Abstract
Purpose
The combination of motor imagery (MI) and neuromuscular electrical stimulation (NMES) can increase the corticospinal excitability suggesting that such association could be efficient in motor performance improvement. However, differential effect has been reported at spinal level after MI and NMES alone. The purpose of this study was to investigate the acute effect on motor performance and spinal excitability following MI, NMES and combining MI and NMES.
Methods
Ten participants were enrolled in three experimental sessions of MI, NMES and MI + NMES targeting plantar flexor muscles. Each session underwent 60 imagined, evoked (20% MVC) or imagined and evoked contractions simultaneously. Before, immediately after and 10 min after each session, maximal M-wave and H-reflex were evoked by electrical nerve stimulation applied at rest and during maximal voluntary contraction (MVC).
Results
The MVC decreased significantly between PRE-POST (− 12.14 ± 6.12%) and PRE-POST 10 (− 8.1 ± 6.35%) for NMES session, while this decrease was significant only between PRE-POST 10 (− 7.16 ± 11.25%) for the MI + NMES session. No significant modulation of the MVC was observed after MI session. The ratio Hmax/Mmax was reduced immediately after NMES session only.
Conclusion
The combination of MI to NMES seems to delay the onset of neuromuscular fatigue compared to NMES alone. This delay onset of neuromuscular fatigue was associated with specific modulation of the spinal excitability. These results suggested that MI could compensate the neuromuscular fatigue induced acutely by NMES until 10 min after the combination of both modalities.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation. All data are available upon request to the authors.
Abbreviations
- ANOVA:
-
Analysis of variance
- EMG:
-
Electromyography
- GM:
-
Gastrocnemius medialis
- HMAX :
-
Maximal H-reflex
- HSUP :
-
Superimposed H-reflex
- MATH :
-
M-wave recorded with the corresponding H-reflex
- MI:
-
Motor imagery
- MIQ-R:
-
Motor Imagery Questionnaire—Revised
- MMAX :
-
Maximal M-wave
- MSUP :
-
Superimposed M-wave
- MVC:
-
Maximal voluntary contraction
- NMES:
-
Neuromuscular electrical stimulation
- SOL:
-
Soleus muscle
- TA:
-
Tibialis anterior
- TTI:
-
Torque time integral
References
Belfiore P, Miele A, Gallè F, Liguori G (2018) Adapted physical activity and stroke: a systematic review. J Sports Med Phys Fit 58:1867–1875. https://doi.org/10.23736/S0022-4707.17.07749-0
Blouin JS, Walsh LD, Nickolls P, Gandevia SC (2009) High-frequency submaximal stimulation over muscle evokes centrally generated forces in human upper limb skeletal muscles. J Appl Physiol 106:370–377. https://doi.org/10.1152/japplphysiol.90939.2008
Bochkezanian V, Newton RU, Trajano GS, Blazevich AJ (2018) Effects of neuromuscular electrical stimulation in people with spinal cord injury. Med Sci Sports Exerc 50:1733–1739. https://doi.org/10.1249/MSS.0000000000001637
Boerio D, Jubeau M, Zory R, Maffiuletti NA (2005) Central and peripheral fatigue after electrostimulation-induced resistance exercise. Med Sci Sports Exerc 37:973–978. https://doi.org/10.1249/01.mss.0000166579.81052.9c
Bouguetoch A, Martin A, Grosprêtre S (2021) Insights into the combination of neuromuscular electrical stimulation and motor imagery in a training-based approach. Eur J Appl Physiol 121:941–955. https://doi.org/10.1007/s00421-020-04582-4
Bray SR, Graham JD, Martin Ginis KA, Hicks AL (2012) Cognitive task performance causes impaired maximum force production in human hand flexor muscles. Biol Psychol 89:195–200. https://doi.org/10.1016/j.biopsycho.2011.10.008
Carroll TJ, Selvanayagam VS, Riek S, Semmler JG (2011) Neural adaptations to strength training: moving beyond transcranial magnetic stimulation and reflex studies. Acta Physiol 202:119–140. https://doi.org/10.1111/j.1748-1716.2011.02271.x
Collins DF, Burke D, Gandevia SC (2001) Large involuntary forces consistent with plateau-like behavior of human motoneurons. J Neurosci 21:4059–4065. https://doi.org/10.1523/jneurosci.21-11-04059.2001
Daniele CA, MacDermott AB (2009) Low-threshold primary afferent drive onto GABAergic interneurons in the superficial dorsal horn of the mouse. J Neurosci 29:686–695. https://doi.org/10.1523/JNEUROSCI.5120-08.2009
Fernandez-Gomez E, Sanchez-Cabeza A (2018) Motor imagery: a systematic review of its effectiveness in the rehabilitation of the upper limb following a stroke. Rev Neurol 66:137–146
Grosprêtre S, Ruffino C, Lebon F (2016) Motor imagery and cortico-spinal excitability: a review. Eur J Sport Sci 16:317–324. https://doi.org/10.1080/17461391.2015.1024756
Grosprêtre S, Gueugneau N, Martin A, Lepers R (2017) Central contribution to electrically induced fatigue depends on stimulation frequency. Med Sci Sports Exerc 49:1530–1540. https://doi.org/10.1249/MSS.0000000000001270
Grosprêtre S, Gueugneau N, Martin A, Lepers R (2018) Presynaptic inhibition mechanisms may subserve the spinal excitability modulation induced by neuromuscular electrical stimulation. J Electromyogr Kinesiol 40:95–101. https://doi.org/10.1016/j.jelekin.2018.04.012
Grosprêtre S, Lebon F, Papaxanthis C, Martin A (2019) Spinal plasticity with motor imagery practice. J Physiol 597:921–934. https://doi.org/10.1113/JP276694
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.2018.08.003
Hultborn H, Jankowska E, Lindström S (1971) Recurrent inhibition of interneurones monosynaptically activated from group Ia afferents. J Physiol 215:613–636
Jeannerod M (1995) Mental imagery in the motor context. Neuropsychologia 33:1419–1432. https://doi.org/10.1016/0028-3932(95)00073-C
Jubeau M, Sartorio A, Marinone PG et al (2008) Comparison between voluntary and stimulated contractions of the quadriceps femoris for growth hormone response and muscle damage. J Appl Physiol 104:75–81. https://doi.org/10.1152/japplphysiol.00335.2007
Kaneko F, Hayami T, Aoyama T, Kizuka T (2014) Motor imagery and electrical stimulation reproduce corticospinal excitability at levels similar to voluntary muscle contraction. J Neuroeng Rehabil 11:1–7. https://doi.org/10.1186/1743-0003-11-94
Lagerquist O, Collins DF (2010) Influence of stimulus pulse width on M-waves, H-reflexes, and torque during tetanic low-intensity neuromuscular stimulation. Muscle Nerve 42:886–893. https://doi.org/10.1002/mus.21762
Lagerquist O, Walsh LD, Blouin JS et al (2009) Effect of a peripheral nerve block on torque produced by repetitive electrical stimulation. J Appl Physiol 107:161–167. https://doi.org/10.1152/japplphysiol.91635.2008
Lotze M, Montoya P, Erb M et al (1999) Activation of cortical and cerebellar motor areas during executed and imagined hand movements: an fMRI study. J Cogn Neurosci 11:491–501. https://doi.org/10.1162/089892999563553
Martin A, Grosprêtre S, Vilmen C et al (2016) The etiology of muscle fatigue differs between two electrical stimulation protocols. Med Sci Sports Exerc. https://doi.org/10.1249/MSS.0000000000000930
Misiaszek JE (2003) The H-reflex as a tool in neurophysiology: its limitations and uses in understanding nervous system function. Muscle Nerve 28:144–160. https://doi.org/10.1002/mus.10372
Mouthon A, Ruffieux J, Wälchli M et al (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
Muthalib M, Jubeau M, Millet GY et al (2010) Biceps brachii muscle oxygenation in electrical muscle stimulation. Clin Physiol Funct Imaging 30:360–368. https://doi.org/10.1111/j.1475-097X.2010.00953.x
Papaiordanidou M, Guiraud D, Varray A (2010a) Kinetics of neuromuscular changes during low-frequency electrical stimulation. Muscle Nerve 41:54–62. https://doi.org/10.1002/mus.21427
Papaiordanidou M, Guiraud D, Varray A (2010b) Does central fatigue exist under low-frequency stimulation of a low fatigue-resistant muscle? Eur J Appl Physiol 110:815–823. https://doi.org/10.1007/s00421-010-1565-9
Papaiordanidou M, Billot M, Varray A, Martin A (2014) Neuromuscular fatigue is not different between constant and variable frequency stimulation. PLoS One 9:1–8. https://doi.org/10.1371/journal.pone.0084740
Piscione J, Grosset JF, Gamet D, Pérot C (2012) Are H-reflex and M-wave recruitment curve parameters related to aerobic capacity? Appl Physiol Nutr Metab 37:990–996. https://doi.org/10.1139/H2012-078
Robin N, Coudevylle GR, Dominique L et al (2021) Translation and validation of the movement imagery questionnaire-3 second French version. J Bodyw Mov Ther 28:540–546. https://doi.org/10.1016/j.jbmt.2021.09.004
Rozand V, Lebon F, Papaxanthis C, Lepers R (2014) Does a mental training session induce neuromuscular fatigue? Med Sci Sports Exerc 46:1981–1989. https://doi.org/10.1249/MSS.0000000000000327
Saito K, Yamaguchi T, Yoshida N et al (2013) Combined effect of motor imagery and peripheral nerve electrical stimulation on the motor cortex. Exp Brain Res 227:333–342. https://doi.org/10.1007/s00221-013-3513-5
Seyri KM, Maffiuletti NA (2011) Effect of electromyostimulation training on muscle strength and sports performance. Strength Cond J 33:70–75
Stinear CM, Byblow WD, Steyvers M et al (2006) Kinesthetic, but not visual, motor imagery modulates corticomotor excitability. Exp Brain Res 168:157–164. https://doi.org/10.1007/s00221-005-0078-y
Takahashi Y, Kawakami M, Yamaguchi T et al (2019) Effects of leg motor imagery combined with electrical stimulation on plasticity of corticospinal excitability and spinal reciprocal inhibition. Front Neurosci 13:1–9. https://doi.org/10.3389/fnins.2019.00149
Theurel J, Lepers R, Pardon L, Maffiuletti NA (2007) Differences in cardiorespiratory and neuromuscular responses between voluntary and stimulated contractions of the quadriceps femoris muscle. Respir Physiol Neurobiol 157:341–347. https://doi.org/10.1016/j.resp.2006.12.002
Traverse E, Lebon F, Martin A (2018) Corticospinal and spinal excitabilities are modulated during motor imagery associated with somatosensory electrical nerve stimulation. Neural Plast. https://doi.org/10.1155/2018/8265427
Trimble MH, Enoka RM (1991) Mechanisms underlying the training effects associated with neuromuscular electrical stimulation. Phys Ther 71:273–280
Upton AR, McComas AJ, Sica RE (1971) Potentiation of “late” responses evoked in muscles during effort. J Neurol Neurosurg Psychiatry 34:699–711. https://doi.org/10.1136/jnnp.34.6.699
Wegrzyk J, Fouré A, Vilmen C et al (2015) Extra forces induced by wide-pulse, high-frequency electrical stimulation: occurrence, magnitude, variability and underlying mechanisms. Clin Neurophysiol 126:1400–1412. https://doi.org/10.1016/j.clinph.2014.10.001
Zehr EP (2002) Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 86:455–468. https://doi.org/10.1007/s00421-002-0577-5
Acknowledgements
We thank all the participants who took part in the experiments.
Funding
This work is funded by Agence nationale de la recherche (ANR) (ANR-20-CE37-0007).
Author information
Authors and Affiliations
Contributions
AM and SG: conceived and designed research; PE: conducted experiments and extracted results; PE: ran statistical analyses and designed graphs tables; PE, AM and SG: analyzed data; PE: wrote the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
There is no conflict of interest or competing interests.
Ethical approval
The experimental protocol was approved by the regional ethic committee (CPP COOM III number 2017-A00064-49; Clinical trial.gouv identifier NCT03334526) and conducted in conformity with the latest version of the Declaration of Helsinki.
Informed consent
Participants gave written informed consent to participate in the present study and to its publication.
Additional information
Communicated by Toshio Moritani.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Eon, P., Grosprêtre, S. & Martin, A. Can motor imagery balance the acute fatigue induced by neuromuscular electrical stimulation?. Eur J Appl Physiol 123, 1003–1014 (2023). https://doi.org/10.1007/s00421-022-05129-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-022-05129-5