Changes in cortical activity associated with adaptive behavior during repeated balance perturbation of unpredictable timing

Andreas Mierau, Thorben Hülsdünker, Heiko K Strüder, Andreas Mierau, Thorben Hülsdünker, Heiko K Strüder

Abstract

The compensation for a sudden balance perturbation, unpracticed and unpredictable in timing and magnitude is accompanied by pronounced postural instability that is suggested to be causal to falls. However, subsequent presentations of an identical perturbation are characterized by a marked decrease of the amplitude of postural reactions; a phenomenon called adaptation or habituation. This study aimed to identify cortical characteristics associated with adaptive behavior during repetitive balance perturbations based on single-trial analyses of the P1 and N1 perturbation-evoked potentials. Thirty-seven young men were exposed to ten transient balance perturbations while balancing on the dominant leg. Thirty two-channel electroencephalography (EEG), surface electromyography (EMG) of the ankle plantar flexor muscles and postural sway (i.e., Euclidean distance of the supporting platform) were recorded simultaneously. The P1 and N1 potentials were localized and the amplitude/latency was analyzed trial by trial. The best match sources for P1 and N1 potentials were located in the parietal (Brodmann area (BA) 5) and midline fronto-central cortex (BA 6), respectively. The amplitude and latency of the P1 potential remained unchanged over trials. In contrast, a significant adaptation of the N1 amplitude was observed. Similar adaptation effects were found with regard to postural sway and ankle plantarflexors EMG activity of the non-dominant (free) leg; i.e., an indicator for reduced muscular co-contraction and/or less temporary bipedal stance to regain stability. Significant but weak correlations were found between N1 amplitude and postural sway as well as EMG activity. These results highlight the important role of the midline fronto-central cortex for adaptive behavior associated with balance control.

Keywords: EEG; N1; P1; adaptation; falls; posture.

Figures

Figure 1
Figure 1
Experimental setup (A) and an example of mean across trials platform oscillations during the initial 5 s after perturbation onset for a representative subject (B).
Figure 2
Figure 2
Raw data traces for (A) mean across subjects and trials electroencephalographic (EEG) activity at electrode Cz and the time windows used for further analyses (top), (B) mean across subjects EMG activity of the dominant leg m. peroneus longus for trial 1 (black) and trial 2 (gray) and (C) mean across subjects EEG activity at electrode Cz for trial 1 (black) and trial 2 (gray).
Figure 3
Figure 3
Mean across subjects platform oscillations (i.e., Euclidean distance) for each trial in the time window pre-N1 and post-N1. Platform oscillations were significantly lower in T1 compared to T2 (initial adaptation) as well as in T2 compared to T10 (longer-term adaptation). Error bars indicate 95% confidence intervals.
Figure 4
Figure 4
LORETA localization (right) of the P1 (upper trace) and N1 (lower trace) potential averaged over trials and subjects (left). A 20 ms peri-peak window was considered for LORETA transformation (blue). LORETA anatomy slides are based on the MNI305 template and locked to the localization of maximal current density during the P1 and N1 potential, respectively. In addition, the coordinates of the voxel reflecting maximal current density (best match) and the corresponding Brodmann area (BA) are presented. Time 0 indicates perturbation onset.
Figure 5
Figure 5
Mean across subjects P1 and N1 amplitude and latency at electrode CPz and FCz, respectively. N1 amplitude was significantly smaller in T1 compared to T2 (initial adaptation), and there was a strong trend towards a further reduction of the N1 amplitude from T2 to T10 (longer-term adaptation). Error bars indicate 95% confidence intervals.
Figure 6
Figure 6
Mean across subjects integrated EMG activity of the ankle plantarflexors in the time window pre-N1 and post-N1 for each trial. EMG activity of the non-dominant m. gastrocnemius lateralis in the time window post-N1 was significantly larger in T1 compared to T10 but not in T1 compared to T2 indicating longer-term but not initial adaptation. Furthermore, EMG activity of the non-dominant m. peroneus longus in the time window post-N1 was significantly larger in T1 compared to T2 as well as in T2 compared to T10 indicating both initial and longer-term adaptation. Error bars indicate 95% confidence intervals.
Figure 7
Figure 7
Correlations between z-scores of the standard normal distribution for the N1 amplitude and platform oscillations (i.e., Euclidean distance) across all subjects and trials in the time window pre-N1 and post-N1. R and p-values indicate correlation coefficients and significance level, respectively.
Figure 8
Figure 8
Correlations between z-scores of the standard normal distribution for the N1 amplitude and muscular activity of the ankle plantarflexors across all subjects and trials in the time window pre-N1 and post-N1. R and p-values indicate correlation coefficients and significance level, respectively. Significant R/P-values are presented in bold.

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