Corticospinal excitability changes during muscle relaxation and contraction in motor imagery.
corticospinal excitability
motor evoked potential
motor imagery
muscle relaxation
transcranial magnetic stimulation
Journal
The European journal of neuroscience
ISSN: 1460-9568
Titre abrégé: Eur J Neurosci
Pays: France
ID NLM: 8918110
Informations de publication
Date de publication:
Oct 2023
Oct 2023
Historique:
revised:
03
08
2023
received:
12
12
2022
accepted:
08
08
2023
pubmed:
29
8
2023
medline:
29
8
2023
entrez:
29
8
2023
Statut:
ppublish
Résumé
To enhance smooth muscle contraction and relaxation during rehabilitation and sports activities, a comprehensive understanding of the motor control mechanisms within the central nervous system is necessary. However, current knowledge on these aspects is insufficient. Therefore, this study aimed to deepen our understanding of motor controls, by investigating the alterations in corticospinal excitability within cortical motor areas related to muscle contraction and relaxation using motor imagery with a reaction time task paradigm. Transcranial magnetic stimulation was used to measure the motor-evoked potentials in the first dorsal interosseous muscle of the right hand after the 'go' signal. Static weak muscle contraction (Experiment 1: 18 healthy participants) and resting state (Experiment 2: 16 healthy participants) were applied as background factors, and a trial without motor imagery was performed as a control. Muscle contraction was maintained in the background in the contraction motor imagery. A decrease in excitability in the relaxation motor imagery task occurred compared with the control. When the muscles were at rest, an increase in excitability in the contraction motor imagery and a transient increase in excitability in the relaxation motor imagery occurred compared with the control condition. Hence, the excitability of contraction and relaxation motor imagery is characterized by a continuous increase in excitability, transient increase and subsequent decrease in excitability, respectively. These results suggest that muscle contraction sensory information in the background condition may be necessary for muscle relaxation. Matching the background conditions may be crucial when utilizing motor imagery for rehabilitation or sports training.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3810-3826Subventions
Organisme : JSPS KAKENHI
ID : 20K11287
Informations de copyright
© 2023 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.
Références
Begum, T., Mima, T., Oga, T., Hara, H., Satow, T., Ikeda, A., Nagamine, T., Fukuyama, H., & Shibasaki, H. (2005). Cortical mechanisms of unilateral voluntary motor inhibition in humans. Neuroscience Research, 53(4), 428-435. https://doi.org/10.1016/j.neures.2005.09.002
Bouguetoch, A., Grosprêtre, S., & Martin, A. (2020). Optimal stimulation parameters for spinal and corticospinal excitabilities during contraction, motor imagery and rest: A pilot study. PLoS ONE, 15(6), e0235074. https://doi.org/10.1371/journal.pone.0235074
Buccolieri, A., Abbruzzese, G., & Rothwell, J. C. (2004). Relaxation from a voluntary contraction is preceded by increased excitability of motor cortical inhibitory circuits. Journal of Physiology, 558(2), 685-695. https://doi.org/10.1113/jphysiol.2004.064774
Case, L. K., Pineda, J., & Ramachandran, V. S. (2015). Common coding and dynamic interactions between observed, imagined, and experienced motor and somatosensory activity. Neuropsychologia, 79(Pt B), 233-245. https://doi.org/10.1016/j.neuropsychologia.2015.04.005
Chen, R., & Hallett, M. (1999). The time course of changes in motor cortex excitability associated with voluntary movement. Canadian Journal of Neurological Sciences. le Journal Canadien des Sciences Neurologiques, 26(3), 163-169. https://doi.org/10.1017/s0317167100000196
Cramer, A. O. J., van Ravenzwaaij, D., Matzke, D., Steingroever, H., Wetzels, R., Grasman, R. P. P. P., Waldorp, L. J., & Wagenmakers, E. J. (2016). Hidden multiplicity in exploratory multiway ANOVA: Prevalence and remedies. Psychonomic Bulletin and Review, 23(2), 640-647. https://doi.org/10.3758/s13423-015-0913-5
Decety, J. (1996). The neurophysiological basis of motor imagery. Behavioural Brain Research, 77(1-2), 45-52. https://doi.org/10.1016/0166-4328(95)00225-1
Eaves, D. L., Riach, M., Holmes, P. S., & Wright, D. J. (2016). Motor imagery during action observation: A brief review of evidence, theory and future research opportunities. Frontiers in Neuroscience, 10, 514. https://doi.org/10.3389/fnins.2016.00514
Fadiga, L., Buccino, G., Craighero, L., Fogassi, L., Gallese, V., & Pavesi, G. (1999). Corticospinal excitability is specifically modulated by motor imagery: A magnetic stimulation study. Neuropsychologia, 37(2), 147-158. https://doi.org/10.1016/s0028-3932(98)00089-x
Hall, C. R. (1997). Measuring movement imagery abilities: A revision of the movement imagery questionnaire. Journal of Mental Imagery, 21(1-2), 143-154.
Hanakawa, T., Dimyan, M. A., & Hallett, M. (2008). Motor planning, imagery, and execution in the distributed motor network: A time-course study with functional MRI. Cerebral Cortex, 18(12), 2775-2788. https://doi.org/10.1093/cercor/bhn036
Hashimoto, R., & Rothwell, J. C. (1999). Dynamic changes in corticospinal excitability during motor imagery. Experimental Brain Research, 125(1), 75-81. https://doi.org/10.1007/s002210050660
Jeannerod, M., & Decety, J. (1995). Mental motor imagery: A window into the representational stages of action. Current Opinion in Neurobiology, 5(6), 727-732. https://doi.org/10.1016/0959-4388(95)80099-9
Kasai, T., & Yahagi, S. (1999). Motor evoked potentials of the first dorsal interosseous muscle in step and ramp index finger abduction. Muscle and Nerve, 22(10), 1419-1425. https://doi.org/10.1002/(sici)1097-4598(199910)22:10<1419::aid-mus12>3.0.co;2-k
Kato, K., Vogt, T., & Kanosue, K. (2019). Brain activity underlying muscle relaxation. Frontiers in Physiology, 10, 1457. https://doi.org/10.3389/fphys.2019.01457
Kato, K., Watanabe, J., Muraoka, T., & Kanosue, K. (2015). Motor imagery of voluntary muscle relaxation induces temporal reduction of corticospinal excitability. Neuroscience Research, 92, 39-45. https://doi.org/10.1016/j.neures.2014.10.013
Kilteni, K., Andersson, B. J., Houborg, C., & Ehrsson, H. H. (2018). Motor imagery involves predicting the sensory consequences of the imagined movement. Nature Communications, 9(1), 1617. https://doi.org/10.1038/s41467-018-03989-0
Kumru, H., Soto, O., Casanova, J., & Valls-Sole, J. (2008). Motor cortex excitability changes during imagery of simple reaction time. Experimental Brain Research, 189(3), 373-378. https://doi.org/10.1007/s00221-008-1433-6
Lebon, F., Ruffino, C., Greenhouse, I., Labruna, L., Ivry, R. B., & Papaxanthis, C. (2019). The neural specificity of movement preparation during actual and imagined movements. Cerebral Cortex, 29(2), 689-700. https://doi.org/10.1093/cercor/bhx350
Motawar, B., Hur, P., Stinear, J., & Seo, N. J. (2012). Contribution of intracortical inhibition in voluntary muscle relaxation. Experimental Brain Research, 221(3), 299-308. https://doi.org/10.1007/s00221-012-3173-x
Mouthon, A., Ruffieux, J., Wälchli, M., Keller, M., & Taube, W. (2015). Task-dependent changes of corticospinal excitability during observation and motor imagery of balance tasks. Neuroscience, 303, 535-543. https://doi.org/10.1016/j.neuroscience.2015.07.031
Naito, E., Kochiyama, T., Kitada, R., Nakamura, S., Matsumura, M., Yonekura, Y., & Sadato, N. (2002). Internally simulated movement sensations during motor imagery activate cortical motor areas and the cerebellum. Journal of Neuroscience, 22(9), 3683-3691. https://doi.org/10.1523/JNEUROSCI.22-09-03683.2002
Nikolova, M., Pondev, N., Christova, L., Wolf, W., & Kossev, A. R. (2006). Motor cortex excitability changes preceding voluntary muscle activity in simple reaction time task. European Journal of Applied Physiology, 98(2), 212-219. https://doi.org/10.1007/s00421-006-0265-y
Ridding, M. C., & Ziemann, U. (2010). Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. Journal of Physiology, 588(13), 2291-2304. https://doi.org/10.1113/jphysiol.2010.190314
Rossini, P. M., Barker, A. T., Berardelli, A., Caramia, M. D., Caruso, G., Cracco, R. Q., Dimitrijević, M. R., Hallett, M., Katayama, Y., & Lücking, C. H. (1994). Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: Basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalography and Clinical Neurophysiology, 91(2), 79-92. https://doi.org/10.1016/0013-4694(94)90029-9
Rousselet, G. A., Foxe, J. J., & Bolam, J. P. (2016). A few simple steps to improve the description of group results in neuroscience. European Journal of Neuroscience, 44(9), 2647-2651. https://doi.org/10.1111/ejn.13400
Ruffino, C., Papaxanthis, C., & Lebon, F. (2017). Neural plasticity during motor learning with motor imagery practice: Review and perspectives. Neuroscience, 341, 61-78. https://doi.org/10.1016/j.neuroscience.2016.11.023
Stinear, C. M., & Byblow, W. D. (2003). Motor imagery of phasic thumb abduction temporally and spatially modulates corticospinal excitability. Clinical Neurophysiology, 114(5), 909-914. https://doi.org/10.1016/s1388-2457(02)00373-5
Stinear, C. M., Byblow, W. D., Steyvers, M., Levin, O., & 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
Sun, Y., Wei, W., Luo, Z., Gan, H., & Hu, X. (2016). Improving motor imagery practice with synchronous action observation in stroke patients. Topics in Stroke Rehabilitation, 23(4), 245-253. https://doi.org/10.1080/10749357.2016.1141472
Suzuki, T., Sugawara, K., Ogahara, K., & Higashi, T. (2016). Time course of corticospinal excitability and intracortical inhibition just before muscle relaxation. Frontiers in Human Neuroscience, 10, 1. https://doi.org/10.3389/fnhum.2016.00001
Suzuki, T., Sugawara, K., Takagi, M., & Higashi, T. (2015). Excitability changes in primary motor cortex just prior to voluntary muscle relaxation. Journal of Neurophysiology, 113(1), 110-115. https://doi.org/10.1152/jn.00489.2014
Takenaka, Y., Suzuki, T., & Sugawara, K. (2021). Time course effect of corticospinal excitability for motor imagery. European Journal of Neuroscience, 54(6), 6123-6134. https://doi.org/10.1111/ejn.15404
Tsukazaki, I., Uehara, K., Morishita, T., Ninomiya, M., & Funase, K. (2012). Effect of observation combined with motor imagery of a skilled hand-motor task on motor cortical excitability: Difference between novice and expert. Neuroscience Letters, 518(2), 96-100. https://doi.org/10.1016/j.neulet.2012.04.061
Uematsu, A., Obata, H., Endoh, T., Kitamura, T., Hortobágyi, T., Nakazawa, K., & Suzuki, S. (2010). Asymmetrical modulation of corticospinal excitability in the contracting and resting contralateral wrist flexors during unilateral shortening, lengthening and isometric contractions. Experimental Brain Research, 206(1), 59-69. https://doi.org/10.1007/s00221-010-2397-x
Werhahn, K. J., Fong, J. K., Meyer, B. U., Priori, A., Rothwell, J. C., Day, B. L., & Thompson, P. D. (1994). The effect of magnetic coil orientation on the latency of surface EMG and single motor unit responses in the first dorsal interosseous muscle. Electroencephalography and Clinical Neurophysiology, 93(2), 138-146. https://doi.org/10.1016/0168-5597(94)90077-9
Wilcox, R. R., & Rousselet, G. A. (2023). An updated guide to robust statistical methods in neuroscience. Current Protocols, 3(3), e719. https://doi.org/10.1002/cpz1.719
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. https://doi.org/10.1016/j.bbr.2011.09.014
Wright, D. J., McCormick, S. A., Birks, S., Loporto, M., & Holmes, P. S. (2015). Action observation and imagery training improve the ease with which athletes can generate imagery. Journal of Applied Sport Psychology, 27(2), 156-170. https://doi.org/10.1080/10413200.2014.968294
Wright, D. J., McCormick, S. A., Williams, J., & Holmes, P. S. (2016). Viewing instructions accompanying action observation modulate corticospinal excitability. Frontiers in Human Neuroscience, 10, 17. https://doi.org/10.3389/fnhum.2016.00017
Wright, D. J., Williams, J., & Holmes, P. S. (2014). Combined action observation and imagery facilitates corticospinal excitability. Frontiers in Human Neuroscience, 8, 951. https://doi.org/10.3389/fnhum.2014.00951
Yahagi, S., Ni, Z., Takahashi, M., Takeda, Y., Tsuji, T., & Kasai, T. (2003). Excitability changes of motor evoked potentials dependent on muscle properties and contraction modes. Motor Control, 7(4), 328-345. https://doi.org/10.1123/mcj.7.4.329
Yotani, K., Nakamoto, H., Ikudome, S., & Yuki, A. (2014). Muscle contraction and relaxation-response time in response to on or off status of visual stimulus. Journal of Physiological Anthropology, 33(1), 23. https://doi.org/10.1186/1880-6805-33-23
Zimmermann-Schlatter, A., Schuster, C., Puhan, M. A., Siekierka, E., & Steurer, J. (2008). Efficacy of motor imagery in post-stroke rehabilitation: A systematic review. Journal of Neuroengineering and Rehabilitation, 5, 8. https://doi.org/10.1186/1743-0003-5-8