurorehabil Neural Repair 24:528–541

    Article  PubMed  Google Scholar 

  • Cogiamanian F, Marceglia S, Ardolino G, Barbieri S, Priori A (2007) Improved isometric force endurance after transcranial direct current stimulation over the human motor cortical areas. Eur J Neurosci 26:242–249

    Article  PubMed  CAS  Google Scholar 

  • Cohen D, Nicolelis MAL (2004) Reduction of single-neuron firing uncertainty by cortical ensembles during motor skill learning. J Neurosci 24:3574–3582

    Article  PubMed  CAS  Google Scholar 

  • Convento S, Bolognini N, Fusaro M, Lollo F, Vallar G (2014) Neuromodulation of parietal and motor activity affects motor planning and execution. Cortex. doi:10.1016/j.cortex.2014.03.006

    Google Scholar 

  • Costa RM, Cohen D, Nicolelis MAL (2004) Differential corticostriatal plasticity during fast and slow motor skill learning in mice. Curr Biol 14:1124–1134

    Article  PubMed  CAS  Google Scholar 

  • Creutzfeldt O, Fromm G, Kapp H (1962) Influence of transcortical dc currents on cortical neuronal activity. Exp Neurol 452:436–452

    Article  Google Scholar 

  • Criscimagna-Hemminger SE, Shadmehr R (2008) Consolidation patterns of human motor memory. J Neurosci 28:9610–9618

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Criscimagna-Hemminger SE, Bastian AJ, Shadmehr R (2010) Size of error affects cerebellar contributions to motor learning. J Neurophysiol 103:2275–2284

    Article  PubMed  PubMed Central  Google Scholar 

  • Crochet S, Fuentealba P, Timofeev I, Steriade M (2004) Selective amplification of neocortical neuronal output by fast prepotentials in vivo. Cereb Cortex 14:1110–1121

    Article  PubMed  CAS  Google Scholar 

  • Cuypers K, Leenus DJF, van den Berg FE, Nitsche MA, Thijs H, Wenderoth N, Meesen RLJ (2013) Is motor learning mediated by tDCS intensity? PLoS One 8:e67344

  • DaSilva AF, Volz MS, Bikson M, Fregni F (2011) Electrode positioning and montage in transcranial direct current stimulation. J Vis Exp 51:1–9

  • Datta A, Truong D, Minhas P, Parra LC, Bikson M (2012) Inter-individual variation during transcranial direct current stimulation and normalization of dose using MRI-derived computational models. Front Psychiatry 3:1–8

    Article  Google Scholar 

  • Della-Maggiore V, Scholz J, Johansen-Berg H, Paus T (2009) The rate of visuomotor adaptation correlates with cerebellar white-matter microstructure. Hum Brain Mapp 30:4048–4053

    Article  PubMed  Google Scholar 

  • Demmer J, Dragunow M, Lawlor PA, Mason SE, Leah JD, Abraham WC, Tate WP (1993) Differential expression of immediate early genes after hippocampal long-term potentiation in awake rats. Brain Res Mol Brain Res 17:279–286

  • Denney D, Brookhart JM (1962) The effects of applied polarization on evoked electro-cortical waves in the cat. Electroencephalogr Clin Neurophysiol 14:885–897

    Article  PubMed  CAS  Google Scholar 

  • Derksen MJ, Ward NL, Hartle KD, Ivanco TL (2007) MAP2 and synaptophysin protein expression following motor learning suggests dynamic regulation and distinct alterations coinciding with synaptogenesis. Neurobiol Learn Mem 87:404–415

    Article  PubMed  CAS  Google Scholar 

  • Di Lazzaro V, Manganelli F, Dileone M, Notturno F, Esposito M, Capasso M, Dubbioso R, Pace M, Ranieri F, Minicuci G, Santoro L, Uncini A (2012) The effects of prolonged cathodal direct current stimulation on the excitatory and inhibitory circuits of the ipsilateral and contralateral motor cortex. J. Neural Transm. 119:1499–1506

    Article  PubMed  Google Scholar 

  • Donchin O, Sawaki L, Madupu G, Cohen LG, Shadmehr R (2002) Mechanisms influencing acquisition and recall of motor memories. J Neurophysiol 88:2114–2123

    Article  PubMed  CAS  Google Scholar 

  • Donchin O, Rabe K, Diedrichsen J, Lally N, Schoch B, Gizewski ER, Timmann D (2012) Cerebellar regions involved in adaptation to force field and visuomotor perturbation. J Neurophysiol 107:134–147. doi:10.1152/jn.00007.2011

  • Edwards D, Cortes M, Datta A, Minhas P, Wassermann EM, Bikson M (2013) Physiological and modeling evidence for focal transcranial electrical brain stimulation in humans: a basis for high-definition tDCS. Neuroimage 74:266–275

    Article  PubMed  Google Scholar 

  • Elbert T, Lutzenberger W, Rockstroh B, Birbaumer N (1981) The influence of low-level transcortical DC-currents on response speed in humans. Int J Neurosci 14:101–114

    Article  PubMed  CAS  Google Scholar 

  • Elsner B, Kugler J, Pohl M, Mehrholz J (2013) Transcranial direct current stimulation (tDCS) for improving function and activities of daily living in patients after stroke. Cochrane Datab Syst Rev 11:CD009645

  • Floyer-Lea A, Wylezinska M, Kincses TZ, Matthews PM (2006) Rapid modulation of GABA concentration in human sensorimotor cortex during motor learning. J Neurophysiol 95:1639–1644

    Article  PubMed  CAS  Google Scholar 

  • Fox GQ, Kötting D, Richardson GP (1984) Investigations into a bioelectric component of synaptogenesis. Brain Res 311:31–37

    Article  PubMed  CAS  Google Scholar 

  • Fregni F, Boggio PS, Mansur CG, Wagner T, Ferreira MJL, Lima MC, Rigonatti SP, Marcolin MA, Freedman SD, Nitsche MA, Pascual-Leone A (2005) Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. NeuroReport 16:1551–1555

    Article  PubMed  Google Scholar 

  • Fregni F, Boggio PS, Santos MC, Lima M, Vieira AL, Rigonatti SP, Silva MTA, Barbosa ER, Nitsche MA, Pascual-Leone A (2006) Noninvasive cortical stimulation with transcranial direct current stimulation in Parkinson’s disease. Mov Disord 21:1693–1702

  • Fritsch B, Reis J, Martinowich K, Schambra HM, Ji Y, Cohen LG, Lu B (2010) Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron 66:198–204

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fu M, Yu X, Lu J, Zuo Y (2012) Repetitive motor learning induces coordinated formation of clustered dendritic spines in vivo. Nature 483:92–95

  • Furuya S, Nitsche MA, Paulus W, Altenmüller E (2014) Surmounting retraining limits in musicians’ dystonia by transcranial stimulation. Ann Neurol 75:700–707. doi:10.1002/ana.24151

  • Galea JM, Celnik PA (2009) Brain polarization enhances the formation and retention of motor memories. J Neurophysiol 102:294–301

  • Galea JM, Jayaram G, Ajagbe L, Celnik PA (2009) Modulation of cerebellar excitability by polarity-specific noninvasive direct current stimulation. J Neurosci 29:9115–9122

  • Galea JM, Vazquez A, Pasricha N, Orban de Xivry J-J, Celnik PA (2011) Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. Cereb Cortex 21:1761–1770

  • Gandolfo F, Li C, Benda BJ, Padoa-Schioppa C, Bizzi E (2000) Cortical correlates of learning in monkeys adapting to a new dynamical environment. Proc Natl Acad Sci USA 97:2259–2263

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gartside IB (1968a) Mechanisms of sustained increases of firing rate of neurons in the rat cerebral cortex after polarization: reverberating circuits or modification of synaptic conductance? Nature 220:382–383

    Article  PubMed  CAS  Google Scholar 

  • Gartside IB (1968b) Mechanisms of sustained increases of firing rate of neurones in the rat cerebral cortex after polarization: role of protein synthesis. Nature 220:382–383

    Article  PubMed  CAS  Google Scholar 

  • Gibo TL, Criscimagna-Hemminger SE, Okamura AM, Bastian AJ (2013) Cerebellar motor learning: are environment dynamics more important than error size? J Neurophysiol 110:322–333. doi:10.1152/jn.00745.2012

  • Goodwill AM, Reynolds J, Daly RM, Kidgell DJ (2013) Formation of cortical plasticity in older adults following tDCS and motor training. Front Aging Neurosci 5:1–9

    Article  Google Scholar 

  • Gross L (2006) Membrane oscillations keep neurons on the right track. PLoS Biol 4:e191

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Grzegorzewska M, Przybylo M, Litynska A, Hess G (2004) Chemically-induced long-term potentiation in rat motor cortex involves activation of extracellular signal-regulated kinase cascade. Brain Res 192–9:1021

    Google Scholar 

  • Hadipour-Niktarash A, Lee CK, Desmond JE, Shadmehr R (2007) Impairment of retention but not acquisition of a visuomotor skill through time-dependent disruption of primary motor cortex. J Neurosci 27:13413–13419

    Article  PubMed  CAS  Google Scholar 

  • Haith AM, Krakauer JW (2013) Model-based and model-free mechanisms of human motor learning. Adv Exp Med Biol 782:1–21

    Article  PubMed  PubMed Central  Google Scholar 

  • Hardwick RM, Celnik PA (2014) Cerebellar direct current stimulation enhances motor learning in older adults. Neurobiol Aging. doi:10.1016/j.neurobiolaging.2014.03.030

  • Hardwick RM, Rottschy C, Miall RC, Eickhoff SB (2012) A quantitative meta-analysis and review of motor learning in the human brain. Neuroimage. doi:10.1016/j.neuroimage.2012.11.020

  • Hattori Y, Moriwaki A, Hori Y (1990) Biphasic effects of polarizing current on adenosine-sensitive generation of cyclic AMP in rat cerebral cortex. Neurosci Lett 116:320–324

    Article  PubMed  CAS  Google Scholar 

  • Henderson AK, Pittman QJ, Teskey GC (2012) High frequency stimulation alters motor maps, impairs skilled reaching performance and is accompanied by an upregulation of specific GABA, glutamate and NMDA receptor subunits. Neuroscience 215:98–113

  • Herzfeld DJ, Pastor D, Haith AM, Rossetti Y, Shadmehr R, O’Shea J (2014) Contributions of the cerebellum and the motor cortex to acquisition and retention of motor memories. Neuroimage. doi:10.1016/j.neuroimage.2014.04.076

    PubMed  Google Scholar 

  • Hess G (2004) Synaptic plasticity of local connections in rat motor cortex. Acta Neurobiol Exp (Wars) 64:271–276

    Google Scholar 

  • Hess G, Aizenman CD, Donoghue JP (1996) Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex. J Neurophysiol 75:1765–1778

    PubMed  CAS  Google Scholar 

  • Heuninckx S, Wenderoth N, Swinnen SP (2008) Systems neuroplasticity in the aging brain: recruiting additional neural resources for successful motor performance in elderly persons. J Neurosci 28:91–99

    Article  PubMed  CAS  Google Scholar 

  • Hill TC, Zito K (2013) LTP-induced long-term stabilization of individual nascent dendritic spines. J Neurosci 33:678–686

    Article  PubMed  CAS  Google Scholar 

  • Hodgson RA, Ji Z, Standish S, Boyd-Hodgson TE, Henderson AK, Racine RJ (2005) Training-induced and electrically induced potentiation in the neocortex. Neurobiol Learn Mem 83:22–32

  • Hosp JA, Molina-Luna K, Atiemo CO, Hertler B, Luft AR (2009) Dopaminergic modulation of motor maps in rat motor cortex: an in vivo study. Neuroscience 159:692–700

    Article  PubMed  CAS  Google Scholar 

  • Hosp JA, Pekanovic A, Rioult-Pedotti M-S, Luft AR (2011) Dopaminergic projections from midbrain to primary motor cortex mediate motor skill learning. J Neurosci 31:2481–2487

    Article  PubMed  CAS  Google Scholar 

  • Huang VS, Haith AM, Mazzoni P, Krakauer JW (2011) Rethinking motor learning and savings in adaptation paradigms: model-free memory for successful actions combines with internal models. Neuron 70:787–801

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Huber D, Gutnisky DA, Peron S, O’Connor DH, Wiegert JS, Tian L, Oertner TG, Looger LL, Svoboda K (2012) Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484:473–478

  • Hummel FC, Celnik PA, Giraux P, Floel A, Wu W-H, Gerloff C, Cohen LG (2005) Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain 128:490–499

    Article  PubMed  Google Scholar 

  • Hummel FC, Voller B, Celnik PA, Floel A, Giraux P, Gerloff C, Cohen LG (2006) Effects of brain polarization on reaction times and pinch force in chronic stroke. BMC Neurosci 7:73

  • Hummel FC, Heise K, Celnik PA, Floel A, Gerloff C, Cohen LG (2010) Facilitating skilled right hand motor function in older subjects by anodal polarization over the left primary motor cortex. Neurobiol Aging 31:2160–2168

    Article  PubMed  PubMed Central  Google Scholar 

  • Hunter T, Sacco P, Nitsche MA, Turner DL (2009) Modulation of internal model formation during force field-induced motor learning by anodal transcranial direct current stimulation of primary motor cortex. J Physiol 587:2949–2961

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ioannidis JPA (2014) Errors (my very own) and the fearful uncertainty of numbers. Eur J Clin Invest. doi:10.1111/eci.12277

  • Islam N, Moriwaki A, Hattori Y, Hori Y (1994) Anodal polarization induces protein kinase C γ (PKCγ)-like immunoreactivity in the rat cerebral cortex. Neurosci Res 21:169–172

    Article  PubMed  CAS  Google Scholar 

  • Islam N, Moriwaki A, Hattori Y, Hayashi Y, Lu YF, Hori Y (1995) c-Fos expression mediated by N-methyl-D-aspartate receptors following anodal polarization in the rat brain. Exp Neurol 133:25–31

    Article  PubMed  CAS  Google Scholar 

  • Isomura Y, Harukuni R, Takekawa T, Aizawa H, Fukai T (2009) Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements. Nat Neurosci 12:1586–1593

    Article  PubMed  CAS  Google Scholar 

  • Ivanco T, Racine R, Kolb B (2000) Morphology of layer III pyramidal neurons is altered following induction of LTP in sensorimotor cortex of the freely moving rat. Synapse 22:16–22

    Article  Google Scholar 

  • Izawa J, Criscimagna-Hemminger SE, Shadmehr R (2012) Cerebellar contributions to reach adaptation and learning sensory consequences of action. J Neurosci 32:4230–4239

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jackson A, Mavoori J, Fetz EE (2006) Long-term motor cortex plasticity induced by an electronic neural implant. Nature 444:56–60

    Article  PubMed  CAS  Google Scholar 

  • Jacobs K, Donoghue JP (1991) Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251(80):944–947

  • Jayaram G, Tang B, Pallegadda R, Vasudevan EVL, Celnik PA, Bastian AJ (2012) Modulating locomotor adaptation with cerebellar stimulation. J Neurophysiol. doi:10.1152/jn.00645.2011

  • Joiner WM, Smith MA (2008) Long-term retention explained by a model of short-term learning in the adaptive control of reaching. J Neurophysiol 100:2948–2955

    Article  PubMed  PubMed Central  Google Scholar 

  • Kabakov AY, Muller PA, Pascual-Leone A, Jensen FE, Rotenberg A (2012) Contribution of axonal orientation to pathway-dependent modulation of excitatory transmission by direct current stimulation in isolated rat hippocampus. J Neurophysiol 107:1881–1889

  • Kandel M, Beis J-M, Le Chapelain L, Guesdon H, Paysant J (2012) Non-invasive cerebral stimulation for the upper limb rehabilitation after stroke: a review. Ann Phys Rehabil Med 55:657–680

    Article  PubMed  CAS  Google Scholar 

  • Kang EK, Paik N-J (2011) Effect of a tDCS electrode montage on implicit motor sequence learning in healthy subjects. Exp Transl Stroke Med 3:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Kargo WJ, Nitz DA (2003) Early skill learning is expressed through selection and tuning of cortically represented muscle synergies. J Neurosci 23:11255–11269

  • Kargo WJ, Nitz DA (2004) Improvements in the signal-to-noise ratio of motor cortex cells distinguish early versus late phases of motor skill learning. J Neurosci 24:5560–5569

    Article  PubMed  CAS  Google Scholar 

  • Karok S, Witney AG (2013) Enhanced motor learning following task-concurrent dual transcranial direct current stimulation. PLoS ONE 8:e85693

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Khedr EM, Shawky OA, El-Hammady DH, Rothwell JC, Darwish ES, Mostafa OM, Tohamy AM (2013) Effect of anodal versus cathodal transcranial direct current stimulation on stroke rehabilitation: a pilot randomized controlled trial. Neurorehabil Neural Repair. doi:10.1177/1545968313484808

  • Kidgell DJ, Goodwill AM, Frazer AK, Daly RM (2013) Induction of cortical plasticity and improved motor performance following unilateral and bilateral transcranial direct current stimulation of the primary motor cortex. BMC Neurosci 14:64

    Article  PubMed  PubMed Central  Google Scholar 

  • Kilavik BE, Roux S, Ponce-Alvarez A, Confais J, Grün S, Riehle A (2009) Long-term modifications in motor cortical dynamics induced by intensive practice. J Neurosci 29:12653–12663

    Article  PubMed  CAS  Google Scholar 

  • Kleim JA, Lussnig E, Schwarz ER, Comery TA, Greenough WT (1996) Synaptogenesis and Fos expression in the motor cortex of the adult rat after motor skill learning. J Neurosci 16:4529–4535

    PubMed  CAS  Google Scholar 

  • Kleim JA, Barbay S, Nudo RJ (1998) Functional reorganization of the rat motor cortex following motor skill learning. J Neurophysiol 80:3321–3325

    PubMed  CAS  Google Scholar 

  • Kleim JA, Bruneau R, Calder K, Pocock D, VandenBerg PM, MacDonald E, Monfils M-H, Sutherland RJ, Nader K (2003) Functional organization of adult motor cortex is dependent upon continued protein synthesis. Neuron 40:167–176

    Article  PubMed  CAS  Google Scholar 

  • Kleim JA, Chan S, Pringle E, Schallert K, Procaccio V, Jimenez R, Cramer SC (2006) BDNF val66met polymorphism is associated with modified experience-dependent plasticity in human motor cortex. Nat Neurosci 9:735–737

  • Klintsova AY, Dickson E, Yoshida R, Greenough WT (2004) Altered expression of BDNF and its high-affinity receptor TrkB in response to complex motor learning and moderate exercise. Brain Res 92–104:1028

    Google Scholar 

  • Komiyama T, Sato TR, O’Connor DH, Zhang Y-X, Huber D, Hooks BM, Gabitto M, Svoboda K (2010) Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature 464:1182–1186

    Article  PubMed  CAS  Google Scholar 

  • Krug M, Lössner B, Ott T (1984) Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res Bull 13:39–42

    Article  PubMed  CAS  Google Scholar 

  • Kubota K (1996) Motor cortical muscimol injection disrupts forelimb movement in freely moving monkeys. Neuroreport 7:2379–2384

  • Kuo M-F, Unger M, Liebetanz D, Lang N, Tergau F, Paulus W, Nitsche MA (2008) Limited impact of homeostatic plasticity on motor learning in humans. Neuropsychologia 46:2122–2128

    Article  PubMed  Google Scholar 

  • Kuo H-I, Bikson M, Datta A, Minhas P, Paulus W, Kuo M-F, Nitsche MA (2012) Comparing cortical plasticity induced by conventional and high-definition 4 × 1 ring tDCS: a neurophysiological study. Brain Stimul. doi:10.1016/j.brs.2012.09.010

  • Lackner J, DiZio P (1994) Rapid adaptation to coriolis force perturbations of arm trajectory. J Neurophysiol 72:299

    PubMed  CAS  Google Scholar 

  • Lakens D, Evers ERK (2014) Sailing from the seas of chaos into the corridor of stability: practical recommendations to increase the informational value of studies. Perspect Psychol Sci 9:278–292

    Article  Google Scholar 

  • Lampropoulou SI, Nowicky AV (2013) The effect of transcranial direct current stimulation on perception of effort in an isolated isometric elbow flexion task. Mot Control 17:412–426

    Google Scholar 

  • Landau WM, Bishop GH, Clare MH (1964) Analysis of the form and distribution of evoked cortical potentials under the influence of polarizing currents. J Neurophysiol 27:788–813

    PubMed  CAS  Google Scholar 

  • Landi SM, Baguear F, Della-Maggiore V (2011) One week of motor adaptation induces structural changes in primary motor cortex that predict long-term memory one year later. J Neurosci 31:11808–11813

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lefebvre S, Dricot L, Gradkowski W, Laloux P, Vandermeeren Y (2012a) Brain activations underlying different patterns of performance improvement during early motor skill learning. Neuroimage 62:290–299

    Article  PubMed  Google Scholar 

  • Lefebvre S, Laloux P, Peeters A, Desfontaines P, Jamart J, Vandermeeren Y (2012b) Dual-tDCS enhances online motor skill learning and long-term retention in chronic stroke patients. Front Hum Neurosci 6:343

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lefebvre S, Thonnard J-L, Laloux P, Peeters A, Jamart J, Vandermeeren Y (2013) Single Session of dual-tDCS transiently improves precision grip and dexterity of the paretic hand after stroke. Neurorehabil Neural Repair. doi:10.1177/1545968313478485

  • Leite J, Carvalho S, Fregni F, Gonçalves ÓF (2011) Task-specific effects of tDCS-induced cortical excitability changes on cognitive and motor sequence set shifting performance. PLoS ONE 6:e24140

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Leversen JSR, Haga M, Sigmundsson H (2012) From children to adults: motor performance across the life-span. PLoS ONE 7:e38830

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Li CS, Padoa-Schioppa C, Bizzi E (2001) Neuronal correlates of motor performance and motor learning in the primary motor cortex of monkeys adapting to an external force field. Neuron 30:593–607

    Article  PubMed  CAS  Google Scholar 

  • Lindenberg R, Renga V, Zhu LL, Nair D, Schlaug G (2010) Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology 75:2176–2184

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ling DSF, Benardo LS, Serrano PA, Blace N, Kelly MT, Crary JF, Sacktor TC (2002) Protein kinase Mzeta is necessary and sufficient for LTP maintenance. Nat Neurosci 5:295–296

    Article  PubMed  CAS  Google Scholar 

  • Lohse KR, Wadden K, Boyd LA, Hodges NJ (2014) Motor skill acquisition across short and long time scales: a meta-analysis of neuroimaging data. Neuropsychologia. doi:10.1016/j.neuropsychologia.2014.05.001

  • Lu X, Ashe J (2005) Anticipatory activity in primary motor cortex codes memorized movement sequences. Neuron 45:967–973

    Article  PubMed  CAS  Google Scholar 

  • Luft AR, Buitrago MM (2005) Stages of motor skill learning. Mol Neurobiol 32:205–216

    Article  PubMed  CAS  Google Scholar 

  • Luft AR, Buitrago MM, Ringer T, Dichgans J, Schulz JB (2004) Motor skill learning depends on protein synthesis in motor cortex after training. J Neurosci 24:6515–6520

    Article  PubMed  CAS  Google Scholar 

  • Lustig C, Shah P, Seidler RD, Reuter-Lorenz PA (2009) Aging, training, and the brain: a review and future directions. Neuropsychol Rev 19:504–522

  • Madhavan S, Weber KA, Stinear JW (2011) Non-invasive brain stimulation enhances fine motor control of the hemiparetic ankle: implications for rehabilitation. Exp Brain Res 209:9–17

    Article  PubMed  Google Scholar 

  • Mahmoudi H, Borhani Haghighi A, Petramfar P, Jahanshahi S, Salehi Z, Fregni F (2011) Transcranial direct current stimulation: electrode montage in stroke. Disabil Rehabil 33:1383–1388

    Article  PubMed  Google Scholar 

  • Mandelblat-Cerf Y, Novick I, Paz R, Link Y, Freeman S, Vaadia E (2011) The neuronal basis of long-term sensorimotor learning. J Neurosci 31:300–313

    Article  PubMed  CAS  Google Scholar 

  • Marquez J, van Vliet P, McElduff P, Lagopoulos J, Parsons M (2013a) Transcranial direct current stimulation (tDCS): does it have merit in stroke rehabilitation? A systematic review. Int J Stroke 1–11. doi:10.1111/ijs.12169 (in press)

  • Marquez CMS, Zhang X, Swinnen SP, Meesen R, Wenderoth N (2013b) Task-specific effect of transcranial direct current stimulation on motor learning. Front Hum Neurosci 7:333

  • Márquez-Ruiz J, Leal-Campanario R, Sánchez-Campusano R, Molaee-Ardekani B, Wendling F, Miranda PC, Ruffini G, Gruart A, Delgado-García JM (2012) Transcranial direct-current stimulation modulates synaptic mechanisms involved in associative learning in behaving rabbits. Proc Natl Acad Sci USA 109:6710–6715

    Article  PubMed  PubMed Central  Google Scholar 

  • Marshall L, Mölle M, Siebner HR, Born J (2005) Bifrontal transcranial direct current stimulation slows reaction time in a working memory task. BMC Neurosci. 6:23

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT (1996) Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation. Brain 119(Pt 4):1183–1198

  • Matsumura M, Sawaguchi T, Kubota K (1992) GABAergic inhibition of neuronal activity in the primate motor and premotor cortex during voluntary movement. J Neurophysiol 68:692–702

    PubMed  CAS  Google Scholar 

  • Matsuo A, Maeoka H, Hiyamizu M, Shomoto K, Morioka S, Seki K (2011) Enhancement of precise hand movement by transcranial direct current stimulation. NeuroReport 22:78–82

    Article  PubMed  Google Scholar 

  • Matsuzaka Y, Picard N, Strick PL (2007) Skill representation in the primary motor cortex after long-term practice. J Neurophysiol 97:1819–1832

    Article  PubMed  Google Scholar 

  • Mazzoni P, Shabbott BA, Cortés JC (2012) Motor control abnormalities in Parkinson’s disease. Cold Spring Harb Perspect Med 2:a009282

  • McCaig CD, Rajnicek AM (1991) Electrical fields, nerve growth and nerve regeneration. Exp Physiol 76:473–494

    PubMed  CAS  Google Scholar 

  • McCambridge AB, Bradnam LV, Stinear CM, Byblow WD (2011) Cathodal transcranial direct current stimulation of the primary motor cortex improves selective muscle activation in the ipsilateral arm. J Neurophysiol. doi:10.1152/jn.00171.2011

  • McHughen SA, Rodriguez PF, Kleim JA, Kleim ED, Crespo LM, Procaccio V, Cramer SC (2010) BDNF val66met polymorphism influences motor system function in the human brain. Cereb Cortex 20:1254–1262

  • McHughen SA, Pearson-Fuhrhop K, Ngo VK, Cramer SC (2011) Intense training overcomes effects of the Val66Met BDNF polymorphism on short-term plasticity. Exp Brain Res 213:415–422

  • Mei F, Nagappan G, Ke Y, Sacktor TC, Lu B (2011) BDNF facilitates L-LTP maintenance in the absence of protein synthesis through PKMζ. PLoS ONE 6:e21568

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Merchant H, Naselaris T, Georgopoulos AP (2008) Dynamic sculpting of directional tuning in the primate motor cortex during three-dimensional reaching. J Neurosci 28:9164–9172

    Article  PubMed  CAS  Google Scholar 

  • Miniussi C, Harris JA, Ruzzoli M (2013) Modelling non-invasive brain stimulation in cognitive neuroscience. Neurosci Biobehav Rev 37:1702–1712

  • Moliadze V, Antal A, Paulus W (2010a) Electrode-distance dependent after-effects of transcranial direct and random noise stimulation with extracephalic reference electrodes. Clin Neurophysiol 121:2165–2171

    Article  PubMed  Google Scholar 

  • Moliadze V, Antal A, Paulus W (2010b) Boosting brain excitability by transcranial high frequency stimulation in the ripple range. J Physiol 588:4891–4904

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Molina-Luna K, Pekanovic A, Röhrich S, Hertler B, Schubring-Giese M, Rioult-Pedotti M-S, Luft AR (2009) Dopamine in motor cortex is necessary for skill learning and synaptic plasticity. PLoS ONE 4:e7082

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Monfils M-H, Plautz EJ, Kleim JA (2005) In search of the motor engram: motor map plasticity as a mechanism for encoding motor experience. Neurosci 11:471–483

  • Morrell F (1961) Effect of anodal polarization on the firing pattern of single cortical cells. Ann N Y Acad Sci 92:860–876

    Article  PubMed  CAS  Google Scholar 

  • Muellbacher W, Ziemann U, Wissel J, Dang N, Kofler M, Facchini S, Boroojerdi B, Poewe W, Hallett M (2002) Early consolidation in human primary motor cortex. Nature 415:640–644

    Article  PubMed  CAS  Google Scholar 

  • Murayama K, Pekrun R, Fiedler K (2013) Research practices that can prevent an inflation of false-positive rates. Personal Soc Psychol Rev. doi:10.1177/1088868313496330

  • Mutha PK, Sainburg RL, Haaland KY (2011) Critical neural substrates for correcting unexpected trajectory errors and learning from them. Brain. doi:10.1093/brain/awr275

  • Nazarpour K, Barnard A, Jackson A (2012) Flexible cortical control of task-specific muscle synergies. J Neurosci 32:12349–12360

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nieuwenhuis S, Forstmann BU, Wagenmakers E (2011) Erroneous analyses of interactions in neuroscience: a problem of significance. Nat Neurosci 14:1105–1107

    Article  PubMed  CAS  Google Scholar 

  • Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527:633–639

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nitsche MA, Schauenburg A, Lang N, Liebetanz D, Exner C, Paulus W, Tergau F (2003) Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. J Cogn Neurosci 15:619–626

    Article  PubMed  Google Scholar 

  • Nitsche MA, Doemkes S, Karakose T, Antal A, Liebetanz D, Lang N, Tergau F, Paulus W, Karaköse T (2007) Shaping the effects of transcranial direct current stimulation of the human motor cortex. J Neurophysiol 97:3109

    Article  PubMed  CAS  Google Scholar 

  • Orban de Xivry J-J, Criscimagna-Hemminger SE, Shadmehr R (2011a) Contributions of the motor cortex to adaptive control of reaching depend on the perturbation schedule. Cereb Cortex 21:1475–1484

  • Orban de Xivry J-J, Marko MK, Pekny SE, Pastor D, Izawa J, Celnik PA, Shadmehr R (2011b) Stimulation of the human motor cortex alters generalization patterns of motor learning. J Neurosci 31:7102–7110

  • Orban de Xivry J-J, Ahmadi-Pajouh MA, Harran MD, Salimpour Y, Shadmehr R (2013) Changes in corticospinal excitability during reach adaptation in force fields. J Neurophysiol 109:124–136

  • Parikh PJ, Cole KJ (2014) Effects of transcranial direct current stimulation in combination with motor practice on dexterous grasping and manipulation in healthy older adults. Physiol Rep 2:n/a–n/a

  • Paz R, Vaadia E (2004) Specificity of sensorimotor learning and the neural code: neuronal representations in the primary motor cortex. J Physiol Paris 98:331–348

    Article  PubMed  Google Scholar 

  • Paz R, Boraud T, Natan C, Bergman H, Vaadia E (2003) Preparatory activity in motor cortex reflects learning of local visuomotor skills. Nat Neurosci 6:882–890

    Article  PubMed  CAS  Google Scholar 

  • Paz R, Natan C, Boraud T, Bergman H, Vaadia E (2005) Emerging patterns of neuronal responses in supplementary and primary motor areas during sensorimotor adaptation. J Neurosci 25:10941–10951

    Article  PubMed  CAS  Google Scholar 

  • Peters AJ, Chen SX, Komiyama T (2014) Emergence of reproducible spatiotemporal activity during motor learning. Nature. doi:10.1038/nature13235

  • Picard N, Matsuzaka Y, Strick PL (2013) Extended practice of a motor skill is associated with reduced metabolic activity in M1. Nat Neurosci 16:1340–1347

  • Prichard G, Weiller C, Fritsch B, Reis J (2014) Effects of different electrical brain stimulation protocols on subcomponents of motor skill learning. Brain Stimul. doi:10.1016/j.brs.2014.04.005

    PubMed  Google Scholar 

  • Priori A, Berardelli A, Rona S, Accornero N, Manfredi M (1998) Polarization of the human motor cortex through the scalp. NeuroReport 9:2257–2260

    Article  PubMed  CAS  Google Scholar 

  • Purpura DP, McMurtry JG (1965) Intracellular activities and evoked potential changes during polarization of motor cortex. J Neurophysiol 28:166–185

    PubMed  CAS  Google Scholar 

  • Radman T, Ramos RL, Brumberg JC, Bikson M (2009) Role of cortical cell type and morphology in subthreshold and suprathreshold uniform electric field stimulation in vitro. Brain Stimul 2:215.e3–228.e3

  • Rahman A, Reato D, Arlotti M, Gasca F, Datta A, Parra LC, Bikson M (2013) Cellular effects of acute direct current stimulation: somatic and synaptic terminal effects. J Physiol. doi:10.1113/jphysiol.2012.247171

  • Ranieri F, Podda MV, Riccardi E, Frisullo G, Dileone M, Profice P, Pilato F, Di Lazzaro V, Grassi C (2012) Modulation of LTP at rat hippocampal CA3-CA1 synapses by direct current stimulation. J Neurophysiol 107:1868–1880

    Article  PubMed  CAS  Google Scholar 

  • Reato D, Rahman A, Bikson M, Parra LC (2010) Low-intensity electrical stimulation affects network dynamics by modulating population rate and spike timing. J Neurosci 30:15067–15079

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Reis J, Fritsch B (2011) Modulation of motor performance and motor learning by transcranial direct current stimulation. Curr Opin Neurol 24:590–596

    Article  PubMed  Google Scholar 

  • Reis J, Schambra HM, Cohen LG, Buch ER, Fritsch B, Zarahn E, Celnik PA, Krakauer JW (2009) Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc Natl Acad Sci USA 106:1590–1595

  • Reis J, Fischer JT, Prichard G, Weiller C, Cohen LG, Fritsch B (2013) Time- but not sleep-dependent consolidation of tDCS-enhanced visuomotor skills. Cereb Cortex. doi:10.1093/cercor/bht208

  • Richardson AG, Overduin SA, Valero-Cabré A, Padoa-Schioppa C, Pascual-Leone A, Bizzi E, Press DZ (2006) Disruption of primary motor cortex before learning impairs memory of movement dynamics. J Neurosci 26:12466–12470

  • Richardson AG, Borghi T, Bizzi E (2012) Activity of the same motor cortex neurons during repeated experience with perturbed movement dynamics. J Neurophysiol 107:3144–3154

    Article  PubMed  PubMed Central  Google Scholar 

  • Rioult-Pedotti M-S, Friedman D, Hess G, Donoghue JP (1998) Strengthening of horizontal cortical connections following skill learning. Nat Neurosci 1:230–234

    Article  PubMed  CAS  Google Scholar 

  • Rioult-Pedotti M-S, Friedman D, Donoghue JP (2000) Learning-induced LTP in neocortex. Science 290 (80):533–536

  • Rosenkranz K, Nitsche MA, Tergau F, Paulus W (2000) Diminution of training-induced transient motor cortex plasticity by weak transcranial direct current stimulation in the human. Neurosci Lett 296:61–63

    Article  PubMed  CAS  Google Scholar 

  • Ruohonen J, Karhu J (2012) tDCS possibly stimulates glial cells. Clin Neurophysiol 123:2006–2009

    Article  PubMed  Google Scholar 

  • Safstrom D, Flanagan JR, Johansson RS (2013) Skill learning involves optimizing the linking of action phases. J Neurophysiol. doi:10.1152/jn.00019.2013

  • Sailer U, Flanagan JR, Johansson RS (2005) Eye-hand coordination during learning of a novel visuomotor task. J Neurosci 25:8833–8842

    Article  PubMed  CAS  Google Scholar 

  • Salimpour Y, Shadmehr R (2014) Motor costs and the coordination of the two arms. J Neurosci 34:1806–1818

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Salimpour Y, Mari Z, Shadmehr R (2013) Motor costs in Parkinson’s disease. In: Translational and computational motor control. http://www.seas.harvard.edu/motorlab/TCMC2013/76.pdf

  • Schaefer AT, Angelo K, Spors H, Margrie TW (2006) Neuronal oscillations enhance stimulus discrimination by ensuring action potential precision. PLoS Biol 4:e163

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schambra HM, Abe M, Luckenbaugh DA, Reis J, Krakauer JW, Cohen LG (2011) Probing for hemispheric specialization for motor skill learning: a transcranial direct current stimulation study. J Neurophysiol 106:652–661

  • Schieber MH, Poliakov AV (1998) Partial inactivation of the primary motor cortex hand area: effects on individuated finger movements. J Neurosci 18:9038–9054

    PubMed  CAS  Google Scholar 

  • Seidler RD (2007) Aging affects motor learning but not savings at transfer of learning. Learn. Mem 14:17–21

    Article  PubMed  Google Scholar 

  • Serrano P, Friedman EL, Kenney J, Taubenfeld SM, Zimmerman JM, Hanna J, Alberini CM, Kelley AE, Maren S, Rudy JW, Yin JCP, Sacktor TC, Fenton AA (2008) PKMzeta maintains spatial, instrumental, and classically conditioned long-term memories. PLoS Biol 6:2698–2706

  • Shadmehr R, Holcomb H (1997) Neural correlates of motor memory consolidation. Science (80) 277:821–825

  • Shadmehr R, Krakauer JW (2008) A computational neuroanatomy for motor control. Exp Brain Res 185:359–381

    Article  PubMed  PubMed Central  Google Scholar 

  • Shadmehr R, Mussa-Ivaldi FA (1994) Adaptive representation of dynamics during learning of a motor task. J Neurosci 14:3208–3224

  • Shadmehr R, Smith MA, Krakauer JW (2010) Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci 33:89–108

    Article  PubMed  CAS  Google Scholar 

  • Shekhawat GS, Stinear CM, Searchfield GD (2013) Transcranial direct current stimulation intensity and duration effects on tinnitus suppression. Neurorehabil. Neural Repair 27:164–172

    Article  PubMed  Google Scholar 

  • Shenoy KV, Sahani M, Churchland MM (2013) Cortical control of arm movements: a dynamical systems perspective. Annu Rev Neurosci 36:337–359

  • Shmuelof L, Krakauer JW, Mazzoni P (2012) How is a motor skill learned? Change and invariance at the levels of task success and trajectory control. J Neurophysiol 108:578–594

  • Siebner HR, Tormos JM, Ceballos-Baumann AO, Auer C, Catala MD, Conrad B, Pascual-Leone A (1999) Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer’s cramp. Neurology 52:529–537

    Article  PubMed  CAS  Google Scholar 

  • Simmons JP, Nelson LD, Simonsohn U (2011) False-positive psychology: undisclosed flexibility in data collection and analysis allows presenting anything as significant. Psychol Sci 22:1359–1366

    Article  PubMed  Google Scholar 

  • Simonsohn U, Nelson LD, Simmons JP (2014) P-curve: a key to the file-drawer. J Exp Psychol Gen 143:534–547

    Article  PubMed  Google Scholar 

  • Smith MA, Shadmehr R (2005) Intact ability to learn internal models of arm dynamics in Huntington’s disease but not cerebellar degeneration. J Neurophysiol 93:2809–2821

    Article  PubMed  Google Scholar 

  • Smith CD, Umberger GH, Manning EL, Slevin JT, Wekstein DR, Schmitt FA, Markesbery WR, Zhang Z, Gerhardt GA, Kryscio RJ, Gash DM (1999) Critical decline in fine motor hand movements in human aging. Neurology 53:1458–1458

  • Smith MA, Ghazizadeh A, Shadmehr R (2006) Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS Biol 4:e179

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sohn MK, Kim BO, Song HT (2012) Effect of stimulation polarity of transcranial direct current stimulation on non-dominant hand function. Ann Rehabil Med 36:1–7

    Article  PubMed  PubMed Central  Google Scholar 

  • Sokolov EN (1977) Brain functions: neuronal mechanisms of learning and memory. Annu Rev Psychol 28:85–112

    Article  Google Scholar 

  • Stagg CJ, Best JG, Stephenson MC, O’Shea J, Wylezinska M, Kincses TZ, Morris PG, Matthews PM, Johansen-Berg H (2009) Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J Neurosci 29:5202–5206

    Article  PubMed  CAS  Google Scholar 

  • Stagg CJ, Bachtiar V, Johansen-Berg H (2011a) The role of GABA in human motor learning. Curr Biol 21:480–484

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Stagg CJ, Jayaram G, Pastor D, Kincses ZT, Matthews PM, Johansen-Berg H (2011b) Polarity and timing-dependent effects of transcranial direct current stimulation in explicit motor learning. Neuropsychologia 49:800–804

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Stagg CJ, Bachtiar V, O’Shea J, Allman C, Bosnell RA, Kischka U, Matthews PM, Johansen-Berg H (2012) Cortical activation changes underlying stimulation-induced behavioural gains in chronic stroke. Brain 135:276–284

    Article  PubMed  PubMed Central  Google Scholar 

  • Taig E, Kuper M, Theysohn N, Timmann D, Donchin O (2012) Deficient use of visual information in estimating hand position in cerebellar patients. J Neurosci 32:16274–16284

    Article  PubMed  CAS  Google Scholar 

  • Tanaka J-I, Horiike Y, Matsuzaki M, Miyazaki T, Ellis-Davies GCR, Kasai H (2008) Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 319 (80):1683–1687

  • Tanaka S, Hanakawa T, Honda M, Watanabe K (2009) Enhancement of pinch force in the lower leg by anodal transcranial direct current stimulation. Exp Brain Res 196:459–465

    Article  PubMed  PubMed Central  Google Scholar 

  • Tanaka T, Takano Y, Tanaka S, Hironaka N, Kobayashi K, Hanakawa T, Watanabe K, Honda M (2013) Transcranial direct-current stimulation increases extracellular dopamine levels in the rat striatum. Front Syst Neurosci 7:6

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tecchio F, Zappasodi F, Assenza G, Tombini M, Vollaro S, Barbati G, Rossini PM (2010) Anodal transcranial direct current stimulation enhances procedural consolidation. J Neurophysiol 104:1134–1140

    Article  PubMed  Google Scholar 

  • Terney D, Chaieb L, Moliadze V, Antal A, Paulus W (2008) Increasing human brain excitability by transcranial high-frequency random noise stimulation. J Neurosci 28:14147–14155

    Article  PubMed  CAS  Google Scholar 

  • Teyler TJ, DiScenna P (1987) Long-term potentiation. Annu Rev Neurosci 10:131–161

    Article  PubMed  CAS  Google Scholar 

  • Thoroughman KA, Shadmehr R (2000) Learning of action through adaptive combination of motor primitives. Nature 407:742–747

  • Trepel C, Racine R (2000) GABAergic modulation of neocortical long-term potentiation in the freely moving rat. Synapse 128:120–128

    Article  Google Scholar 

  • Tyryshkin K, Coderre AM, Glasgow JI, Herter TM, Bagg SD, Dukelow SP, Scott SH (2014) A robotic object hitting task to quantify sensorimotor impairments in participants with stroke. J Neuroeng Rehabil 11:47

    Article  PubMed  PubMed Central  Google Scholar 

  • Valentino F, Cosentino G, Brighina F, Pozzi NG, Sandrini G, Fierro B, Savettieri G, D’Amelio M, Pacchetti C (2014) Transcranial direct current stimulation for treatment of freezing of gait: a cross-over study. Mov Disord 00:1–5

    CAS  Google Scholar 

  • Vandermeeren Y, Lefebvre S, Desfontaines P, Laloux P (2013) Could dual-hemisphere transcranial direct current stimulation (tDCS) reduce spasticity after stroke? Acta Neurol Belg 113:87–89

    Article  PubMed  Google Scholar 

  • Verheyden G, Purdey J, Burnett M, Cole J, Ashburn A (2013) Immediate effect of transcranial direct current stimulation on postural stability and functional mobility in Parkinson’s disease. Mov Disord 28:2040–2041

    Article  PubMed  Google Scholar 

  • Villalta JI, Landi SM, Fló A, Della-Maggiore V (2013) Extinction interferes with the retrieval of visuomotor memories through a mechanism involving the sensorimotor cortex. Cereb Cortex. doi:10.1093/cercor/bht346

  • Vines BW, Nair DG, Schlaug G (2006) Contralateral and ipsilateral motor effects after transcranial direct current stimulation. NeuroReport 17:671–674

    Article  PubMed  Google Scholar 

  • Vines BW, Cerruti C, Schlaug G (2008a) Dual-hemisphere tDCS facilitates greater improvements for healthy subjects’ non-dominant hand compared to uni-hemisphere stimulation. BMC Neurosci 9:103

    Article  PubMed  PubMed Central  Google Scholar 

  • Vines BW, Nair DG, Schlaug G (2008b) Modulating activity in the motor cortex affects performance for the two hands differently depending upon which hemisphere is stimulated. Eur J Neurosci 28:1667–1673

    Article  PubMed  Google Scholar 

  • Von Kraus LM, Sacktor TC, Francis JT (2010) Erasing sensorimotor memories via PKMzeta inhibition. PLoS ONE 5:e11125

    Article  CAS  Google Scholar 

  • Voronin L (1968) Action of surface polarization on intracellular unit activity in the motor cortex of waking rabbits. Neurosci Behav Physiol 18:691–698

    Article  Google Scholar 

  • Wang L, Conner JM, Rickert J, Tuszynski MH (2011) Structural plasticity within highly specific neuronal populations identifies a unique parcellation of motor learning in the adult brain. Proc Natl Acad Sci USA 108:1–6

    Article  Google Scholar 

  • Ward NS (2003) Age-related changes in the neural correlates of motor performance. Brain 126:873–888

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Waters-Metenier S, Husain M, Wiestler T, Diedrichsen J (2014) Bihemispheric transcranial direct current stimulation enhances effector-independent representations of motor synergy and sequence learning. J Neurosci 34:1037–1050

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Williams JA, Pascual-Leone A, Fregni F (2010) Interhemispheric modulation induced by cortical stimulation and motor training. Phys Ther 90:398–410

    Article  PubMed  Google Scholar 

  • Xu T, Yu X, Perlik AJ, Tobin WF, Zweig JA, Tennant KA, Jones T, Zuo Y (2009) Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 462:915–919

  • Yang G, Pan F, Gan W-B (2009) Stably maintained dendritic spines are associated with lifelong memories. Nature 462:920–924

    Article  PubMed  CAS  Google Scholar 

  • Yu X, Zuo Y (2010) Spine plasticity in the motor cortex. Curr Opin Neurobiol 21:169–174

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zimerman M, Heise KF, Hoppe J, Cohen LG, Gerloff C, Hummel FC (2012) Modulation of training by single-session transcranial direct current stimulation to the intact motor cortex enhances motor skill acquisition of the paretic hand. Stroke 43:2185–2191

    Article  PubMed  Google Scholar 

  • Zimerman M, Nitsch M, Giraux P, Gerloff C, Cohen LG, Hummel FC (2013) Neuroenhancement of the aging brain: restoring skill acquisition in old subjects. Ann Neurol 73:10–15

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by NIH grant R01 NS078311. JJOdX is supported by a Brains Back to Brussels fellowship from the Brussels Region (Belgium).

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Orban de Xivry, JJ., Shadmehr, R. Electrifying the motor engram: effects of tDCS on motor learning and control. Exp Brain Res 232, 3379–3395 (2014). https://doi.org/10.1007/s00221-014-4087-6

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  • DOI: https://doi.org/10.1007/s00221-014-4087-6

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