Short-term inhibition of spinal reflexes in multiple lower limb muscles after neuromuscular electrical stimulation of ankle plantar flexors

Abstract

Neuromuscular electrical stimulation (NMES) of lower limbs elicits muscle contractions through the activation of efferent fibers and concomitant recruitment of afferent fibers, which can modulate excitability of the central nervous system. However, neural mechanisms of NMES and how unilateral stimulation of the soleus affects spinal reflexes in multiple lower limb muscles bilaterally remains unknown. Twelve able-bodied participants were recruited, and spinal reflex excitability changes were tested after four interventions, each applied for 60 s, on the right plantar flexors: (1) motor-level NMES; (2) sensory-level NMES; (3) voluntary contraction; (4) rest. Spinal reflexes were elicited using single-pulse transcutaneous spinal cord stimulation applied on the lumbar level of the spinal cord to evoke bilateral responses in multiple lower limb muscles, while maximum motor response (Mmax) was tested in the soleus by stimulating the posterior tibial nerve. Spinal reflexes and Mmax before each intervention were compared to immediately after and every 5 min subsequently, for 15 min. Results showed that motor-level NMES inhibited spinal reflexes of the soleus and other studied muscles of the ipsilateral leg, but not the contralateral leg (except vastus medialis) for 15 min, while not affecting soleus muscle properties (Mmax). Voluntary contraction effect lasted less than 5 min, while sensory-level NMES and rest did not produce an effect. Short-term spinal reflex excitability was likely affected because antidromic impulses during motor-level NMES coincided in the spinal cord with afferent inputs to induce spinal neuroplasticity, whereas afferent input alone did not produce short-term effects. Such activation of muscles with NMES could reduce spasticity in individuals with neurological impairments.

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Abbreviations

ANOVA:

Analysis of variance

BF:

Biceps femoris

FES:

Functional electrical stimulation

H-reflex:

Hoffmann reflex

M max :

Maximum motor response

NMES:

Neuromuscular electrical stimulation

PPS:

Paired-pulse stimulus

TA:

Tibialis anterior

tSCS:

Transcutaneous spinal cord stimulation

tSCSamp :

Peak-to-peak amplitude of the spinal reflexes

VM:

Vastus medialis

Sol:

Soleus

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Acknowledgements

This project was funded by the Japan Society for the Promotion of Science Grants-in-Aid for Scientific Research (KAKENHI) (Grant numbers: 17F17733 and 26242056).

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Correspondence to Matija Milosevic.

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M.R.P. is a shareholder in company MyndTec Inc. The remaining authors have no conflicts of interest.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Milosevic, M., Masugi, Y., Obata, H. et al. Short-term inhibition of spinal reflexes in multiple lower limb muscles after neuromuscular electrical stimulation of ankle plantar flexors. Exp Brain Res 237, 467–476 (2019). https://doi.org/10.1007/s00221-018-5437-6

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Keywords

  • Neuromuscular electrical stimulation
  • Spinal reflex
  • Neuroplasticity
  • Soleus
  • Rehabilitation