Direct and crossed effects of somatosensory electrical stimulation on motor learning and neuronal plasticity in humans

M P Veldman, I Zijdewind, S Solnik, N A Maffiuletti, K M M Berghuis, M Javet, J Négyesi, T Hortobágyi, M P Veldman, I Zijdewind, S Solnik, N A Maffiuletti, K M M Berghuis, M Javet, J Négyesi, T Hortobágyi

Abstract

Purpose: Sensory input can modify voluntary motor function. We examined whether somatosensory electrical stimulation (SES) added to motor practice (MP) could augment motor learning, interlimb transfer, and whether physiological changes in neuronal excitability underlie these changes.

Methods: Participants (18-30 years, n = 31) received MP, SES, MP + SES, or a control intervention. Visuomotor practice included 300 trials for 25 min with the right-dominant wrist and SES consisted of weak electrical stimulation of the radial and median nerves above the elbow. Single- and double-pulse transcranial magnetic stimulation (TMS) metrics were measured in the intervention and non-intervention extensor carpi radialis.

Results: There was 27 % motor learning and 9 % (both p < 0.001) interlimb transfer in all groups but SES added to MP did not augment learning and transfer. Corticospinal excitability increased after MP and SES when measured at rest but it increased after MP and decreased after SES when measured during contraction. No changes occurred in intracortical inhibition and facilitation. MP did not affect the TMS metrics in the transfer hand. In contrast, corticospinal excitability strongly increased after SES with MP + SES showing sharply opposite of these effects.

Conclusion: Motor practice and SES each can produce motor learning and interlimb transfer and are likely to be mediated by different mechanisms. The results provide insight into the physiological mechanisms underlying the effects of MP and SES on motor learning and cortical plasticity and show that these mechanisms are likely to be different for the trained and stimulated motor cortex and the non-trained and non-stimulated motor cortex.

Keywords: Corticospinal excitability; Interlimb transfer; Motor evoked potential; Primary motor cortex; Transcranial magnetic stimulation.

Figures

Fig. 1
Fig. 1
Schematic overview of the experimental design. Baseline measurements including maximal compound action potentials (Mmax), corticospinal excitability (CSE), short-interval intracortical inhibition (SICI), intracortical facilitation (ICF), contralateral facilitation (CLF), and ipsilateral silent period (iSP) were performed before familiarization of the visuomotor task and after completion of one of the three interventions and motor tests
Fig. 2
Fig. 2
Increases in motor performance after motor practice (MP), somatosensory electrical stimulation (SES), and MP + SES in the intervention (open bars) and non-intervention (filled bars). Motor performance was computed as a reduction in template-matching errors. Performance improved more after MP and MP + SES in the right hand compared to SES. Asterisk, significant Time main effect (p < 0.05, open and filled bars, respectively, pooled, not graphed); dagger, significant Group by Time interaction (p < 0.05). Vertical bars denote +1SD
Fig. 3
Fig. 3
Raw data of changes in corticospinal excitability after motor practice (MP) and somatosensory electrical stimulation (SES). Representative 10-trial-averaged motor evoked potentials (MEPs) measured in the extensor carpi radialis (ECR) representing changes in corticospinal excitability before (gray lines) and after (black lines) the three interventions in the intervention left M1 (a–c) and non-intervention right M1 (d–f)
Fig. 4
Fig. 4
Corticospinal excitability increases in all groups in the intervention M1 and after somatosensory electrical stimulation (SES) in the non-intervention M1. Corticospinal excitability before (open bars) and after (filled bars) the three interventions in the intervention left M1 (Panel A) and non-intervention right M1 (Panel B). Corticospinal excitability increased more after SES compared to MP and MP + SES in both M1s. Interconnected dots represent individual changes and vertical bars denote +1SD. Asterisk significant Time main effect (p < 0.05); dagger significant Group by Time interaction (p < 0.05)
Fig. 5
Fig. 5
Group and individual changes in short-interval intracortical inhibition (SICI) after motor practice (MP), somatosensory electrical stimulation (SES), and MP + SES in the non-intervention right M1. Conditioned motor evoked potentials (MEP) before (open bars) and after (filled bars) the three interventions. Lower values for SICI represent higher intracortical inhibition. Group data show that SICI increased after SES and decreased after MP + SES in the non-intervention M1 while MP did not modify SICI. Interconnected dots represent individual changes and vertical bars denote +1SD. Asterisk significant Time main effect (p < 0.05); dagger and section sign, significant Group by Time interaction (p < 0.05)
Fig. 6
Fig. 6
Group and individual changes in interhemispheric inhibition (IHI) and facilitation (CLF) after motor practice (MP) and somatosensory electrical stimulation (SES). IHI and CLF from the left M1 to the right M1 graphed before (open bars) and after (filled bars) the three interventions. IHI decreased after SES but increased after MP, resulting in a cancelation effect after MP + SES (Panel A). Opposite effects were found for CLF (Panel B). Interconnected dots represent individual changes and vertical bars denote +1SD. Asterisk significant Time main effect (p < 0.05); dagger and section sign significant Group by Time interaction (p < 0.05)

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