Combining Motor Imagery and Action Observation with Vibratory Stimulation Increases Corticomotor Excitability in Healthy Young Adults — Oak Academic Publishing
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Combining Motor Imagery and Action Observation with Vibratory Stimulation Increases Corticomotor Excitability in Healthy Young Adults
Center for Information and Neural Networks (CiNet), Advanced ICT Research Institute, National Institute of Information and Communications Technology (NICT), Osaka, Japan
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Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan
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Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan
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Center for Information and Neural Networks (CiNet), Advanced ICT Research Institute, National Institute of Information and Communications Technology (NICT), Osaka, Japan
1 Center for Information and Neural Networks (CiNet), Advanced ICT Research Institute, National Institute of Information and Communications Technology (NICT), Osaka, Japan
2 Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan
3 Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan
4 Center for Information and Neural Networks (CiNet), Advanced ICT Research Institute, National Institute of Information and Communications Technology (NICT), Osaka, Japan
Vibratory stimulation but also motor imagery and action observation can induce corticomotor modulation, as a bottom-up stimulus and top-down stimuli, respectively. However, it remains unknown whether the combination of motor imagery, action observation, and vibratory stimulation can effectively increase corticomotor excitability. This study aimed to investigate the effect of motor imagery and/or action observation, in the presence or absence of vibratory stimulation, on the corticomotor excitability of healthy young adults. Vibratory stimulation was provided to the palm of the right hand. Action observation consisted in viewing a movie of someone else’s finger flexion and extension movements. The imagery condition required the participants to imagine they were moving their fingers while viewing the movie and attempting to move their fingers in accordance with the movie. Eleven right-handed healthy young adults were asked to perform six conditions randomly: 1) vibratory stimulation, imagery, and action observation, 2) vibratory stimulation and action observation, 3) vibratory stimulation and viewing of a blank screen, 4) imagery and action observation, 5) action observation, and 6) viewing of a blank screen. Single-pulse transcranial magnetic stimulation was conducted to assess corticomotor excitability and the peak-to-peak amplitude of the motor evoked potentials. The results showed that vibratory stimulation increases corticospinal excitability. The findings further revealed that performing motor imagery while viewing finger movement is more effective at inducing an augmentation of corticomotor excitability compared to action observation alone. Thus, the combination of motor imagery, action observation, and vibratory stimulation can effectively augment corticomotor excitability.
KeywordsMotor Evoked PotentialTranscranial Magnetic StimulationVibratory StimulationMotor ImageryAction Observation
Kaelin-Lang, A., Luft, A.R., Sawaki, L., Burstein, A.H., Sohn, Y.H. and Cohen, L.G. (2002) Modulation of Human Corticomotor Excitability by Somatosensory Input. Journal of Physiology, 540, 623-633. https://doi.org/10.1113/jphysiol.2001.012801
Hamdy, S., Rothwell, J.C., Aziz, Q., Singh, K.D. and Thompson, D.G. (1998) Long-Term Reorganization of Human Motor Cortex Driven by Short-Term Sensory Stimulation. Nature Neuroscience, 1, 64-68. https://doi.org/10.1038/264
Vidoni, E.D., Acerra, N.E., Dao, E., Meehan, S.K. and Boyd, L.A. (2010) Role of the Primary Somatosensory Cortex in Motor Learning: An rTMS Study. Neurobiology of Learning and Memory, 93, 532-539. https://doi.org/10.1016/j.nlm.2010.01.011
Rosenkranz, K. and Rothwell, J.C. (2012) Modulation of Proprioceptive Integration in the Motor Cortex Shapes Human Motor Learning. Journal of Neuroscience, 32, 9000-9006. https://doi.org/10.1523/JNEUROSCI.0120-12.2012
Goodwin, G.M., McCloskey, D.I. and Matthews, P.B. (1972) The Contribution of Muscle Afferents to Kinaesthesia Shown by Vibration Induced Illusions of Movement and by the Effects of Paralysing Joint Afferents. Brain, 95, 705-748. https://doi.org/10.1093/brain/95.4.705
Burke, D., Hagbarth, K.E., Löfstedt, L. and Wallin, B.G. (1976) The Responses of Human Muscle Spindle Endings to Vibration of Non-Contracting Muscles. Journal of Physiology, 261, 673-693. https://doi.org/10.1113/jphysiol.1976.sp011580
Roll, J.P. and Vedel, J.P. (1982) Kinaesthetic Role of Muscle Afferents in Man, Studied by Tendon Vibration and Microneurography. Experimental Brain Research, 47, 177-190. https://doi.org/10.1007/BF00239377
Roll, J.P., Vedel, J.P. and Ribot, E. (1989) Alteration of Proprioceptive Messages Induced by Tendon Vibration in Man: a Microneurographic Study. Experimental Brain Research, 76, 213-222. https://doi.org/10.1007/BF00253639
Calvin-Figuière, S., Romaiguère, P., Gilhodes, J.C. and Roll, J.P. (1999) Antagonist Motor Responses Correlate with Kinesthetic Illusions Induced by Tendon Vibration. Experimental Brain Research, 124, 342-350. https://doi.org/10.1007/s002210050631
Siggelkow, S., Kossev, A., Schubert, M., Kappels, H.H., Wolf, W. and Dengler, R. (1999) Modulation of Motor Evoked Potentials by Muscle Vibration: The Role of Vibration Frequency. Muscle and Nerve, 22, 1544-1548. https://doi.org/10.1002/(SICI)1097-4598(199911)22:11 3.0.CO;2-8
Steyvers, M., Levin, O., Verschueren, S.M. and Swinnen, S.P. (2003) Frequency-Dependent Effects of Muscle Tendon Vibration on Corticospinal Excitability: A TMS Study. Experimental Brain Research, 151, 9-14. https://doi.org/10.1007/s00221-003-1427-3
Steyvers, M., Levin, O., Van Baelen, M. and Swinnen, S.P. (2003) Corticospinal Excitability Changes Following Prolonged Muscle Tendon Vibration. NeuroReport, 14, 1901-1905. https://doi.org/10.1097/00001756-200310270-00004
Forner-Cordero, A., Steyvers, M., Levin, O., Alaerts, K. and Swinnen, S.P. (2008) Changes in Corticomotor Excitability Following Prolonged Muscle Tendon Vibration. Behavioural Brain Research, 190, 41-49. https://doi.org/10.1016/j.bbr.2008.02.019
De Gail, P., Lance, J.W. and Neilson, P.D. (1966) Differential Effects on Tonic and Phasic Reflex Mechanisms Produced by Vibration of Muscles in Man. Journal of Neurology, Neurosurgery, and Psychiatry, 29, 1-11. https://doi.org/10.1136/jnnp.29.1.1
Martin, B.J. and Park, H.S. (1997) Analysis of the Tonic Vibration Reflex: Influence of Vibration Variables on Motor Unit Synchronization and Fatigue. European Journal of Applied Physiology and Occupational Physiology, 75, 504-511. https://doi.org/10.1007/s004210050196
Murillo, N., Valls-Sole, J., Vidal, J., Opisso, E., Medina, J. and Kumru, H. (2014) Focal Vibration in Neurorehabilitation. European Journal of Physical and Rehabilitation Medicine, 50, 231-242.
Deuschl, G., Ludolph, A., Schenck, E. and Lücking, C.H. (1989) The Relations between Long-Latency Reflexes in Hand Muscles, Somatosensory Evoked Potentials and Transcranial Stimulation of Motor Tracts. Electroencephalography and Clinical Neurophysiology, 74, 425-430. https://doi.org/10.1016/0168-5597(89)90031-2
MacKinnon, C.D., Verrier, M.C. and Tatton, W.G. (2000) Motor Cortical Potentials Precede Long-Latency EMG Activity Evoked by Imposed Displacements of the Human Wrist. Experimental Brain Research, 131, 477-490. https://doi.org/10.1007/s002219900317
Lewis, G.N., Polych, M.A. and Byblow, W.D. (2004) Proposed Cortical and Sub-Cortical Contributions to the Long-Latency Stretch Reflex in the Forearm. Experimental Brain Research, 156, 72-79. https://doi.org/10.1007/s00221-003-1767-z
Pruszynski, J.A., Kurtzer, I. and Scott, S.H. (2011) The Long-Latency Reflex Is Composed of at Least Two Functionally Independent Processes. Journal of Neurophysiology, 106, 449-459. https://doi.org/10.1152/jn.01052.2010
Roll, J.P., Gilhodes, J.C. and Tardy-Gervet, M.F. (1980) Perceptive and Motor Effects of Muscular Vibrations in the Normal Human: Demonstration of a Response by Opposing Muscles. Archives Italiennes de Biologie, 118, 51-71.
Feldman, A.G. and Latash, M.L. (1982) Inversions of Vibration-Induced Senso-Motor Events Caused by Supraspinal Influences in Man. Neuroscience Letters, 31, 147-151. https://doi.org/10.1016/0304-3940(82)90107-0
Mulder, T. (2007) Motor Imagery and Action Observation: Cognitive Tools for Rehabilitation. Journal of Neural Transmission, 114, 1265-1278. https://doi.org/10.1007/s00702-007-0763-z
Jeannerod, M. (1994) The Representing Brain: Neural Correlates of Motor Intention and Imagery. Behavioral and Brain Sciences, 17, 187-202. https://doi.org/10.1017/S0140525X00034026
Jeannerod, M. (1995) Mental Imagery in the Motor Context. Neuropsychologia, 33, 1419-1432. https://doi.org/10.1016/0028-3932(95)00073-C
Fadiga, L., Buccino, G., Craighero, L., Fogassi, L., Gallese, V. and Pavesi, G. (1999) Corticospinal Excitability Is Specifically Modulated by Motor Imagery: A Magnetic Stimulation Study. Neuropsychologia, 37, 147-158. https://doi.org/10.1016/S0028-3932(98)00089-X
Lotze, M. and Cohen, L.G. (2006) Volition and Imagery in Neurorehabilitation. Cognitive and Behavioral Neurology, 19, 135-140. https://doi.org/10.1097/01.wnn.0000209875.56060.06
Lotze, M. and Halsband, U. (2006) Motor Imagery. Journal of Physiology, Paris, 99, 386-395. https://doi.org/10.1016/j.jphysparis.2006.03.012
Naito, E., Kochiyama, T., Kitada, R., Nakamura, S., Matsumura, M., Yonekura, Y. and Sadato, N. (2002) Internally Simulated Movement Sensations during Motor Imagery Activate Cortical Motor Areas and the Cerebellum. Journal of Neuroscience, 22, 3683-3691. https://doi.org/10.1523/JNEUROSCI.22-09-03683.2002
Leonardo, M., Fieldman, J., Sadato, N., Campbell, G., Ibañez, V., Cohen, L., Deiber, M.P., Jezzard, P., Pons, T., Turner, R., Le Bihan, D. and Hallett, M. (1995) A Functional MagenticResonance Imaging Study of Cortical Regions Associated with Motor Task Execution and Motor Ideation in Humans. Human Brain Mapping, 3, 83-92. https://doi.org/10.1002/hbm.460030205
Sabbah, P., Simond, G., Levrier, O., Habib, M., Trabaud, V., Murayama, N., Mazoyer, B.M., Briant, J.F., Raybaud, C. and Salamon, G. (1995) Functional Magnetic Resonance Imaging at 1.5 T during Sensory Motor and Cognitive Tasks. European Neurology, 35, 131-136. https://doi.org/10.1159/000117108
Porro, C.A., Francescato, M.P., Cettolo, V., Diamond, M.E., Baraldi, P., Zuiani, C., Bazzocchi, M. and di Prampero, P.E. (1996) Primary Motor and Sensory Cortex Activation during Motor Performance and Motor Imagery: A Functional Magnetic Resonance Imaging Study. Journal of Neuroscience, 16, 7688-7698. https://doi.org/10.1159/000117108
Roth, M., Decety, J., Raybaudi, M., Massarelli, R., Delon-Martin, C., Segebarth, C., Morand, S., Gemignani, A., Décorps, M. and Jeannerod, M. (1996) Possible Involvement of Primary Motor Cortex in Mentally Simulated Movement: a Functional Magnetic Resonance Imaging Study. NeuroReport, 7, 1280-1284. https://doi.org/10.1097/00001756-199605170-00012
Lotze, M., Montoya, P., Erb, M., Hülsmann, E., Flor, H., Klose, U., Birbaumer, N. and Grodd, W. (1999) Activation of Cortical and Cerebellar Motor Areas during Executed and Imagined Hand Movements: an fMRI Study. Journal of Cognitive Neuroscience, 11, 491-501. https://doi.org/10.1162/089892999563553
Gerardin, E., Sirigu, A., Lehéricy, S., Poline, J.B., Gaymard, B., Marsault, C., Agid, Y. and Le Bihan, D. (2000) Partially Overlapping Neural Networks for Real and Imagined Hand Movements. Cerebral Cortex, 10, 1093-1104. https://doi.org/10.1093/cercor/10.11.1093
Nair, D.G., Purcott, K.L., Fuchs, A., Steinberg, F. and Kelso, J.A.S. (2003) Cortical and Cerebellar Activity of the Human Brain during Imagined and Executed Unimanual and Bimanual Movement Sequences. A Functional MRI Study. Cognitive Brain Research, 15, 250-260. https://doi.org/10.1016/S0926-6410(02)00197-0
Roland, P.E., Larsen, B., Lassen, N.A. and Skinhøj, E. (1980) Supplementary Motor Area and Other Cortical Areas in Organization of Voluntary Movements in Man. Journal of Neurophysiology, 43, 118-136. https://doi.org/10.1152/jn.1980.43.1.118
Stephan, K.M., Fink, G.R., Passingham, R.E., Silbersweig, D., Ceballos-Baumann, A.O., Frith, C.D. and Frackowiak, R.S.J. (1995) Functional Anatomy of the Mental Representation of Upper Extremity Movements in Healthy Subjects. Journal of Neurophysiology, 73, 373-386. https://doi.org/10.1152/jn.1995.73.1.373
Dechent, P., Merboldt, K.D. and Frahm, J. (2004) Is the Human Primary Motor Cortex Involved in Motor Imagery? Brain Research. Cognitive Brain Research, 19, 138-144. Erratum in: Brain Research. Cognitive Brain Research (2004), 20, 533. https://doi.org/10.1016/j.cogbrainres.2004.05.001
Guillot, A., Collet, C., Nguyen, V.A., Malouin, F., Richards, C. and Doyon, J. (2009) Brain Activity during Visual versus Kinesthetic Imagery: An fMRI Study. Human Brain Mapping, 30, 2157-2172. https://doi.org/10.1002/hbm.20658
Olsson, C.J., Jonsson, B., Larsson, A. and Nyberg, L. (2008) Motor Representations and Practice Affect Brain Systems Underlying Imagery: An FMRI Study of Internal Imagery in Novices and Active High Jumpers. Open Neuroimaging Journal, 2, 5-13. https://doi.org/10.2174/1874440000802010005
Hanakawa, T., Immisch, I., Toma, K., Dimyan, M.A., Van Gelderen, P. and Hallett, M. (2003) Functional Properties of Brain Areas Associated with Motor Execution and Imagery. Journal of Neurophysiology, 89, 989-1002. https://doi.org/10.1152/jn.00132.2002
Hétu, S., Grégoire, M., Saimpont, A., Coll, M.P., Eugène, F., Michon, P.E. and Jackson, P.L. (2013) The Neural Network of Motor Imagery: An ALE Meta-Analysis. Neuroscience and Biobehavioral Reviews, 37, 930-949. https://doi.org/10.1016/j.neubiorev.2013.03.017
Ruby, P. and Decety, J. (2003) What You Believe versus What You Think They Believe: a Neuroimaging Study of Conceptual Perspective-Taking. European Journal of Neuroscience, 17, 2475-2480. https://doi.org/10.1046/j.1460-9568.2003.02673.x
Solodkin, A., Hlustik, P., Chen, E.E. and Small, S.L. (2004) Fine Modulation in Network Activation during Motor Execution and Motor Imagery. Cerebral Cortex, 14, 1246-1255. https://doi.org/10.1093/cercor/bhh086
Stinear, C.M., Byblow, W.D., Steyvers, M., Levin, O. and Swinnen, S.P. (2006) Kinesthetic, but Not Visual, Motor Imagery Modulates Corticomotor Excitability. Experimental Brain Research, 168, 157-164. https://doi.org/10.1007/s00221-005-0078-y
Rizzolatti, G. and Craighero, L. (2004) The Mirror-Neuron System. Annual Review of Neuroscience, 27, 169-192. https://doi.org/10.1146/annurev.neuro.27.070203.144230
Fadiga, L., Craighero, L. and Olivier, E. (2005) Human Motor Cortex Excitability during the Perception of Others’ Action. Current Opinion in Neurobiology, 15, 213-218. https://doi.org/10.1016/j.conb.2005.03.013
Craighero, L., Metta, G., Sandini, G. and Fadiga, L. (2007) The Mirror-Neurons System: Data and Models. Progress in Brain Research, 164, 39-59. https://doi.org/10.1016/S0079-6123(07)64003-5
Keysers, C. and Fadiga, L. (2008) The Mirror Neuron System: New Frontiers. Social Neuroscience, 3, 193-198. https://doi.org/10.1080/17470910802408513
Fabbri-Destro, M. and Rizzolatti, G. (2008) Mirror Neurons and Mirror Systems in Monkeys and Humans. Physiology (Bethesda), 23, 171-179. https://doi.org/10.1152/physiol.00004.2008
Cattaneo, L. and Rizzolatti, G. (2009) The Mirror Neuron System. Archives of Neurology, 66, 557-560. https://doi.org/10.1001/archneurol.2009.41
Decety, J. and Boisson, D. (1990) Effect of Brain and Spinal Cord Injuries on Motor Imagery. European Archives of Psychiatry and Clinical Neuroscience, 240, 39-43. https://doi.org/10.1007/BF02190091
Dominey, P., Decety, J., Broussolle, E., Chazot, G. and Jeannerod, M. (1995) Motor Imagery of a Lateralized Sequential Task Is Asymmetrically Slowed in Hemi-Parkinson’s Patients. Neuropsychologia, 33, 727-741. https://doi.org/10.1016/0028-3932(95)00008-Q
McAvinue, L.P. and Robertson, I.H. (2008) Measuring Motor Imagery Ability: A Review. European Journal of Cognitive Psychology, 20, 232-251. https://doi.org/10.1080/09541440701394624
Rossini, P.M., Burke, D., Chen, R., Cohen, L.G., Daskalakis, Z., Di Iorio, R., Di Lazzaro, V., Ferreri, F., Fitzgerald, P.B., George, M.S., Hallett, M., Lefaucheur, J.P., Langguth, B., Matsumoto, H., Miniussi, C., Nitsche, M.A., Pascual-Leone, A., Paulus, W., Rossi, S., Rothwell, J.C., Siebner, H.R., Ugawa, Y., Walsh, V. and Ziemann, U. (2015) Non-Invasive Electrical and Magnetic Stimulation of the Brain, Spinal Cord, Roots and Peripheral Nerves: Basic Principles and Procedures for Routine Clinical and Research Application. An Updated Report from an I.F.C.N. Committee. Clinical Neurophysiology, 126, 1071-1107. https://doi.org/10.1016/j.clinph.2015.02.001
Faul, F., Erdfelder, E., Buchner, A. and Lang, A.G. (2009) Statistical Power Analyses Using G*Power 3.1: Tests for Correlation and Regression Analyses. Behavior Research Methods, 41, 1149-1160. https://doi.org/10.3758/BRM.41.4.1149
Oldfield, R.C. (1971) The Assessment and Analysis of Handedness: The Edinburgh Inventory. Neuropsychologia, 9, 97-113. https://doi.org/10.1016/0028-3932(71)90067-4
Zipp, P. (1982) Recommendations for the Standardization of Lead Positions in Surface Electromyography. European Journal of Applied Physiology and Occupational Physiology, 50, 41-54. https://doi.org/10.1007/BF00952243
Takala, E.P. and Toivonen, R. (2013) Placement of Forearm Surface EMG Electrodes in the Assessment of Hand Loading in Manual Tasks. Ergonomics, 56, 1159-1166. https://doi.org/10.1080/00140139.2013.799235
Poenaru, D., Cinteza, D., Petrusca, I., Cioc, L. and Dumitrascu, D. (2016) Local Application of Vibration in Motor Rehabilitation-Scientific and Practical Considerations. Maedica, 11, 227-231.
Yahagi, S. and Kasai, T. (1998) Facilitation of Motor Evoked Potentials (MEPs) in First Dorsal Interosseous (FDI) Muscle Is Dependent on Different Motor Images. Electroencephalography and Clinical Neurophysiology, 109, 409-417. https://doi.org/10.1016/S0924-980X(98)00041-1
Cavaleri, R. Schabrun, S.M. and Chipchase, L.S. (2015) Determining the Number of Stimuli Required to Reliably Assess Corticomotor Excitability and Primary Motor Cortical Representations Using Transcranial Magnetic Stimulation (TMS): A Protocol for a Systematic Review and Meta-Analysis. Systematic Reviews, 11, 107. https://doi.org/10.1186/s13643-015-0095-2
Cavaleri, R., Schabrun, S.M. and Chipchase, L.S. (2017) The Number of Stimuli Required to Reliably Assess Corticomotor Excitability and Primary Motor Cortical Representations Using Transcranial Magnetic Stimulation (TMS): A Systematic Review and Meta-Analysis. Systematic Reviews, 6, 48. https://doi.org/10.1186/s13643-017-0440-8
Claus, D., Mills, K.R. and Murray, N.M. (1988) Facilitation of Muscle Responses to Magnetic Brain Stimulation by Mechanical Stimuli in Man. Experimental Brain Research, 71, 273-278. https://doi.org/10.1007/BF00247487
Kossev, A., Siggelkow, S., Schubert, M., Wohlfarth, K. and Dengler, R. (1999) Muscle Vibration: Different Effects on Transcranial Magnetic and Electrical Stimulation. Muscle and Nerve, 22, 946-948. https://doi.org/10.1002/(SICI)1097-4598(199907)22:7 3.0.CO;2-O
Suzuki, T., Suzuki, M., Kanemura, N. and Hamaguchi, T. (2019) Differential Effect of Visual and Proprioceptive Stimulation on Corticospinal Output for Reciprocal Muscles. Frontiers in Integrative Neuroscience, 29, 13-63. https://doi.org/10.3389/fnint.2019.00063
Hashimoto, R. and Rothwell, J.C. (1999) Dynamic Changes in Corticospinal Excitability during Motor Imagery. Experimental Brain Research, 125, 75-81. https://doi.org/10.1007/s002210050660
Kasai, T., Kawai, S., Kawanishi, M. and Yahagi, S. (1997) Evidence for Facilitation of Motor Evoked Potentials (MEPs) Induced by Motor Imagery. Brain Research, 744, 147-150. https://doi.org/10.1016/S0006-8993(96)01101-8
Sakamoto, M., Muraoka, T., Mizuguchi, N. and Kanosue, K. (2009) Combining Observation and Imagery of an Action Enhances Human Corticospinal Excitability. Neuroscience Research, 65, 23-27. https://doi.org/10.1016/j.neures.2009.05.003
Strigaro, G., Ruge, D., Chen, J.C., Marshall, L., Desikan, M., Cantello, R. and Rothwell, J.C. (2015) Interaction between Visual and Motor Cortex: A Transcranial Magnetic Stimulation Study. Journal of Physiology, 593, 2365-2377. https://doi.org/10.1113/JP270135
Rosenkranz, K. and Rothwell, J.C. (2003) Differential Effect of Muscle Vibration on Intracortical Inhibitory Circuits in Humans. Journal of Physiology, 551, 649-660. https://doi.org/10.1113/jphysiol.2003.043752
Rosenkranz, K., Pesenti, A., Paulus, W. and Tergau, F. (2003) Focal Reduction of Intracortical Inhibition in the Motor Cortex by Selective Proprioceptive Stimulation. Experimental Brain Research, 149, 9-16. https://doi.org/10.1007/s00221-002-1330-3
Lapole, T., Temesi, J., Arnal, P.J., Gimenez, P., Petitjean, M. and Millet, G.Y. (2015) Modulation of Soleus Corticospinal Excitability during Achilles Tendon Vibration. Experimental Brain Research, 233, 2655-2662. https://doi.org/10.1007/s00221-015-4336-3
Kito, T., Hashimoto, T., Yoneda, T., Katamoto, S. and Naito, E. (2006) Sensory Processing during Kinesthetic Aftereffect Following Illusory Hand Movement Elicited by Tendon Vibration. Brain Research, 1114, 75-84. https://doi.org/10.1016/j.brainres.2006.07.062
Kim, Y.H., You, S.H., Ko, M.H., Park, J.W., Lee, K.H., Jang, S.H., Yoo, W.K. and Hallett, M. (2006) Repetitive Transcranial Magnetic Stimulation-Induced Corticomotor Excitability and Associated Motor Skill Acquisition in Chronic Stroke. Stroke, 37, 1471-1476. https://doi.org/10.1161/01.STR.0000221233.55497.51