Accessible Requires Authentication Published by De Gruyter June 25, 2013

Corticospinal Excitability Following Short-Term Motor Imagery Training of a Strength Task

Michael C.M. Leung, Michael Spittle and Dawson J. Kidgell

Abstract

Motor imagery and actual movement engage similar neural structures, however, whether they produce similar training-related corticospinal adaptations has yet to be established. The aim of this study was to compare changes in strength and corticospinal excitability following short-term motor imagery strength training and short-term strength training. Transcranial magnetic stimulation (TMS) was applied over the contralateral motor cortex (M1) to elicit motor-evoked potentials in the dominant biceps brachii muscle prior to and following 3-week strength training using actual bicep curls or motor imagery of bicep curls. The strength training (n = 6) and motor imagery (n = 6) groups underwent three supervised training sessions per week for 3 weeks. Participants completed four sets of six to eight repetitions (actual or imagined) at a training load of 80% of their one-repetition maximum. The control group (n = 6) were required to maintain their current level of physical activity. Both training groups exhibited large performance gains in strength (p < 0.001; strength training 39% improvement, imagery 16% improvement), which were significantly different between groups (p = 0.027). TMS revealed that the performance improvements observed in both imagery and strength training were accompanied by increases in corticospinal excitability (p < 0.001), however, these differences were not significantly different between groups (p = 0.920). Our findings suggest that both strength training and motor imagery training utilised similar neural substrates within the primary M1, however, strength training resulted in greater gains in strength than motor imagery strength training. This difference in strength increases may be attributed to adaptations during strength training that are not confined to the primary M1. These findings have theoretical implications for functional equivalent views of motor imagery as well as important therapeutic implications.

References

Aagard, P., Simonsen, E., Andersen, J., Magnusson, P., & Dyhre-Poulsen, P. (2002). Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. Journal of Applied Physiology, 92, 2309–2318. Search in Google Scholar

Aoyama, T., & Kaneko, F. (2011). The effect of motor imagery on gain modulation of the spinal reflex. Brain Research, 1372, 41–48. Search in Google Scholar

Beck, S., Taube, W., Gruber, M., Amtage, F., Gollhofer, A., & Schubert, M. (2007). Task-specific changes in motor evoked potentials of lower limb muscles after different training interventions. Brain Research, 1179(51–60). Search in Google Scholar

Bonnet, M., Decety, J., Requin, J., & Jeannerod, M. (1997). Mental simulation of an action modulates the excitability of spinal reflex pathways in man. Cognitive Brain Research, 5, 221–228. Search in Google Scholar

Decety, J., Perani, D., Jeannerod, M., Bettinardi, V., Tadary, B., Woods, R.,... Fazio, F. (1994). Mapping motor representations with positron emission tomography. Nature, 371, 600–602. Search in Google Scholar

Deiber, M., Ibanez, V., Honda, M., Sadato, N., Raman, R., & Hallett, M. (1998). Cerebral processes related to visuomotor imagery and generation of simple finger movements studied with positron emission tomography. NeuroImage, 2, 73–85. Search in Google Scholar

Del Balso, C., & Cafarelli, E. (2007). Adaptations in the activation of human skeletal muscle induced by short-term isometric resistance training. Journal of Applied Physiology, 103, 402–411. Search in Google Scholar

Duchateau, J., & Enoka, R. (2002). Neural adaptations with chronic activity patterns in able-bodied humans. American Journal of Physical Medical & Rehabilitation. Search in Google Scholar

Facchini, S., Muellbacher, W., Battaglia, F., Boroojerdi, B., & Hallett, M. (2002). Focal enhancement of motor cortex excitability during motor imagery: a transcranial magnetic stimulation study. Acta Neurologica Scandinavica, 105, 146–151. Search in Google Scholar

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, 147–158. Search in Google Scholar

Feltz, D., & Landers, D. (1983). The effect of mental practice on motor skill learning and performance: A meta-analysis. Journal of Sport Pyschology, 2, 211–220. Search in Google Scholar

Fery, Y. (2003). Differentiating visual and kinesthetic imagery in mental practice. Canadian Journal of Experimental Psychology, 57, 1–10. Search in Google Scholar

Fimland, M., Helgerrud, J., Gruber, M., Leivseth, G., & Hoff, J. (2009). Functional maximal strength training induces neural transfer to single-joint tasks. European Journal of Applied Physiology, 107, 21–29. Search in Google Scholar

Folland, J., & Williams, A. (2007). The adaptations to strength training, morphological and neurological contributions to increased strength training. Sports Medicine, 37(2), 145–168. Search in Google Scholar

Frith, C., & Dolan, R. (1997). Brain mechanisms associated with top-down processes in perception. Philosophical Transcations of the Royal Society B: Biological Sciences, 352, 1221–1230. Search in Google Scholar

Gandevia, S., Wilson, L., Inglis, T., & Burke, D. (1997). Mental rehearsal of motor tasks recruits α – motoneurones but fails to recruit human fusimotor neurones selectively. Journal of Physiology, 505, 259–266. Search in Google Scholar

Goodwill, A., Pearce, A. J., & Kidgell, D. J. (2012). Corticomotor plasticity following unilateral strength training. Muscle and Nerve. Search in Google Scholar

Griffin, L., & Cafarelli, E. (2007). Transcranial magnetic stimulation during resistance training of the tibialis anterior msucle. Journal of Electromyography and Kinesiology, 17, 446–452. Search in Google Scholar

Hashimoto, R., & Rothwell, J. C. (1999). Dynamic changes in corticospinal excitability during motor imagery. Experimental Brain Research, 125(1), 75–81. Search in Google Scholar

He, S., Dum, R., & Strick, P. (1996). Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere. Journal of Neuroscience, 15, 3284–3306. Search in Google Scholar

Hinder, M., Schmidt, M., Garry, M. I., Carroll, T., & Summers, J. J. (2011). Absence of cross-limb transfer of performance gains following ballistic motor practice in older adults. Journal of Applied Physiology, 110, 166–174. Search in Google Scholar

Jeannerod, M. (1994). The representing brain: Neural correlates of motor intention and imagery. Behavioural and Brain Sciences, 17, 187–245. Search in Google Scholar

Jeannerod, M. (1995). Mental imagery in the motor context. Neuropsychologia, 33, 1419–1432. Search in Google Scholar

Jeannerod, M. (2001). Neural simulation of action: a unifying mechanism for motor cognition. NeuroImage, 14, 103–109. Search in Google Scholar

Jensen, J., Marstrand, P., & Nielsen, J. (2005). Motor skill training and strength training are associated with different plastic changes in the central nervous system. Journal of Applied Physiology, 99, 1558–1568. Search in Google Scholar

Kamen, G., & Knight, C. (2004). Training-related adaptations in motor unit discharge rate in young and older adults. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 59, 1334–1338. Search in Google Scholar

Kasai, T., Kawai, S., Kawanishi, M., & Yahagi, S. (1997). Evidence for facilitation of motor evoked potentials (MEPs) induced by motor imagery. Brain Research, 744, 147–150. Search in Google Scholar

Kidgell, D. J., & Pearce, A. J. (2010). Corticospinal properties following short-term strength training of an intrinsic hand muscle. Human Movement Science, 29, 631–641. Search in Google Scholar

Kidgell, D. J., Stokes, M., Castricum, T., & Pearce, A. J. (2010). Neurophysiological responses after short-term strength training of the biceps brachii muscle. Journal of Strength and Conditioning Research, 0, 1–10. Search in Google Scholar

Kidgell, D. J., Stokes, M., & Pearce, A. J. (2011). Strength training of one limb increases corticomotor excitability projecting to the contralateral homologous limb. Motor Control, 15,247–266. Search in Google Scholar

Kiers, L., Fernando, B., & Tomkins, D. (1997). Facilitory effect of thinking about movement on magnetic motor-evoked potentials. Electroencephalography and clinical neurophysiology, 744(1), 147–150. Search in Google Scholar

Lackner, E., & Hummelsheim, H. (2003). Motor-evoked potentials are facilitated during perceptual identification of hand position in healthy subjects and stroke patients. Clinical Rehabilitation, 17, 648–655. Search in Google Scholar

Lee, M., Gandevia, S., & Carroll, T. (2009). Short-term strength training does not change cortical voluntary activation. Medicine and Science in Sports and Exercise, 41, 1452–1460. Search in Google Scholar

Li, S., Latash, M., & Zatsiosky, V. (2004). Effects of motor imagery on finger force responses to transcranial magnetic stimulation. Cognitive Brain Research, 20, 273–280. Search in Google Scholar

Lotze, M., Montoya, P., Erb, M., Hulsmann, E., Flor, H., & Klose, U. (1999). Activation of cortical and cerebellar motor areas during executed and imagined hand movements: An fMRI study. Journal of Cognitive Neuroscience, 11(5), 491–501. Search in Google Scholar

Morris, T., Spittle, M., & Watt, A. (2005). Imagery in sport. Champaign, Illinois. Search in Google Scholar

Mulder, T., de Vries, S., & Zijlstra, S. (2005). Observation, imagination and execution of an effortful movement: more evidence for a central explanation of motor imagery. Experimental Brain Research, 163, 344–351. Search in Google Scholar

Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9(1), 97–113. Search in Google Scholar

Parsons, L., Fox, P., Downs, J., Glass, T., Hirsch, T., Martin, C.,... Lancaster, J. (1995). Use of implicit motor imagery for visual shape discrimination as revealed by PET. Nature, 375, 54–58. Search in Google Scholar

Peterson, M., Rhea, M., & Alvar, B. (2005). Applications of the dose-response for muscular strength development: A review of meta-analytic efficacy and reliability for designing training prescription. Journal of Strength and Conditioning Research, 19, 950–958. Search in Google Scholar

Pfurtscheller, G., & Neuper, C. (1997). Motor imgaery activates primary sensorimotor area in humans. Neuroscience Letters, 239, 65–68. Search in Google Scholar

Porro, C., Cettolo, V., Francescato, M., & Baraldi, P. (2000). Ipsilateral involvement of primary motor cortex during motor imagery. European Journal of Neuroscience, 12, 3059–3063. Search in Google Scholar

Ranganathan, V., Siemionow, V., Liu, J., Sahgal, V., & Yue, G. (2004). From mental power to muscle power – gaining strength by using the mind. Neuropsychologia, 42, 944–956. Search in Google Scholar

Rossi, S., Pasqualetti, P., Tecchio, F., Pauri, F., & Rossini, P. M. (1998). Corticospinal excitability modulation during mental simulation of wrist movements in human subjects. Neuroscience Letters, 243, 147–151. Search in Google Scholar

Roth, M., Decety, J., Raybaudi, M., Massarelli, R., Delon-Martin, C., Segebarth, C.,... Jeannerod, M. (1996). Possible involvement of primary motor cortex in mentally simulated movement: a functional magnetic imaging study. Cognitive Neuroscience, 7, 1280–1284. Search in Google Scholar

Semmler, J., & Enoka, R. (2000). Neural contributions to changes in muscle strength (Vol. IX). Malden: Blackwell. Search in Google Scholar

Shima, N., Ishida, K., Katayama, K., Morotome, Y., Sato, Y., & Miyamura, M. (2002). Cross education of muscular strength during unilateral resistance training and detraining. European Journal of Applied Physiology, 86, 284–294. Search in Google Scholar

Stephan, K., Fink, G., Passingham, R., Silbersweig, D., Ceballos-Baumann, A., Frith, C., & Frackowiak, R. (1995). Functional anatomy of the mental representation of upper extremity movements in healthy subjects. Journal of Neurophysiology, 73, 373–386. Search in Google Scholar

Stinear, C. (Ed.). (2010). Corticospinal facilitation during motor imagery. Oxford, UK: Oxford University Press. Search in Google Scholar

Stinear, C., & Byblow, W. (2003a). Motor imagery of phasic thumb abduction temporally and spatially modulates corticospinal excitability. Clinical Neurophysiology, 114, 909–914. Search in Google Scholar

Stinear, C., & Byblow, W. (2003b). Role of intracortical inhibition in selective and muscle activation. Journal of Neurophysiology, 89, 2014–2020. Search in Google Scholar

Stinear, C., & Byblow, W. (2004). Modulation of corticospinal excitability and intracortical inhibition during motor imagery is task-dependent. Experimental Brain Research, 157, 351–358. Search in Google Scholar

Stinear, C., Byblow, W., Steyvers, M., Levin, O., & Swinnen, S. (2006). Kinesthetic, but not visual, motor imagery modulates corticospinal excitability. Experimental Brain Research, 157, 351–358. Search in Google Scholar

Van Cutsem, M., Duchateau, J., & Hainaut, K. (1998). Changes in single motor unit behaviour contribute to the increase in contraction speed after dynamic training in humans. Journal of Physiology, 513, 295–305. Search in Google Scholar

Voisin, J., Mercier, C., Jackson, P., Richards, C., & Malouin, F. (2011). Is somatosensory excitability more affected by the perspective or modality content of motor imagery. Neuroscience Letters, 493, 33–37. Search in Google Scholar

Voti, P., Conte, A., Suppa, A., Iezzi, E., Bologna, M., Anieelo, M.,... Berardelli, A. (2011). Correlation between cortical plasticity, motor learning and BDNF genotype in healthy subjects. Experimental Brain Research, 212, 91–99. Search in Google Scholar

Weier, A. T., & Kidgell, D. J. (2012). Strength training with superimposed whole body vibration does not preferentially modulate cortical plasticity. The Scientific World Journal, 2012, 1–9. Search in Google Scholar

Williams, J., Pearce, A. J., Loporto, M., Morris, T., & Holmes, P. (2011). The relationship between corticospinal excitability during motor imagery and motor imagery ability. Behavioural Brain Research. Search in Google Scholar

Yahagi, S., & Kasai, T. (1999). Motor evoked potentials induced by motor imgaery reveal a functional asymmetry of cortical motor control in left- and right-handed human subjects. Journal of Neurophysiology, 67, 1114–1123. Search in Google Scholar

Yahagi, S., Shimura, Y., & Kasai, T. (1996). An increase in cortical excitability with no change in spinal excitability during motor imagery. Perceptual Motor Skills, 83, 288–290. Search in Google Scholar

Yue, G., & Cole, K. (1992). Strength increases from the motor program: comparison of training with maximal voluntary and imagined muscle contractions. Journal of Neurophysiology, 67(5), 1114–1123. Search in Google Scholar

Zijdewind, I., Butler, J., Gandevia, S., & Taylor, J. (2006). The origin of activity in the biceps brachii muscle during voluntary contractions of the contralateral elbow flexor muscles. Experimental Brain Research, 175, 526–535. Search in Google Scholar

Published Online: 2013-06-25

©2013 by Walter de Gruyter Berlin / Boston