Effect of Task Failure on Intermuscular Coherence Measures in Synergistic Muscles

Abstract

The term "task failure" describes the point when a person is not able to maintain the level of force required by a task. As task failure approaches, the corticospinal command to the muscles increases to maintain the required level of force in the face of a decreased mechanical efficacy. Nevertheless, most motor tasks require the synergistic recruitment of several muscles. How this recruitment is affected by approaching task failure is still not clear. The increase in the corticospinal drive could be due to an increase in synergistic recruitment or to overlapping commands sent to the muscles individually. Herein, we investigated these possibilities by combining intermuscular coherence and synergy analysis on signals recorded from three muscles of the quadriceps during dynamic leg extension tasks. We employed muscle synergy analysis to investigate changes in the coactivation of the muscles. Three different measures of coherence were used. Pooled coherence was used to estimate the command synchronous to all three muscles, pairwise coherence the command shared across muscle pairs and residual coherence the command peculiar to each couple of muscles. Our analysis highlights an overall decrease in synergistic command at task failure and an intensification of the contribution of the nonsynergistic shared command.

Figure 1

Experimental setup and data analysis. (a) Experimental setup. Subjects were seated on a leg extension machine in an upright position. They were asked to perform repetitions of a knee extension task until task failure. Surface EMG signals were recorded from three muscles of the quadriceps: rectus femoris (RF), vastus lateralis (VL), and vastus medialis (VM). (b) EMG signals were band-pass filtered between 30 and 450 Hz, full-wave rectified, and low-pass filtered with a cutoff frequency of 15 Hz to extract the envelope. (c) Nonnegative matrix factorization algorithm was applied to data for LIE and HIE to reconstruct the activity of the three muscles as a single motor module W containing the relative activation weights of the three muscles as recruited by an activation signal H so that M_r ≈ WxH where M_r is the reconstructed matrix. (d) For the coherence analysis, EMG signals were detrended demodulated by means of Hilbert transform. (e) Then, coherence analysis was performed across the three muscles together (pooled coherence), between pairs of muscles (pairwise coherence) and between pairs of muscles after removing components common to the third muscle (residual coherence).

Figure 2

Changes in the muscle module at task failure. The synergistic activation of the RF, VL, and VM in the knee extension task is exploited using the muscle synergy framework. Muscle weighting coefficients are reported for each muscle and each condition (baseline versus task failure) for both (a) LIE and (b) HIE. (c) The compound synergy activation is reported for both LIE and HIE at baseline and task failure. Significance is reported for the comparison baseline versus task failure. ^∗P < 0.05, ^∗∗P < 0.01. RF: rectus femoris; VL: vastus lateralis; VM: vastus medialis; LIE: low-intensity exercise; HIE: high-intensity exercise. All bar plots are presented as the mean ± standard deviation.

Figure 3

Changes in the pooled coherence at task failure. Pooled intermuscular coherence profiles are reported for (a) LIE and (b) HIE. Solid black line represents the baseline condition. Dashed line represents the task failure one. Dotted line is used to depict the confidence level. (c) Average maximum values of the pooled intermuscular coherence across all subjects for both LIE and HIE. Significance is reported for the comparison baseline versus task failure. ^∗P < 0.05. LIE: low-intensity exercise; HIE: high-intensity exercise. All bar plots are presented as the mean ± standard deviation.

Figure 4

Pairwise coherence. Pairwise z-score intermuscular coherence profiles (solid lines) as averaged across all subjects for baseline (solid black line) and task failure (solid grey line) and residual pairwise z-score intermuscular coherence profiles (dashed lines) as averaged across all subjects for baseline (dashed black line) and task failure (dashed grey line). Profiles are depicted for the conditions (a) LIE and (b) HIE and for the pairs (from the top): VL-VM, VL-RF, and VM-RF. Dotted black line represents the confidence level. RF: rectus femoris; VL: vastus lateralis; VM: vastus medialis; LIE: low-intensity exercise; HIE: high-intensity exercise.

Figure 5

Changes in gamma pairwise and residual coherence at task failure. Average maximum value across all subjects in the range [30–100] Hz for the (a) pairwise intermuscular coherence and the (b) residual intermuscular coherence for the pairs (from the top): VL-VM, VL-RF, and VM-RF. Significance is reported for the comparison baseline versus task failure. ^∗P < 0.05. RF: rectus femoris; VL: vastus lateralis; VM: vastus medialis; LIE: low-intensity exercise; HIE: high-intensity exercise. All bar plots are presented as the mean ± standard deviation.

Figure 6

Percentage contribution of the residual coherence in the pairwise coherence. The subplots present the following muscle pairs (from top to bottom): VL-VM, VL-RF, and VM-RF. Significance is reported for the comparison baseline versus task failure. ^∗P < 0.05. RF: rectus femoris; VL: vastus lateralis; VM: vastus medialis; LIE: low-intensity exercise; HIE: high-intensity exercise. All bar plots are presented as the mean ± standard deviation.

Figure 7

Conceptual model of the possible hypothesis suggested for the CNS to regulate the activity of synergistic muscles at task failure. At baseline, the three muscles receive a direct independent cortical command to each muscle (represented as the black pointed arrow) and a synergistic one of both cortical and spinal origin (represented as the common arrow that shades from dark grey, cortical component, to light grey, spinal component). When task failure occurs, the CNS suppresses the synergistic activation (represented as the common solid arrow becoming thinner) in favour of an increased cortical drive to the single muscle (represented as the individual pointed arrows becoming thicker) to keep the level of performance.