Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-28T17:34:00.521Z Has data issue: false hasContentIssue false
  • English
  • Français

Primary Motor Cortex Excitability Is Modulated During the Mental Simulation of Hand Movement

Published online by Cambridge University Press:  16 February 2017

Christian Hyde ,
Ian Fuelscher ,
Jarrad A.G. Lum ,
Jacqueline Williams ,
Jason He  and
Peter G. Enticott
Christian Hyde*
Affiliation:
Cognitive Neuroscience Unit, School of Psychology, Deakin University, Geelong, Australia
Ian Fuelscher
Affiliation:
Cognitive Neuroscience Unit, School of Psychology, Deakin University, Geelong, Australia
Jarrad A.G. Lum
Affiliation:
Cognitive Neuroscience Unit, School of Psychology, Deakin University, Geelong, Australia
Jacqueline Williams
Affiliation:
Institute of Sport, Exercise and Active Living, Victoria University, Melbourne, Australia
Jason He
Affiliation:
Cognitive Neuroscience Unit, School of Psychology, Deakin University, Geelong, Australia
Peter G. Enticott
Affiliation:
Cognitive Neuroscience Unit, School of Psychology, Deakin University, Geelong, Australia
*
Correspondence and reprint requests to: Christian Hyde, Cognitive Neuroscience Unit, School of Psychology, Deakin University, Burwood Campus, 221 Burwood Hwy, Burwood, 3125, Victoria, Australia. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Objectives: It is unclear whether the primary motor cortex (PMC) is involved in the mental simulation of movement [i.e., motor imagery (MI)]. The present study aimed to clarify PMC involvement using a highly novel adaptation of the hand laterality task (HLT). Methods: Participants were administered single-pulse transcranial magnetic stimulation (TMS) to the hand area of the left PMC (hPMC) at either 50 ms, 400 ms, or 650 ms post stimulus presentation. Motor-evoked potentials (MEPs) were recorded from the right first dorsal interosseous via electromyography. To avoid the confound of gross motor response, participant response (indicating left or right hand) was recorded via eye tracking. Participants were 22 healthy adults (18 to 36 years), 16 whose behavioral profile on the HLT was consistent with the use of a MI strategy (MI users). Results: hPMC excitability increased significantly during HLT performance for MI users, evidenced by significantly larger right hand MEPs following single-pulse TMS 50 ms, 400 ms, and 650 ms post stimulus presentation relative to baseline. Subsequent analysis showed that hPMC excitability was greater for more complex simulated hand movements, where hand MEPs at 50 ms were larger for biomechanically awkward movements (i.e., hands requiring lateral rotation) compared to simpler movements (i.e., hands requiring medial rotation). Conclusions: These findings provide support for the modulation of PMC excitability during the HLT attributable to MI, and may indicate a role for the PMC during MI. (JINS, 2017, 23, 185–193)

Keywords

Motor imageryTMSMotor cognitionCorticospinal excitabilityHand laterality taskHand rotation task, MEP
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 23 , Special Issue 2: Special Issue: Motor Cognition , February 2017 , pp. 185 - 193
Copyright
Copyright © The International Neuropsychological Society 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alexander, G.E., & Crutcher, M.D. (1990). Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends in Neurosciences, 13(7), 266–271.Google Scholar
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society . Series B (Methodological), 289–300.Google Scholar
Blefari, M.L., Sulzer, J., Hepp-Reymond, M.-C., Kollias, S., & Gassert, R. (2015). Improvement in precision grip force control with self-modulation of primary motor cortex during motor imagery. Frontiers in behavioral neuroscience, 9.CrossRefGoogle ScholarPubMed
Bode, S., Koeneke, S., & Jäncke, L. (2007). Different strategies do not moderate primary motor cortex involvement in mental rotation: a TMS study. Behavioral and Brain Functions, 3(1), 1.Google Scholar
Butson, M.L., Hyde, C., Steenbergen, B., & Williams, J. (2014). Assessing motor imagery using the hand rotation task: Does performance change across childhood? Human movement science, 35, 50–65.Google Scholar
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.Google Scholar
Decety, J. (1996). Do imagined and executed actions share the same neural substrate? Cognitive brain research, 3(2), 87–93.Google Scholar
Di Rienzo, F., Collet, C., Hoyek, N., & Guillot, A. (2014). Impact of neurologic deficits on motor imagery: a systematic review of clinical evaluations. Neuropsychology review, 24(2), 116–147.Google Scholar
Eisenegger, C., Herwig, U., & Jäncke, L. (2007). The involvement of primary motor cortex in mental rotation revealed by transcranial magnetic stimulation. European Journal of Neuroscience, 25(4), 1240–1244.Google Scholar
Fadiga, L., Buccino, G., Craighero, L., Fogassi, L., Gallese, V., & Pavesi, G. (1998). Corticospinal excitability is specifically modulated by motor imagery: a magnetic stimulation study. Neuropsychologia, 37(2), 147–158.Google Scholar
Fiori, F., Sedda, A., Ferrè, E., Toraldo, A., Querzola, M., Pasotti, F., & Lunetta, C. (2013). Exploring motor and visual imagery in Amyotrophic Lateral Sclerosis. Experimental Brain Research, 226(4), 537–547.CrossRefGoogle ScholarPubMed
Fiori, F., Sedda, A., Ferre, E.R., Toraldo, A., Querzola, M., Pasotti, F., & Redaelli, T. (2014). Motor imagery in spinal cord injury patients: moving makes the difference. Journal of neuropsychology, 8(2), 199–215.Google Scholar
Fitzgibbon, B., Fitzgerald, P., & Enticott, P. (2014). An examination of the influence of visuomotor associations on interpersonal motor resonance. Neuropsychologia, 56, 439–446.Google Scholar
Frens, M., & Erkelens, C. (1991). Coordination of hand movements and saccades: evidence for a common and a separate pathway. Experimental Brain Research, 85(3), 682–690.Google Scholar
Fuelscher, I., Williams, J., Enticott, P.G., & Hyde, C. (2015). Reduced motor imagery efficiency is associated with online control difficulties in children with probable developmental coordination disorder. Research in developmental disabilities, 45, 239–252.Google Scholar
Fuelscher, I., Williams, J., Wilmut, K., Enticott, P., & Hyde, C. (2016). Modelling the Maturation of Grip Selection Planning and Action Representation: insights from typical and atypical motor development. Frontiers in Psychology, 7, 10.3389/fpsyg.2016.00108.CrossRefGoogle ScholarPubMed
Ganis, G., Keenan, J.P., Kosslyn, S.M., & Pascual-Leone, A. (2000). Transcranial magnetic stimulation of primary motor cortex affects mental rotation. Cerebral Cortex, 10(2), 175–180.Google Scholar
Guillot, A., Di Rienzo, F., MacIntyre, T., Moran, A.P., & Collet, C. (2012). Imagining is not doing but involves specific motor commands: a review of experimental data related to motor inhibition.Google Scholar
Gut, M., Urbanik, A., Forsberg, L., Binder, M., Rymarczyk, K., Sobiecka, B., & Grabowska, A. (2007). Brain correlates of right-handedness. Acta neurobiologiae experimentalis, 67(1), 43.Google Scholar
Hanakawa, T. (2015). Organizing motor imageries. Neuroscience research.Google Scholar
Hétu, S., Grégoire, M., Saimpont, A., Coll, M.-P., Eugène, F., Michon, P.-E., & Jackson, P.L. (2013). The neural network of motor imagery: an ALE meta-analysis. Neuroscience & Biobehavioral Reviews, 37(5), 930–949.Google Scholar
Hyde, C., Fuelscher, I., Buckthought, K., Enticott, P.G., Gitay, M.A., & Williams, J. (2014). Motor imagery is less efficient in adults with probable developmental coordination disorder: Evidence from the hand rotation task. Research in developmental disabilities, 35(11), 3062–3070.Google Scholar
Hyde, C., Wilmut, K., Fuelscher, I., & Williams, J. (2013). Does implicit motor imagery ability predict reaching correction efficiency? A test of recent models of human motor control. Journal of motor behavior, 45(3), 259–269.Google Scholar
Ionta, S., Perruchoud, D., Draganski, B., & Blanke, O. (2012). Body context and posture affect mental imagery of hands. PloS one, 7(3), e34382.Google Scholar
Jeannerod, M. (2006). Motor cognition: What actions tell the self. Oxford University Press.Google Scholar
Kosslyn, S.M., Digirolamo, G.J., Thompson, W.L., & Alpert, N.M. (1998). Mental rotation of objects versus hands: Neural mechanisms revealed by positron emission tomography. Psychophysiology, 35(02), 151–161.Google Scholar
Kosslyn, S.M., Ganis, G., & Thompson, W.L. (2001). Neural foundations of imagery. Nature Reviews Neuroscience, 2(9), 635–642.CrossRefGoogle ScholarPubMed
Lacourse, M.G., Orr, E.L., Cramer, S.C., & Cohen, M.J. (2005). Brain activation during execution and motor imagery of novel and skilled sequential hand movements. Neuroimage, 27(3), 505–519.Google Scholar
Lebon, F., Byblow, W.D., Collet, C., Guillot, A., & Stinear, C.M. (2012). The modulation of motor cortex excitability during motor imagery depends on imagery quality. European Journal of Neuroscience, 35(2), 323–331.Google Scholar
Malouin, F., & Richards, C.L. (2013). Clinical applications of motor imagery in rehabilitation Multisensory Imagery (pp. 397–419): Springer.Google Scholar
McCarron, L. (1997). McCarron assessment of neuromuscular development: fine and gross motor abilities (revised). Texas: McCarron-Dial Systems: Inc.Google Scholar
Meister, I.G., Boroojerdi, B., Foltys, H., Sparing, R., Huber, W., & Töpper, R. (2003). Motor cortex hand area and speech: implications for the development of language. Neuropsychologia, 41(4), 401–406.Google Scholar
Parsons, L.M. (1994). Temporal and kinematic properties of motor behavior reflected in mentally simulated action. Journal of Experimental Psychology: Human Perception and Performance, 20(4), 709.Google Scholar
Parsons, L.M., & Fox, P.T. (1998). The neural basis of implicit movements used in recognising hand shape. Cognitive Neuropsychology, 15, 583–616.Google Scholar
Pearce, A.J., & Kidgell, D.J. (2009). Corticomotor excitability during precision motor tasks. Journal of Science and Medicine in Sport, 12(2), 280–283.Google Scholar
Pelgrims, B., Michaux, N., Olivier, E., & Andres, M. (2011). Contribution of the primary motor cortex to motor imagery: a subthreshold TMS study. Human brain mapping, 32(9), 1471–1482.Google Scholar
Perrey, S. (2013). Promoting motor function by exercising the brain. Brain sciences, 3(1), 101–122.Google Scholar
Rathelot, J.-A., & Strick, P.L. (2009). Subdivisions of primary motor cortex based on cortico-motoneuronal cells. Proceedings of the National Academy of Sciences, 106(3), 918–923.Google Scholar
Sauner, D., Bestmann, S., Siebner, H.R., & Rothwell, J.C. (2006). No evidence for a substantial involvement of primary motor hand area in handedness judgements: a transcranial magnetic stimulation study. European Journal of Neuroscience, 23(8), 2215–2224.Google Scholar
Sharma, N., Pomeroy, V.M., & Baron, J.-C. (2006). Motor imagery a backdoor to the motor system after stroke? Stroke, 37(7), 1941–1952.CrossRefGoogle Scholar
Sparing, R., Meister, I., Wienemann, M., Buelte, D., Staedtgen, M., & Boroojerdi, B. (2007). Task‐dependent modulation of functional connectivity between hand motor cortices and neuronal networks underlying language and music: a transcranial magnetic stimulation study in humans. European Journal of Neuroscience, 25(1), 319–323.CrossRefGoogle Scholar
Spruijt, S., van der Kamp, J., & Steenbergen, B. (2015). Current insights in the development of children’s motor imagery ability. Frontiers in Psychology, 6.Google Scholar
Stinear, C.M. (2010). Corticospinal facilitation during motor imagery. The neurophysiological foundations of mental and motor imagery, 47–61.CrossRefGoogle Scholar
Stinear, C.M., Coxon, J.P., & Byblow, W.D. (2009). Primary motor cortex and movement prevention: where Stop meets Go. Neuroscience & Biobehavioral Reviews, 33(5), 662–673.Google Scholar
Ter Horst, A.C., van Lier, R., & Steenbergen, B. (2010). Mental rotation task of hands: differential influence number of rotational axes. Experimental Brain Research, 203(2), 347–354.Google Scholar
Tokimura, H., Asakura, T., Tokimura, Y., Oliviero, A., & Rothwell, J. (1996). Speech‐induced changes in corticospinal excitability. Annals of neurology, 40(4), 628–634.Google Scholar
Tomasino, B., Borroni, P., Isaja, A., & Ida Rumiati, R. (2005). The role of the primary motor cortex in mental rotation: a TMS study. Cognitive Neuropsychology, 22(3-4), 348–363.Google Scholar
Townsend, J.T., & Ashby, F.G. (1978). Methods of modeling capacity in simple processing systems. Cognitive theory, 3, 200–239.Google Scholar
Townsend, J.T., & Ashby, F.G. (1983). Stochastic modeling of elementary psychological processes. CUP Archive.Google Scholar
Williams, J., Pearce, A.J., Loporto, M., Morris, T., & Holmes, P.S. (2012). The relationship between corticospinal excitability during motor imagery and motor imagery ability. Behavioural brain research, 226(2), 369–375.Google Scholar
Williams, J., Thomas, P., Maruff, P., Butson, M., & Wilson, P. (2006). Motor, visual and egocentric transformations in children with developmental coordination disorder. Child: care, health and development, 32(6), 633–647.Google Scholar
Zapparoli, L., Invernizzi, P., Gandola, M., Berlingeri, M., De Santis, A., Zerbi, A., & Paulesu, E. (2014). Like the back of the (right) hand? A new fMRI look on the hand laterality task. Experimental Brain Research, 232(12), 3873–3895.Google Scholar