Muscle activation in response to perturbations during standing (Figure 3)
Figure 3 illustrates the sequence and magnitude of muscle activations (color-coded) in response to physical perturbations during the standing conditions. The figure comprises data on EMG onset latency, duration and magnitude of each muscle activation seen during all standing experimental conditions. Complementing this figure is Table 1 (Supplementary file #3), which details the corresponding numeric values. In addition, Supplementary file #6 provides the statistical output from the analyses of onset latency and duration of activation during standing conditions.
Description of muscle onset patterns of vertical perturbations
During standing conditions, downward perturbations led to a shorter onset latency of anterior muscles (see Table 1, Figure 3) (earliest activation was observed at the rectus femoris; e.g. 0.66±0.32s, right-side muscle after eyes-closed conditions) when compared to posterior muscles (latest activation was observed at the paraspinals; e.g. 1.03±0.22s, right-side muscle after eyes-closed conditions). For instance, the pattern was observed in all comparisons between left and right paraspinals vs. all anterior muscles (e.g. p=0.0053 and p=0.0004 when compared to left tibialis anterior), with the only exception being left paraspinal vs. left rectus abdominis (p=0.0579); the pattern was also evident in the comparisons between left biceps femoris vs. left tibialis anterior (p=0.0162), left and right rectus femoris (p=0.0021 and p<0.0001, respectively), right rectus abdominis (p=0.0063) and left and right external oblique (p=0.0317 and p=0.0241, respectively); and for right biceps femoris vs. right rectus femoris (p=0.0025) (all comparisons based on the computation of marginal means for each combination of muscle and perturbation direction, independent of the factor for sensory condition).
In contrast, upward perturbations triggered earlier onset latencies of posterior muscles, marked by earliest activation at the biceps femoris (see Table 1, Figure 3) (e.g. 0.50±0.39s, left-side muscle following static-camera conditions) and latest activation at the rectus abdominis (e.g. 1.08±0.49s, right-side muscle following static-camera conditions). For instance, both (left and right) gastrocnemius and biceps femoris had an onset latency significantly earlier than the anterior muscles (e.g. p=0.0026 for right gastrocnemius; and p=0.0001 for right biceps femoris, respectively, compared to right rectus femoris); the only exceptions were left gastrocnemius vs. right tibialis anterior (p=0.1352) and right gastrocnemius vs. right tibialis anterior (p=0.1061). Finally, the onset latency of lower-leg antagonist muscles (i.e. tibialis anterior and gastrocnemius) were not statistically different to each other following vertical perturbations, except that the left tibialis anterior was activated earlier than left and right gastrocnemius after upward perturbations (p=0.0070 and p=0.0048, respectively; see Figure 3).
Muscle activation - Comparison of vertical and horizontal perturbations
Forward perturbations led to earlier onset latencies of anterior muscles, whereas posterior muscles were the first to respond after backward perturbations; similar to downward and upward perturbations, respectively (see Table 1, Figure 3). Unlike vertical perturbations, during which proximal leg muscles activated first, forward and backward perturbations elicited initial activation of the distal leg muscles (tibialis anterior and gastrocnemius). For instance, following forward perturbations, left tibialis anterior activated earlier than left and right paraspinals (respectively p=0.0004 and p=0.0039). In turn, following backward perturbations, right gastrocnemius activated earlier than both left and right rectus abdominis and external oblique (p<0.0001 for each of the four comparisons).
Onset latencies were shorter during horizontal perturbations (fastest responses followed forward perturbations) in comparison to vertical perturbations (downward perturbations generated the most delayed responses); for instance, p<0.0001 in the comparison between downward and forward perturbations, independent of the factors for muscle and sensory condition.
Duration of activation (similar to onset latency) was shorter following horizontal perturbations in comparison to vertical perturbations, with backward perturbations eliciting the longest durations (p<0.0001 in the comparisons of backward, forward perturbations vs. downward, upward perturbations, independent of the factors for muscle and sensory condition).
Magnitude of activation was usually larger for horizontal (forward and backward) perturbations when compared to vertical perturbations (downward and upward). The pattern was observed for all muscles. For example, magnitude of the right biceps femoris was larger for backward than for downward perturbations (p=0.0016), and larger for backward than for upward perturbations (p<0.0001).
Muscle activation - Comparison of visual conditions during physical perturbations
Static-camera conditions led to longer onset latencies in comparison to both eyes-closed (p=0.0085) and dynamic-camera conditions (p<0.0001).
The eyes-closed condition led to longer durations of activation in comparison to static-camera (p<0.0001) and dynamic-camera conditions (p=0.0008).
Statistically different magnitudes were observed across the three sensory conditions. For instance, the eyes-closed condition elicited the largest magnitudes, which were significantly higher than in the dynamic-camera condition that elicited the lowest activation magnitudes. This pattern was evident for all muscles; e.g., for the left paraspinals, in the comparisons between eyes-closed vs. static camera (p=0.0445) and vs. dynamic camera conditions (p=0.0014). Exceptions to this pattern were the right rectus femoris (p=0.0751, from ANOVA results within the sensory condition factor), right external oblique (p=0.085), and for both left and right rectus abdominis muscles (respectively, p=0.0954 and p=0.1206).
Extrapolated center of mass - Description and comparison after vertical and horizontal perturbations
Major ellipse angles were significantly larger (over 90 degrees) following both downward and upward perturbations, in comparison to both forward and backward perturbations (during which, angles were approximately 90 degrees) (Figure 4). Vertical perturbations generated larger minor ellipse angles (approximately 30 degrees) in comparison to horizontal perturbations (approximately zero degrees) (p<0.0001). Moreover, minor ellipse angles were greater in static-camera conditions in comparison to both dynamic-camera (p=0.0318) and eyes-closed conditions (p=0.0115).
The area of the extrapolated center of mass was significantly larger following forward perturbations when compared to the remaining three perturbation directions (p<0.0001). Similar results were found for the major and minor axes of the ellipses. Backward perturbations elicited larger areas than both downward (p=0.0004) and upward perturbations (p=0.0003), and backward perturbations elicited larger major (but not minor) axes than both vertical perturbations (p<0.0001).
Extrapolated center of mass - Comparison of visual conditions and before vs. after perturbation
In the analysis of conditions prior to perturbation onset, we found that eyes-closed conditions generated larger major ellipse angles (near 90 degrees) in comparison to both static-camera (p=0.0100) and dynamic-camera conditions (p=0.0084).
In the comparisons pre vs. post perturbation onset, we found that ellipse area, as well as major and minor axes increased after perturbation, which occurred for all combinations of sensory conditions and perturbation directions (e.g. respectively, p=0.0002, p=0.0001 and p<0.0001 for downward perturbations in dynamic camera conditions). However, major and minor axis angles only exhibited significant changes for both downward and upward perturbations and not for horizontal perturbations (p<0.05). For example, for upward perturbations with static camera, we observed changes in major (p=0.0247) and minor angles (p=0.0125); but for forward perturbations in dynamic camera no changes were observed in major (p=0.3441) and minor angles (p=0.4652). Importantly, major angles for dynamic- and static-camera conditions usually transitioned from ~60°-70° (before perturbation) to ~110-120° (after perturbation), while major axis angles during the eyes-closed condition commonly exhibited a transition from ~90° to ~30°.
Muscle activations in response to perturbations during walking (Figure 5)
Figure 5 illustrates the sequence and magnitude of muscle activations (color-coded) in response to physical perturbations during walking. The figure comprises data on EMG onset latency, duration, and magnitude of each muscle activation seen during walking. Complementing this figure is Table 2 (Supplementary file #4), which details the corresponding numeric values. In addition, Supplementary file #6 provides the statistical output from the analysis of onset latency and duration of activation during walking conditions.
Description of muscle onset patterns of vertical perturbations
Following downward perturbations, the contralateral deltoid had an earlier response (i.e. onset latency) in comparison to the ipsilateral deltoid (0.38±0.33s vs. 0.55±0.36s, p=0.0394), and the ipsilateral gastrocnemius had an earlier response in comparison to the respective contralateral muscle (0.50±0.32s vs. 0.95±0.52s, p<0.0001). In addition, contralateral external oblique, paraspinal and deltoid muscles were the first to be activated; all of which had a latency significantly shorter than the ipsilateral tibialis anterior and rectus abdominis, and contralateral gastrocnemius (e.g. the contralateral deltoid compared, respectively, to the latter three muscles: p=0.0036, p=0.0164 and p<0.0001).
Following upward perturbations, no differences between ipsilateral and contralateral muscles were found. Both ipsilateral and contralateral rectus femoris were first to respond (e.g. contralateral side: 0.34±0.16s), with a latency significantly shorter than that of the gastrocnemius bilaterally (e.g. contralateral side: 0.60±0.31s; p=0.0011), the ipsilateral external oblique (p=0.0184) and contralateral deltoid (p=0.0228). After the activation of rectus femoris, the ipsilateral biceps femoris and the contralateral rectus abdominis activated, which exhibited earlier onset latencies than the gastrocnemius (p=0.0074 and p=0.0050, respectively).
Downward perturbations generated a shorter duration of activation in the contralateral gastrocnemius (0.53±0.29s) compared to all other muscles; for example, in the comparisons with contralateral tibialis anterior (p=0.0032) and biceps femoris (p=0.0020), and with ipsilateral paraspinal (p=0.0012) and deltoid (p=0.0027) muscles. In addition, the ipsilateral deltoid had a shorter activation when compared to the contralateral deltoid (0.79±0.29s vs. 0.95±0.31s, p=0.0291). The muscles with the longest durations of activation were the contralateral paraspinal, external oblique and deltoid.
After upward perturbations, the contralateral gastrocnemius had the shortest duration of activation (0.67±0.25s) when compared to all other muscles (e.g., when compared to ipsilateral and contralateral rectus abdominis: p=0.0108 and p=0.0186 respectively). The only exception to this pattern was with ipsilateral external oblique: 0.77±0.28s, p=0.1770. The longest durations were evident at the ipsilateral tibialis anterior, contralateral deltoid, and mainly, in both paraspinals; all of these muscles’ durations of activation were significantly longer than those of the contralateral gastrocnemius and ipsilateral external oblique. For example, p<0.0001 in the comparison between ipsilateral tibialis anterior and contralateral gastrocnemius, and p=0.0027 when comparing ipsilateral external oblique and paraspinal muscles.
Muscle activation - Comparison of vertical and horizontal perturbations
Onset latency after downward perturbations was significantly longer (i.e. delayed) when compared to the upward (p=0.0021), forward (p=0.0002) and backward (p<0.0001) perturbations.
Duration of activation after downward perturbations was shorter in comparison to both upward (p=0.0023) and forward perturbations (p<0.0001), but not to backward perturbations (p=0.3786).
Effects of visual-only perturbations (Figures 6-7)
Effective muscle activation (i.e., removing the “no response” cases, see Methods) following visual perturbations was evident 118 to 143 times per participant out of 192 exposures to visual perturbations (exposures being defined by 3 repetitions of 4 perturbation directions across 16 muscles), for an average of 67.7% effective muscle responses. For an example of a response to a visual perturbation, see Figure 6.
Figure 7 illustrates the sequence and magnitude of muscle activations (color-coded) in response to visual perturbations. Complementing this figure is Table 3 (Supplementary file #5), which details the numeric values. In addition, Supplementary file #6 provides the statistical output from the analysis of onset latency and duration of activation during visual conditions.
Forward visual perturbations led to the most delayed onset latencies, significantly longer when compared to the downward (p=0.0002), upward (p=0.0015) and backward (p<0.0001) visual perturbations. No statistical effect on onset latency was found across muscles (p=0.0969) (Figure 7).
Longest duration of activation was observed in tibialis anterior, gastrocnemius, and biceps femoris. In contrast, the left rectus abdominis presented with the shortest duration of activation (e.g., compared with the left side of the aforementioned three muscles, respectively, p=0.0004, p=0.0011 and p=0.0014). Backward visual perturbations led to the longest durations of activation, whereas forward visual perturbations led to the shortest durations of activation. For instance, duration of activation following forward visual perturbations was shorter than downward (p=0.0014) and backward (p=<0.0001) visual perturbations, but not when compared to upward visual perturbations (p=0.0851).
Within visual perturbations, different perturbation directions did not lead to significantly different magnitudes within each muscle (e.g., p=0.5858 in the analysis for right biceps femoris).