Anodal tDCS over the supplementary motor area increases motor overflow during imagined aiming movement
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Abstract
Neural networks subserving motor imagery and action observation overlap with those involved in motor execution. The precise roles of specific cortical areas in these processes are not fully understood. One cortical area implicated in motor imagery is the supplementary motor area (SMA). To test the role of SMA in motor imagery, participants without any known neurological disorders (N = 23) completed three versions of a reciprocal manual aiming task (imagined, observed, and executed movements) before and after transcranial direct current stimulation (tDCS) was applied to the SMA. Anodal, cathodal, and sham (inactive) stimulation protocols were compared within participants. Although the speed-accuracy trade-off observed in the aiming task was not affected by tDCS, the amount of incidental movement during imagery (motor overflow) increased following anodal stimulation. Additionally, imagined movement time was associated less strongly with an implicit measure of motor imagery (hand laterality judgement) following anodal tDCS compared to the sham condition. No effects of tDCS were found for action observation or movement execution. These results suggest that anodal stimulation applied over SMA may subtly disrupt processes underlying motor imagery, either through unintended inhibitory effects or via excitatory effects on adjacent areas of the motor cortex.
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References
Bek J, Gowen E, Vogt S, Crawford TJ, Poliakoff E (2019) Combined action observation and motor imagery influences hand movement amplitude in Parkinson’s disease. Parkinsonism Relat Disord. https://doi.org/10.1016/j.parkreldis.201811001
Bek J, Holmes PS, Craig CE, Franklin ZC, Sullivan M, Webb J, Crawford TJ, Vogt S, Gowen E, Poliakoff E (2021) Action imagery and observation in neurorehabilitation for Parkinson’s disease (ACTION-PD): development of a user-informed home training intervention to improve functional hand movements. Parkinson’s Dis 2021:1–14. https://doi.org/10.1155/2021/4559519
Bek J, Humphries S, Poliakoff E, Brady N (2022) Mental rotation of hands and objects in ageing and Parkinson’s disease: differentiating motor imagery and visuospatial ability. Exp Brain Res 240(7):1991–2004. https://doi.org/10.1007/s00221-022-06389-5
Blampain J, Ott L, Delevoye-Turrell YN (2018) Seeing action simulation as it unfolds: the implicit effects of action scenes on muscle contraction evidenced through the use of a grip-force sensor. Neuropsychologia 114:231–242. https://doi.org/10.1016/j.neuropsychologia.2018年04月02日6
Bolzoni F, Bruttini C, Esposti R, Castellani C, Cavallari P (2015) Transcranial direct current stimulation of SMA modulates anticipatory postural adjustments without affecting the primary movement. Behav Brain Res 291:407–413. https://doi.org/10.1016/j.bbr.2015年05月04日4
Borges LR, Fernandes AB, Melo LP, Guerra RO, Campos TF (2018) Action observation for upper limb rehabilitation after stroke. Cochrane Database System Rev. https://doi.org/10.1002/14651858.CD011887.pub2
Brady N, Maguinness C, Choisdealbha ÁN (2011) My hand or yours? Markedly different sensitivity to egocentric and allocentric views in the hand laterality task. PLoS ONE. https://doi.org/10.1371/journal.pone.0023316
Caligiore D, Mustile M, Spalletta G, Baldassarre G (2017) Action observation and motor imagery for rehabilitation in Parkinson’s disease: a systematic review and an integrative hypothesis. Neurosci Biobehav Rev 72:210–222. https://doi.org/10.1016/j.neubiorev.201611005
Carlsen AN, Eagles JS, MacKinnon CD (2015) Transcranial direct current stimulation over the supplementary motor area modulates the preparatory activation level in the human motor system. Behav Brain Res 279:68–75. https://doi.org/10.1016/j.bbr.201411009
Caspers S, Zilles K, Laird AR, Eickhoff SB (2010) ALE meta-analysis of action observation and imitation in the human brain. Neuroimage 50(3):1148–1167. https://doi.org/10.1016/j.neuroimage.2009年12月11日2
Cerritelli B, Maruff P, Wilson P, Currie J (2000) The effect of an external load on the force and timing components of mentally represented actions. Behav Brain Res 108(1):91–96. https://doi.org/10.1016/S0166-4328(99)00138-2
Chandrasekharan S, Binsted G, Ayres F, Higgins L, Welsh TN (2012) Factors that affect action possibility judgements: recent experience with the action and the current body state. Q J Exp Psychol 65(5):976–993. https://doi.org/10.1080/17470218.2011.638720
Chye S, Valappil AC, Wright DJ, Frank C, Shearer DA, Tyler CJ, Diss CE, Mian OS, Tillin NA, Bruton AM (2022) The effects of combined action observation and motor imagery on corticospinal excitability and movement outcomes: two meta-analyses. Neurosci Biobehav Rev 143:104911. https://doi.org/10.1016/j.neubiorev.2022.104911
Conson M, De Bellis F, Baiano C, Zappullo I, Raimo G, Finelli C, Ruggiero I, Positano M, Trojano L (2020) Sex differences in implicit motor imagery: evidence from the hand laterality task. Acta Psychol. https://doi.org/10.1016/j.actpsy.2020.103010
Conson M, Volpicella F, De Bellis F, Orefice A, Trojano L (2017) Like the palm of my hands": motor imagery enhances implicit and explicit visual recognition of one’s own hands. Acta Psychol. https://doi.org/10.1016/j.actpsy.201709006
Cross ES, Kraemer DJM, Hamilton AFD, Kelley WM, Grafton ST (2009) Sensitivity of the action observation network to physical and observational learning. Cereb Cortex 19(2):315–326. https://doi.org/10.1093/cercor/bhn083
Date S, Kurumadani H, Watanabe T, Sunagawa T (2015) Transcranial direct current stimulation can enhance ability in motor imagery tasks. NeuroReport 26(11):613–617
De Waal FB, Preston SD (2017) Mammalian empathy: behavioural manifestations and neural basis. Nat Rev Neurosci 18(8):498–509
Di Rienzo F, Debarnot U, Daligault S, Saruco E, Delpuech C, Doyon J, Collet C, Guillot A (2016) Online and offline performance gains following motor imagery practice: a comprehensive review of behavioral and neuroimaging studies. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2016.00315
Dum RP, Strick PL (2002) Motor areas in the frontal lobe of the primate. Physiol Behav 77(4):677–682. https://doi.org/10.1016/S0031-9384(02)00929-0
Evans C, Zich C, Lee JSA, Ward N, Bestmann S (2022) Inter-individual variability in current direction for common tDCS montages. Neuroimage 260:119501. https://doi.org/10.1016/j.neuroimage.2022.119501
Filmer HL, Dux PE, Mattingley JB (2014) Applications of transcranial direct current stimulation for understanding brain function. Trends Neurosci 37(12):742–753. https://doi.org/10.1016/j.tins.201408003
Fitts PM (1954) The information capacity of the human motor system in controlling the amplitude of movement. J Exp Psychol 47(6):381–391. https://doi.org/10.1037/h0055392
Glover S, Baran M (2017) The motor-cognitive model of motor imagery: evidence from timing errors in simulated reaching and grasping. J Exp Psychol Hum Percep Perf 43(7):1359
Glover S, Bibby E, Tuomi E (2020) Executive functions in motor imagery: support for the motor-cognitive model over the functional equivalence model. Exp Brain Res 238(4):931–944. https://doi.org/10.1007/s00221-020-05756-4
Goldberg G (1985) Supplementary motor area structure and function: review and hypotheses. Behav Brain Sci 8(4):567–588. https://doi.org/10.1017/S0140525X00045167
Grosjean M, Shiffrar M, Knoblich G (2007) Fitts’s law holds for action perception. Psychol Sci 18(2):95–99. https://doi.org/10.1111/j.1467-9280.2007.01854.x
Grush R (2004) The emulation theory of representation: Motor control, imagery, and perception. Behav Brain Sci 27(3):377–396. https://doi.org/10.1017/S0140525X04000093
Guidali G, Arrigoni E, Bolognini N, Pisoni A (2025) M1 large-scale network dynamics support human motor resonance and its plastic reshaping. Neuroimage 308:121082. https://doi.org/10.1016/j.neuroimage.2025.121082
Guillot A, Rienzo FD, Frank C, Debarnot U, MacIntyre TE (2024) From simulation to motor execution: a review of the impact of dynamic motor imagery on performance. Int Rev Sport Exerc Psychol 17(1):420–439. https://doi.org/10.1080/1750984X.2021.2007539
Hardwick RM, Caspers S, Eickhoff SB, Swinnen SP (2018) Neural correlates of action: comparing meta-analyses of imagery, observation, and execution. Neurosci Biobehav Rev 94:31–44. https://doi.org/10.1016/J.NEUBIOREV.201808003
Hassanzahraee M, Nitsche MA, Zoghi M, Jaberzadeh S (2020) Determination of anodal tDCS duration threshold for reversal of corticospinal excitability: an investigation for induction of counter-regulatory mechanisms. Brain Stimul 13(3):832–839. https://doi.org/10.1016/j.brs.2020年02月02日7
Hayduk-Costa G, Drummond NM, Carlsen AN (2013) Anodal tDCS over SMA decreases the probability of withholding an anticipated action. Behav Brain Res 257:208–214. https://doi.org/10.1016/j.bbr.2013年09月03日0
Holmes P, Calmels C (2008) A neuroscientific review of imagery and observation use in sport. J Motor Behav. https://doi.org/10.3200/JMBR.40.5.433-445
Huang Y, Datta A, Bikson M, Parra LC (2019) Realistic volumetric-approach to simulate transcranial electric stimulation—ROAST—a fully automated open-source pipeline. J Neural Eng 16(5):056006
Hupfeld KE, Ketcham CJ, Schneider HD (2017) Transcranial direct current stimulation (tDCS) to the supplementary motor area(SMA) influences performance on motor tasks. Exp Brain Res 235(3):851–859. https://doi.org/10.1007/s00221-016-4848-5
Hurst AJ, Boe SG (2022) Imagining the way forward: a review of contemporary motor imagery theory. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2022.1033493
Jeannerod M (2001) Neural simulation of action: a unifying mechanism for motor cognition. Neuroimage 14(1):S103–S109. https://doi.org/10.1006/nimg.2001.0832
Karabanov AN, Saturnino GB, Thielscher A, Siebner HR (2019) Can transcranial electrical stimulation localize brain function? Front Psychol. https://doi.org/10.3389/fpsyg.2019.00213
Kasess CH, Windischberger C, Cunnington R, Lanzenberger R, Pezawas L, Moser E (2008) The suppressive influence of SMA on M1 in motor imagery revealed by fMRI and dynamic causal modeling. Neuroimage 40(2):828–837. https://doi.org/10.1016/j.neuroimage.2007年11月04日0
Kim YK, Shin SH (2014) Comparison of effects of transcranial magnetic stimulation on primary motor cortex and supplementary motor area in motor skill learning (randomized, cross over study). Front Human Neurosci 8. https://doi.org/10.3389/fnhum.2014.00937
Kirimoto H, Yoshida S, Matsumoto T, Kojima S, Suzuki M, Onishi H, Tamaki H (2013) P 71. The effects of cathodal transcranial direct current stimulation of the supplementary motor area on the function of anticipatory postural adjustments. Clin Neurophysiol 124(10):e98–e99. https://doi.org/10.1016/j.clinph.2013年04月14日9
Koski L, Wohlschläger A, Bekkering H, Woods RP, Dubeau M-C, Mazziotta JC, Iacoboni M (2002) Modulation of motor and premotor activity during imitation of target-directed actions. Cereb Cortex 12(8):847–855. https://doi.org/10.1093/cercor/12.8.847
Kraeutner SN, Eppler SN, Stratas A, Boe SG (2020) Generate, maintain, manipulate? Exploring the multidimensional nature of motor imagery. Psychol Sport Exercise. https://doi.org/10.1016/j.psychsport.2020.101673
Lapenta O, Minati L, Fregni F, Boggio P (2013) Je pense donc je fais: Transcranial direct current stimulation modulates brain oscillations associated with motor imagery and movement observation. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2013.00256
Martel M, Glover S (2023) TMS over dorsolateral prefrontal cortex affects the timing of motor imagery but not overt action: further support for the motor-cognitive model. Behav Brain Res 437:114125. https://doi.org/10.1016/j.bbr.2022.114125
Meers R, Nuttall HE, Vogt S (2020) Motor imagery alone drives corticospinal excitability during concurrent action observation and motor imagery. Cortex 126:322–333. https://doi.org/10.1016/j.cortex.2020年01月01日2
Mehler DMA, Williams AN, Krause F, Lührs M, Wise RG, Turner DL, Linden DEJ, Whittaker JR (2019) The BOLD response in primary motor cortex and supplementary motor area during kinesthetic motor imagery based graded fMRI neurofeedback. Neuroimage 184:36–44. https://doi.org/10.1016/j.neuroimage.201809007
Moghadas Tabrizi Y, Yavari M, Shahrbanian S, Gharayagh Zandi H (2019) Transcranial direct current stimulation on prefrontal and parietal areas enhances motor imagery. NeuroReport 30(9):653–657. https://doi.org/10.1097/WNR.0000000000001253
Moran A, O’Shea H (2019) Motor imagery practice and skilled performance in sport: from efficacy to mechanisms. In: Skill acquisition in sport. 3rd ed). Routledge
Morya E, Monte-Silva K, Bikson M, Esmaeilpour Z, Biazoli CE, Fonseca A, Bocci T, Farzan F, Chatterjee R, Hausdorff JM, da Silva Machado DG, Brunoni AR, Mezger E, Moscaleski LA, Pegado R, Sato JR, Caetano MS, Sá KN, Tanaka C, Okano AH (2019) Beyond the target area: an integrative view of tDCS-induced motor cortex modulation in patients and athletes. J Neuroeng Rehabil 16(1):141. https://doi.org/10.1186/s12984-019-0581-1
Nachev P, Kennard C, Husain M (2008) Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 9(11):856–869. https://doi.org/10.1038/nrn2478
Neige C, Massé-Alarie H, Mercier C (2018) Stimulating the healthy brain to investigate neural correlates of motor preparation: a systematic review. Neural Plast 2018(1):5846096. https://doi.org/10.1155/2018/5846096
Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, Paulus W, Hummel F, Boggio PS, Fregni F, Pascual-Leone A (2008) Transcranial direct current stimulation: state of the art 2008. Brain Stimul 1(3):206–223. https://doi.org/10.1016/j.brs.200806004
Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57(10):1899–1901. https://doi.org/10.1212/WNL.57.10.1899
Nomura T, Kirimoto H (2018) Anodal transcranial direct current stimulation over the supplementary motor area improves anticipatory postural adjustments in older adults. Front Human Neurosci 12. https://doi.org/10.3389/fnhum.2018.00317
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113. https://doi.org/10.1016/0028-3932(71)90067-4
Parsons LM (1994) Temporal and kinematic properties of motor behavior reflected in mentally simulated action. J Exp Psychol Hum Percept Perform 20(4):709–730. https://doi.org/10.1037/0096-1523204.709
Pathak A, Patel S, Karlinsky A, Taravati S, Welsh TN (2023) The "eye" in imagination: the role of eye movements in a reciprocal aiming task. Behav Brain Res 441:114261. https://doi.org/10.1016/j.bbr.2022.114261
Peirce J, Gray JR, Simpson S, MacAskill M, Höchenberger R, Sogo H, Kastman E, Lindeløv JK (2019) PsychoPy2: experiments in behavior made easy. Behav Res Methods 51(1):195–203. https://doi.org/10.3758/s13428-018-01193-y
Poldrack RA (2006) Can cognitive processes be inferred from neuroimaging data? Trends Cogn Sci 10(2):59–63. https://doi.org/10.1016/j.tics.200512004
Ray M, Dewey D, Kooistra L, Welsh TN (2013) The relationship between the motor system activation during action observation and adaptation in the motor system following repeated action observation. Hum Mov Sci 32(3):400–411. https://doi.org/10.1016/J.HUMOV.201202003
Roberts JW, Constable MD, Burgess R, Lyons JL, Welsh TN (2018) The influence of intrapersonal sensorimotor experiences on the corticospinal responses during action–observation. Soc Neurosci 13(2):246–256. https://doi.org/10.1080/17470919.2017.1289979
Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120(12):2008–2039. https://doi.org/10.1016/j.clinph.2009年08月01日6
Sadler CM, Kami AT, Nantel J, Carlsen AN (2021) Transcranial direct current stimulation of supplementary motor area improves upper limb kinematics in Parkinson’s disease. Clin Neurophysiol 132(11):2907–2915. https://doi.org/10.1016/j.clinph.2021年06月03日1
Scott MW, Wood G, Holmes PS, Williams J, Marshall B, Wright DJ (2021) Combined action observation and motor imagery: an intervention to combat the neural and behavioural deficits associated with developmental coordination disorder. Neurosci Biobehav Rev 127:638–646
Sevdalis V, Raab M (2014) Empathy in sports, exercise, and the performing arts. Psychol Sport Exerc 15(2):173–179. https://doi.org/10.1016/j.psychsport.2013年10月01日3
Siebner HR, Lang N, Rizzo V, Nitsche MA, Paulus W, Lemon RN, Rothwell JC (2004) Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J Neurosci 24(13):3379–3385. https://doi.org/10.1523/JNEUROSCI.5316-03.2004
Solodkin A, Hlustik P, Chen EE, Small SL (2004) Fine modulation in network activation during motor execution and motor imagery. Cereb Cortex 14(11):1246–1255. https://doi.org/10.1093/cercor/bhh086
Stagg CJ, Antal A, Nitsche MA (2018) Physiology of transcranial direct current stimulation. J ECT 34(3):144. https://doi.org/10.1097/YCT.0000000000000510
Tak S, Kempny AM, Friston KJ, Leff AP, Penny WD (2015) Dynamic causal modelling for functional near-infrared spectroscopy. Neuroimage 111:338–349. https://doi.org/10.1016/j.neuroimage.2015年02月03日5
Team RC (2021) R Core Team 2021. R: A Language and Environment for Statistical Computing
Temporiti F, Adamo P, Cavalli E, Gatti R (2020) Efficacy and characteristics of the stimuli of action observation therapy in subjects with Parkinson’s disease: a systematic review. Front Neurol 11:808. https://doi.org/10.3389/fneur.2020.00808
Veldema J, Gharabaghi A, Jansen P (2021) Non-invasive brain stimulation in modulation of mental rotation ability: a systematic review and meta-analysis. Eur J Neurosci 54(10):7493–7512. https://doi.org/10.1111/ejn.15490
Vogt S, Di Rienzo F, Collet C, Collins A, Guillot A (2013) Multiple roles of motor imagery during action observation. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2013.00807
Vollmann H, Conde V, Sewerin S, Taubert M, Sehm B, Witte OW, Villringer A, Ragert P (2013) Anodal transcranial direct current stimulation (tDCS) over supplementary motor area (SMA) but not pre-SMA promotes short-term visuomotor learning. Brain Stimul 6(2):101–107. https://doi.org/10.1016/j.brs.2012年03月01日8
Wang XM, Welsh TN (2024) TAT-HUM: trajectory analysis toolkit for human movements in Python. Behav Res Methods. https://doi.org/10.3758/s13428-024-02378-4
Wong L, Manson GA, Tremblay L, Welsh TN (2013) On the relationship between the execution, perception, and imagination of action. Behav Brain Res 257:242–252. https://doi.org/10.1016/j.bbr.2013年09月04日5
Yang K, Xi X, Wang T, Wang J, Kong W, Zhao Y-B, Zhang Q (2021) Effects of transcranial direct current stimulation on brain network connectivity and complexity in motor imagery. Neurosci Lett 757:135968. https://doi.org/10.1016/j.neulet.2021.135968
Yoxon E, Pacione SM, Song J-H, Welsh TN (2017) The action-specific effect of execution on imagination of reciprocal aiming movements. Hum Mov Sci 54:51–62. https://doi.org/10.1016/j.humov.201703007
Yoxon E, Welsh TN (2019) Rapid motor cortical plasticity can be induced by motor imagery training. Neuropsychologia. https://doi.org/10.1016/J.NEUROPSYCHOLOGIA.2019.107206
Acknowledgements
The authors thank Maryam Hassanzahraee, Joyce Chen, and Bisman Mangat for feedback on study design and interpretation, and Sydney Winokur and Zheng Tan for assistance with data processing and modelling.
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This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC). J. Bek was also supported by funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No. 101034345.
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Bek, J., Wang, X.M. & Welsh, T.N. Anodal tDCS over the supplementary motor area increases motor overflow during imagined aiming movement. Exp Brain Res 243, 248 (2025). https://doi.org/10.1007/s00221-025-07196-4
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