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Changes in spinal but not cortical excitability following combined electrical stimulation of the tibial nerve and voluntary plantar-flexion

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Abstract

Unilateral training involving voluntary contractions, neuromuscular electrical stimulation (NMES), or a combination of the two can increase the excitability of neural circuits bilaterally within the CNS. Many rehabilitation programs are designed to promote such “neuroplasticity” to improve voluntary movement following CNS damage. While much is known about this type of activity-dependent plasticity for the muscles that dorsi-flex the ankle, similar information is not available for the plantar-flexors. Presently, we assessed the excitability of corticospinal (CS) and spinal circuits for both soleus (SOL) muscles before and after voluntary contractions of the right plantar-flexors (VOL; 5 s on–5 s off, 40 min), NMES of the right tibial nerve (tnNMES; 5 s on–5 s off, 40 min), or both together (V + tnNMES). CS excitability for the right (rSOL) and left SOL (lSOL) muscles was assessed by quantifying motor evoked potentials elicited by transcranial magnetic stimulation. Spinal excitability was assessed using measures from the ascending limb of the M-wave versus H-reflex recruitment curve. CS excitability did not change for rSOL (the activated muscle) or lSOL following any condition. In contrast, there was a marked increase in spinal excitability for rSOL, but only following V + tnNMES; the slope of the M-wave versus H-reflex recruitment curve increased approximately twofold (pre = 7.9; post = 16.2) and H-reflexes collected when the M-wave was ~5 % of the maximal M-wave (Mmax) increased by ~1.5× (pre = 19 % Mmax, post = 29 % Mmax). Spinal excitability for lSOL did not change following any condition. Thus, only voluntary contractions that were coupled with NMES increased CNS excitability, and this occurred only in the ipsilateral spinal circuitry. These results are in marked contrast to previous studies showing NMES-induced changes in CS excitability for every other muscle studied and suggest that the mechanisms that regulate activity-dependent neuroplasticity are different for SOL than other muscles. Further, while rehabilitation strategies involving voluntary training and/or NMES of the plantar-flexors may be beneficial for producing movement and reducing atrophy, a single session of low-intensity NMES and voluntary training may not be effective for strengthening CS pathways to the SOL muscle.

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Acknowledgments

This work was supported by a grant from the Natural Sciences and Engineering Research Council of Canada. The authors also thank Mr. Alejandro Ley for his technical support.

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Correspondence to David F. Collins.

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Lagerquist, O., Mang, C.S. & Collins, D.F. Changes in spinal but not cortical excitability following combined electrical stimulation of the tibial nerve and voluntary plantar-flexion. Exp Brain Res 222, 41–53 (2012). https://doi.org/10.1007/s00221-012-3194-5

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