Modulation of torque evoked by wide-pulse, high-frequency neuromuscular electrical stimulation and the potential implications for rehabilitation and training

Chris Donnelly, Jonathan Stegmüller, Anthony J Blazevich, Fabienne Crettaz von Roten, Bengt Kayser, Daria Neyroud, Nicolas Place, Chris Donnelly, Jonathan Stegmüller, Anthony J Blazevich, Fabienne Crettaz von Roten, Bengt Kayser, Daria Neyroud, Nicolas Place

Abstract

The effectiveness of neuromuscular electrical stimulation (NMES) for rehabilitation is proportional to the evoked torque. The progressive increase in torque (extra torque) that may develop in response to low intensity wide-pulse high-frequency (WPHF) NMES holds great promise for rehabilitation as it overcomes the main limitation of NMES, namely discomfort. WPHF NMES extra torque is thought to result from reflexively recruited motor units at the spinal level. However, whether WPHF NMES evoked force can be modulated is unknown. Therefore, we examined the effect of two interventions known to change the state of spinal circuitry in opposite ways on evoked torque and motor unit recruitment by WPHF NMES. The interventions were high-frequency transcutaneous electrical nerve stimulation (TENS) and anodal transcutaneous spinal direct current stimulation (tsDCS). We show that TENS performed before a bout of WPHF NMES results in lower evoked torque (median change in torque time-integral: - 56%) indicating that WPHF NMES-evoked torque might be modulated. In contrast, the anodal tsDCS protocol used had no effect on any measured parameter. Our results demonstrate that WPHF NMES extra torque can be modulated and although the TENS intervention blunted extra torque production, the finding that central contribution to WPHF NMES-evoked torques can be modulated opens new avenues for designing interventions to enhance WPHF NMES.

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Schematic diagram of experimental design. IH-reflex = stimulation intensity used to elicit a maximal H-reflex. IMmax = 120% of stimulation intensity used to elicit a maximal M-wave. Stimulation intensity of wide-pulse, high-frequency neuromuscular electrical stimulation (WPHF NMES, stimulation frequency: 100 Hz, pulse duration: 1 ms) was set to produce an initial torque level of 5% maximal voluntary contraction torque. In the transcutaneous electrical nerve stimulation (TENS) experiment, the intervention was high-frequency TENS (TENS trial) or no stimulation (Control trial) delivered over the plantar flexors for 15 min and the bout of WPHF NMES consisted of 3 x 20-s contractions separated by 40-s recovery. In the transcutaneous spinal direct current stimulation (tsDCS) experiment, the intervention was anodal tsDCS (tsDCS trial) or a sham stimulation (Sham trial) delivered over the 11th thoracic vertebrae for 20 min. The bout of WPHF NMES consisted of one contraction.
Figure 2
Figure 2
Original WPHF NMES-evoked torque and EMG traces for one participant presented before (WPHF NMES-Pre) and after (WPHF NMES-Post) (A) a 15-min period of TENS (TENS trial) or no stimulation (Control trial) and (B) a 20-min period of tsDCS (tsDCS trial) or sham stimulation (Sham trial). Each window lasts 1500 ms and includes the final 26 stimulation artefacts of each 20-s WPHF NMES. The insert shows the complete WPHF NMES (20-s stimulation) force trace. In the TENS experiment (A) compared to the control condition, WPHF NMES-evoked torque and sustained EMG activity were reduced following a 15-min period of TENS. In the tsDCS experiment (B) there was no increase in WPHF NMES-evoked torque or sustained EMG activity following a 20-min period of tsDCS or sham stimulation.
Figure 3
Figure 3
(A) Torque-time integral (TTI) presented before (WPHF NMES-Pre) and after (WPHF NMES-Post) a 15-min period of TENS (TENS trial) or no stimulation (Control trial). (B) Change in the TTI after a 15-min period of TENS (TENS trial) or no stimulation (Control trial). (C) TTI presented before (WPHF NMES-Pre) and after (WPHF NMES-Post) a 20-min period of tsDCS (tsDCS trial) or sham stimulation (Sham trial). (D) Change in the TTI after a 20-min period of tsDCS (tsDCS trial) or sham stimulation (Sham trial). Data are presented as individual data points and the line represents the median. *Significant difference between trials (P = 0.001). In TENS experiment (A,B) a significant reduction in the torque-time integral was observed when wide-pulse, high-frequency NMES stimulations were imposed after a bout of TENS compared to the control condition. In tsDCS (C,D) no significant change in the torque-time integral was observed when a wide-pulse, high-frequency NMES stimulation was imposed after a bout of tsDCS compared to the sham condition.
Figure 4
Figure 4
(A) Initial and final torque during WPHF NMES presented for the mean of all WPHF NMES-Pre contractions in the TENS experiment. (B) Extra torque presented before (WPHF NMES-Pre) and after (WPHF NMES-Post) a 15-min period of TENS (TENS trial) or no stimulation (Control trial). (C) Change in extra torque after a 15-min period of TENS (TENS trial) or no stimulation (Control trial). (D) Initial and final torque during WPHF NMES presented for the mean of all WPHF NMES-Pre contractions in the tsDCS experiment. (E) Extra torque presented before (WPHF NMES-Pre) and after (WPHF NMES-Post) a 20-min period of tsDCS (tsDCS trial) or sham stimulation (Sham trial). (F) Change in extra torque after a 20-min period of tsDCS (tsDCS trial) or sham stimulation (Sham trial). Data are presented as individual data points and the line represents the median. *Significant difference between trials (A: P = 0.037, C: P = 0.013). In TENS experiment (A–C) a significant reduction in extra torque was observed when wide-pulse, high-frequency NMES stimulations were imposed after a bout of TENS compared to the control condition. In the tsDCS experiment (D–F) no significant change in extra torque was observed when a wide-pulse, high-frequency NMES stimulation was imposed after a bout of tsDCS compared to the sham condition.
Figure 5
Figure 5
(A) Sustained EMG amplitude recorded before (WPHF NMES-Pre) and after (WPHF NMES-Post) a 15-min period of TENS (TENS trial) or no stimulation (Control trial). (B) Change in sustained EMG amplitude after a 15-min period of TENS (TENS trial) or no stimulation (Control trial). (C) Sustained EMG amplitude recorded before (WPHF NMES-Pre) and after (WPHF NMES-Post) a 20-min period of tsDCS (tsDCS trial) or sham stimulation (Sham trial). (D) Change in sustained EMG amplitude recorded after a 20-min period of tsDCS (tsDCS trial) or sham stimulation (Sham trial). Data are presented as individual data points and the line represents the median. *Significant difference between trials (P = 0.005). A significant reduction in EMG activity was observed in the period immediately after the cessation of wide-pulse, high-frequency NMES stimulations when imposed after a bout of TENS compared to the control condition (A,B). In the tsDCS experiment (C,D) no significant change in EMG activity was observed in the period immediately after the cessation a wide-pulse, high-frequency NMES stimulation was imposed after a bout of tsDCS compared to the sham condition.
Figure 6
Figure 6
Relationship between changes in the torque-time integral (TTI) and (A) extra torque and (B) sustained EMG amplitude following a 15-min period of TENS. Extreme value (included in analysis) is represented by an unfilled circle. Removing this participant from the analysis did not affect the conclusion. Significant, negative (Spearman’s) correlations were observed; no correlation was detected in the control condition.

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