Group-level cortical and muscular connectivity during perturbations to walking and standing balance

Abstract

Maintaining balance is a complex process requiring multisensory processing and coordinated muscle activation. Previous studies have indicated that the cortex is directly involved in balance control, but less information is known about cortical flow of signals for balance. We studied source-localized electrocortical effective connectivity dynamics of healthy young subjects (29 subjects: 14 male and 15 female) walking and standing with both visual and physical perturbations to their balance. The goal of this study was to quantify differences in group-level corticomuscular connectivity responses to sensorimotor perturbations during walking and standing. We hypothesized that perturbed visual input during balance would transiently decrease connectivity between occipital and parietal areas due to disruptive visual input during sensory processing. We also hypothesized that physical pull perturbations would increase cortical connections to central sensorimotor areas because of higher sensorimotor integration demands. Our findings show decreased occipito-parietal connectivity during visual rotations and widespread increases in connectivity during pull perturbations focused on central areas, as expected. We also found evidence for communication from cortex to muscles during perturbed balance. These results show that sensorimotor perturbations to balance alter cortical networks and can be quantified using effective connectivity estimation.

Keywords: Balance perturbation; Effective connectivity; Electroencephalography; Independent component analysis; Virtual reality.

Conflict of interest statement

Declarations of interest: none

Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.

Figures

Figure 1.. Sketch of the two perturbation types.

During the experiment, subjects were physically or visually perturbed while either walking or standing on a treadmill-mounted balance beam. During the rotation perturbations (left), subjects wore a virtual reality headset and had their field of view briefly rotated 20 degrees clockwise or counterclockwise. Pull perturbations (right) involved a brief, mediolateral tug at the subject’s waist. Colored dots denote approximate EMG placements at 8 lower leg muscles: left tibialis anterior (pink), left peroneus longus (orange), left medial gastrocnemius (blue), left soleus (red), right tibialis anterior (yellow), right peroneus longus (purple), right medial gastrocnemius (green) and right soleus (cyan).

Figure 2.. Schematic of processing pipeline.

The EEG (green) and EMG (red) preprocessing steps are shown, along with the corticomuscular connectivity estimation (blue).

Figure 3.. Cortical cluster locations.

Cortical dipole locations for all 29 subjects are shown after retaining at most one dipole per cluster per subject. Dipoles are colored according to the 8 identified cortical clusters: left occipital (pink), right occipital (orange), posterior parietal (blue), anterior parietal (red), left sensorimotor (yellow), right sensorimotor (purple), supplementary motor area (green), and anterior cingulate (cyan). Large dots denote each cluster centroid.

Figure 4.. Cortical event-related spectral perturbations (ERSPs) to visual rotations.

EEG spectral power modulations to rotation perturbations are shown during standing and walking conditions. Results were generated from the fitted models for each subject, instead of averaging across trials. We subtracted out baseline activity during the half-second before perturbation onset. Red indicates increased spectral power compared to baseline, known as synchronization, while blue reflects a decrease in spectral power relative to baseline, known as desynchronization. We set non-significant differences from baseline to 0 (p>0.05). Vertical dashed lines indicate perturbation onset at 0 seconds and offset at 0.5 seconds. We found distinct spectral patterns in theta (4–8 Hz), alpha (8–13 Hz), and low gamma (30–50 Hz), primarily in occipital and posterior parietal areas.

Figure 5.. Cortical event-related spectral perturbations (ERSPs) to physical pulls.

EEG spectral power modulations to pull perturbations are displayed during standing and walking conditions using fitted models for each subject. We subtracted out the half-second before perturbation onset as a baseline. Red indicates increased spectral power compared to baseline, or synchronization, while blue reflects decreased spectral power relative to baseline, or desynchronization. We zeroed out all non-significant differences from baseline (p>0.05). Vertical dashed lines indicate perturbation onset at 0 seconds and offset at 1 second. We found similar synchronization/desynchronization patterns to the visual perturbations, but primarily located in central motor areas.

Figure 6.. Muscular event-related spectral perturbations (ERSPs) to physical pulls.

Lower leg EMG spectral power fluctuations to pull perturbations are shown during standing and walking conditions, after averaging fitted model results across subjects. We subtracted out the half-second before perturbation onset as a baseline. Red indicates an increase in spectral power compared to baseline, while blue reflects decreased spectral power relative to baseline. We zeroed out any non-significant differences from baseline (p>0.05). Vertical dashed lines indicate perturbation onset at 0 seconds and offset at 1 second. EMG ERSPs show increased magnitude from walking to standing across all muscles recorded from, particularly for both medial gastrocnemius muscles.

Figure 7:. Baseline connectivity results.

Plots show mean baseline (A) cortical, (B) muscular, and (C) corticomuscular connectivity with standard error bars. Results were assessed using a two-way ANOVA with false discovery rate correction for multiple comparisons (# means significant effect of (A) perturbation, (B) inter/intra-leg, or (C) corticomuscular connectivity direction; † indicates significant effect of physical task, p

Figure 8:. Perturbation-evoked cortical connectivity.

Chord diagrams show average cortico-cortical connection strengths during the 1 second after perturbation onset, after subtracting baseline activity during the half-second preceding perturbation onset. Cortical areas are left occipital (LO), right occipital (RO), posterior parietal (PP), anterior parietal (AP), left sensorimotor (LS), right sensorimotor (RS), supplementary motor area (SMA), and anterior cingulate (ACC). Red connections indicate significantly increased connectivity from baseline in both directions, blue ones indicate significantly decreased connectivity from baseline in both directions, and magenta ones denote one direction is significantly increased from baseline while the other direction is significantly decreased. Gray denotes non-significant connections. Each cortical area’s arc segment is scaled from 0 to 12e-4. Alpha connectivity during stand rotate was decreased between nearby occipital (LO, RO, PP) and parietal (LS, RS, AP) areas. In stand pull, supplementary motor area was a hub of theta connectivity, with significant bidirectional connections between it and LS, AP, ACC, RS, and RO. The SMA and ACC connection persists during walk pull, but otherwise walking conditions have minimal similarities to the stand conditions.

Figure 9:. Perturbation-evoked intermuscular connectivity.

Chord diagrams show average intermuscular connection strengths during the 1 second following perturbation onset, after subtracting baseline activity during the half-second preceding perturbation onset. Lower leg muscles are left/right tibialis anterior (LTA/RTA), left/right peroneus longus (LPL/RPL), left/right medial gastrocnemius (LMG/RMG), and left/right soleus (LSO/RSO). Red connections indicate significantly increased connectivity from baseline in both directions, blue ones denote significantly decreased connectivity from baseline in both directions, and magenta ones indicate significantly increased connectivity from baseline in one direction with significantly decreased connectivity in the other direction. Gray denotes non-significant connections. Muscles in each diagram are split by left/right leg. Scale is 0 to 20e-4. Peroneus longus/soleus and tibialis anterior/peroneus longus connections persist across all conditions. Additionally, LMG and LSO show stronger incoming theta connections than RMG and RSO during stand pull.

Figure 10:. Event-related corticomuscular connectivity.

Chord diagrams show average corticomuscular connection strengths during the 1 second following perturbation onset, following baseline subtraction of the half-second preceding perturbation onset. Cortical sources are left occipital (LO), right occipital (RO), posterior parietal (PP), anterior parietal (AP), left sensorimotor (LS), right sensorimotor (RS), supplementary motor area (SMA), and anterior cingulate (ACC). Lower leg muscles are left/right tibialis anterior (LTA/RTA), left/right peroneus longus (LPL/RPL), left/right medial gastrocnemius (LMG/RMG), and left/right soleus (LSO/RSO). Red connections indicate significantly increased connectivity from baseline in both directions, blue ones denote significantly decreased connectivity from baseline in both directions, and magenta ones indicate one direction is significantly increased from baseline while the other direction is significantly decreased. Gray denotes non-significant connections. Only connections between muscles and cortical areas are displayed. Scale is only 0 to 2e-4. Overall, connectivity is stronger from the cortex to the muscles compared to the reverse direction. During stand pull, alpha connectivity decreased from baseline at LPL and between LS and RMG, while theta connectivity increased between LMG and RS, RO, AP, and ACC.