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. 2020 Dec 1;124(6):1875-1884.
doi: 10.1152/jn.00341.2020. Epub 2020 Oct 14.

Balance perturbation-evoked cortical N1 responses are larger when stepping and not influenced by motor planning

Aiden M Payne  1 , Lena H Ting  1   2
Affiliations

Balance perturbation-evoked cortical N1 responses are larger when stepping and not influenced by motor planning

Aiden M Payne et al. J Neurophysiol. .

Abstract

The cortical N1 response to balance perturbation is observed in electroencephalography recordings simultaneous to automatic balance-correcting muscle activity. We recently observed larger cortical N1s in individuals who had greater difficulty resisting compensatory steps, suggesting the N1 may be influenced by stepping or changes in response strategy. Here, we test whether the cortical N1 response is influenced by stepping (planned steps versus feet-in-place) or prior planning (planned vs. unplanned steps). We hypothesized that prior planning of a step would reduce the amplitude of the cortical N1 response to balance perturbations. In 19 healthy young adults (ages 19-38; 8 men and 11 women), we measured the cortical N1 amplitude evoked by 48 backward translational support-surface perturbations of unpredictable timing and amplitude in a single experimental session. Participants were asked to plan a stepping reaction on half of perturbations, but to resist stepping otherwise. Perturbations included an easy (8 cm, 16 cm/s) perturbation that was identical across participants and did not naturally elicit compensatory steps, and a height-adjusted difficult (18-22 cm, 38-42 cm/s) perturbation that frequently elicited compensatory steps despite instructions to resist stepping. In contrast to our hypothesis, cortical N1 response amplitudes did not differ between planned and unplanned stepping reactions, but cortical responses were 11% larger with the execution of planned compensatory steps compared with nonstepping responses to difficult perturbations. These results suggest a possible role for the cortical N1 in the execution of compensatory steps for balance recovery, and this role is not influenced by whether the compensatory step was planned before the perturbation.NEW & NOTEWORTHY The cortical N1 response to balance perturbation is larger when executing compensatory steps, suggesting a relationship between the cortical N1 and subsequent motor behavior. Additionally, the cortical N1 response is not impacted by prior planning of the stepping reaction, suggesting that predictability of the motor outcome does not impact the N1 in the same way as predictability of the perturbation stimulus.

Keywords: EEG; biomechanics; electromyography; kinematics; posture.

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Conflict of interest statement

No conflicts of interest, financial or otherwise, are declared by the authors.

Figures

Fig. 1.
Fig. 1.
Experimental design. Participants were instructed whether or not to plan to step in response to upcoming perturbations. In some cases, participants failed to resist taking a compensatory step, resulting in an unplanned step that was not intended before the perturbation. We test the effect of stepping by comparing stepping reactions (planned step) to nonstepping reactions (planned no step), and we test the effect of planning by comparing planned steps to unplanned steps.
Fig. 2.
Fig. 2.
Instruction to step induced a lateral weight shift but did not influence step latency. A: bar plot shows preperturbation (50–150 ms before perturbation onset) vertical load forces under the stance leg. Forces are shown for trials in which participants were asked to step (denoted by shades of yellow), and for trials in which participants were asked to resist stepping (denoted by black and red). *Significant difference, α = 0.05. B: latency to foot-off is shown for planned steps to easy perturbations (denoted in light yellow), latency to planned steps to difficult perturbations is denoted in dark yellow. Latency to foot-off is shown in red for unplanned steps to difficult perturbations. Latencies to foot-off did not differ between conditions at α = 0.05. There is no black bar corresponding to the nonstepping condition in B because there was no foot-off in this condition, but this nonstepping condition is included in A because this represents the bulk of the trials in which participants were asked not to step.
Fig. 3.
Fig. 3.
Changes in evoked responses with step execution between behaviors that are congruent with the task goal. A: group-averaged cortical responses are shown for nonstepping (black) and planned stepping reactions (yellow) in easy perturbations (left) and difficult perturbations (right). Vertical dashed bars indicate the time window of 100–200 ms. The bar plots show the mean and standard deviation of the difference in N1 response amplitude between the corresponding conditions across participants (planned step – no step). B: group-averaged electromyograph (EMG) responses are shown for each muscle for the same conditions shown in A. Vertical dashed bars indicate the baseline (−150 to −50 ms), early (100–200 ms), and late (200–300 ms) time windows. Bar plots show the mean and standard deviation of the difference in EMG activity between corresponding conditions in each time window across participants. C: group-averaged electrodermal responses are shown for the same conditions shown in A. Vertical dashed bars indicate the time window of 2–6 s. The bar plots show the mean and SD of the difference in electrodermal response amplitude between corresponding conditions. *Significant differences in paired t tests between response conditions within the corresponding time window, α = 0.05 (i.e., any bar marked with an asterisk is significantly different from 0). MG, medial gastrocnemius; SC, sternocleidomastoid; TA, tibialis anterior.
Fig. 4.
Fig. 4.
Changes in evoked responses with prior planning of executed steps. A: group-averaged cortical responses are shown for planned steps (yellow) and unplanned steps (red) in difficult perturbations. Vertical dashed bars indicate the time window of 100–200 ms. The bar plot shows the mean and SD of the difference in N1 response amplitude between conditions across participants (unplanned step – planned step). B: group-averaged EMG responses are shown for each muscle for the same conditions shown in A. Vertical dashed bars indicate the baseline (−150 to −50 ms), early (100–200 ms), and late (200–300 ms) time windows. Bar plots show the mean and SD of the difference in EMG activity between conditions in each time window across participants. C: group-averaged electrodermal responses are shown for the same conditions shown in A. Vertical dashed bars indicate the time window of 2–6 s. The bar plot shows the mean and standard deviation of the difference in electrodermal response amplitude between conditions. *Significant differences in paired t tests between response conditions within the corresponding time window, α = 0.05 (i.e., any bar marked with an asterisk is significantly different from 0). MG, medial gastrocnemius; SC, sternocleidomastoid; TA, tibialis anterior.
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