Effects of pulse width and frequency on evoked responses in electrostimulation: comparison between three muscle groups
Authors: Popesco Timothée , Gardet Quentin , Bossard Jonathan , Maffiuletti Nicola A. , Place Nicolas 
Published: February 2024

Introduction
Neuromuscular electrical stimulation (NMES) is an innovative and effective (re)training strategy to improve or restore neuromuscular function (Maffiuletti et al., 2018). Contractions induced by NMES differ in many aspects from voluntary contractions, as motor unit (MU) recruitment is random, synchronous and spatially fixed (mostly superficial; Maffiuletti, 2010). Consequently, several limitations, such as higher fatigability (Vanderthommen et al., 1999) and discomfort (Delitto et al., 1992) might restrain its clinical implementation. The use of specific stimulation parameters may partly overcome these limitations. Indeed, the use of wide pulses (≥ 1 ms) delivered at low stimulation intensity leads to a preferential recruitment of Ia sensory axons (Veale et al., 1973) which may promote MU central (reflexive) recruitment. Furthermore, the high stimulation frequencies (> 80 Hz) would facilitate the temporal summation of post-synaptic excitatory potentials and reflexively activate spinal motoneurons through Ia afferents (Dideriksen et al., 2015), which may increase force production. Another potential advantage of wide pulse high frequency (WPHF) NMES is that low stimulation intensities are required to limit antidromic collision, and these lower intensities are associated with less discomfort (Delitto et al., 1992). Therefore, by stimulating at intensities expected to generate ~10% of the maximal voluntary contraction (MVC) force, WPHF NMES induces, in some individuals, a progressive increase in force during the stimulation, called ‘extra force’. It can reach up to 80% of the MVC force in plantar flexors (Neyroud et al., 2018) but the response to WPHF NMES in other muscle groups is less documented. Extra force is usually accompanied by a prolongation of the surface electromyographic (EMG) activity after cessation of the stimulation, also called ‘sustained EMG activity’ which is interpreted as MU recruited through the central pathway (Neyroud et al, 2018). The main aim of the present study was to explore the effect of varying stimulation parameters on the NMES-evoked force and sustained EMG activity in the plantar flexors, knee extensors and elbow flexors. It was hypothesized that the plantar flexors would show higher centrally-mediated responses to NMES than knee extensors and elbow flexors, especially with large pulse duration.
Methods
Sixteen volunteers, 2 women and 14 men (29 ± 6 yr, 177 ± 6 cm, 74 ± 11 kg) participated to three experimental sessions - one for each muscle group - in a randomized order. The experimental protocol was similar for the three muscle groups and included twelve 10-s NMES trains separated by at least 2 min of rest and delivered at an intensity set initially to evoke 10% of the maximal voluntary contraction force. Stimulation trains were randomly delivered with a combination of frequencies (20, 50, 100 and 147 Hz) and pulse durations (0.2, 1 and 2 ms). Force was collected using specific isometric ergometers and EMG activity was recorded with bipolar electrodes on the soleus, vastus lateralis and biceps brachii muscles. Extra force was calculated as the relative force difference between the last second and the 2nd second of stimulation. Sustained EMG activity was identified as the visible activity on the EMG after the end of the stimulation and quantified over 500 ms as the root mean square (RMS) of this signal normalized by the RMS of the EMG activity measured during the MVC.
Results
Stimulation frequency. Extra force was significantly higher for the plantar flexors than for the elbow flexors at 50 Hz (69 ± 68% vs 38 ± 53%, p = 0.025), 100 Hz (84 ± 71% vs 21 ± 72%, p < 0.001) and 147 Hz (75 ± 84% vs 16 ± 82%, p < 0.001), but not at 20 Hz (p = 0.649). For all the tested frequencies, extra force was not significantly different between plantar flexors and knee extensors (p = 0.065 - 0.743). Extra force was significantly higher for the knee extensors than for the elbow flexors at 100 Hz (63 ± 106% vs 21 ± 72%, p = 0.012), but not at the other frequencies (p = 0.156 - 0.388). Sustained EMG activity was significantly higher for the plantar flexors than for the elbow flexors at all frequencies (p < 0.001) as well as compared to the knee extensors at 50 Hz, 100 Hz and 147 Hz (p = 0.010, p = 0.009, p = 0.003 respectively) but not at 20 Hz (p = 0.483). Finally, sustained EMG activity was significantly higher for the knee extensors than for the elbow flexors at for all the tested stimulation frequencies (p < 0.05).
Pulse duration. Extra force was significantly higher for the plantar flexors than for the elbow flexors with pulse durations of 1 ms (76 ± 74% vs 23 ± 48%, p < 0.001) and 2 ms (73 ± 70% vs 29 ± 88%, p < 0.001) but not with 0.2 ms (p = 0.064). Extra force was not significantly different between the plantar flexors and the knee extensors, and the knee extensors showed a higher extra force than elbow flexors with 1 ms (56 ± 99% vs 23 ± 48%, p = 0.002). Sustained EMG activity was significantly higher for the plantar flexors than the elbow flexors with all pulse durations (p < 0.001) and than the knee extensors with 1 and 2 ms (p < 0.001). Knee extensors showed a higher sustained EMG activity than elbow flexors with 0.2 ms and 2 ms (p < 0.001) but not with 1 ms.
Discussion/Conclusion
WPHF NMES is a promising tool for (re)training and the results of the present study suggest that its use to induce centrally-mediated force is more pertinent in lower limb muscles. The difference in responses between muscle groups could be explained by muscle typology and density in neuromuscular spindles. Indeed, muscles involved in precise movements and postural control have a greater number of neuromuscular spindles, which are mainly located in type 1 fibers (Botterman et al., 1978). The greater centrally-mediated responses in the plantar flexors compared with the elbow flexors can be explained by the difference in muscle typology (more type I muscle fibers in the postural lower limb muscles). It may also justify the absence of difference in extra force between plantar flexors and knee extensors as they both contribute to postural maintenance (Jusić et al., 1995). Since the effectiveness of NMES for neuromuscular adaptations depends on the amount of force generated during training (Maffiuletti et al., 2018), these results suggest that the use of WPHF NMES would be efficient on plantar flexors and knee extensors for training and rehabilitation and that wide pulses and high frequencies should be preferentially used when implementing this NMES modality in clinical settings.
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