Long-Lasting Event-Related Beta Synchronizations of Electroencephalographic Activity in Response to Support-Surface Perturbations During Upright Stance: A Pilot Study Associating Beta Rebound and Active Monitoring in the Intermittent Postural Control

Abstract

Movement related beta band cortical oscillations, including beta rebound after execution and/or suppression of movement, have drawn attention in upper extremity motor control literature. However, fewer studies focused on beta band oscillations during postural control in upright stance. In this preliminary study, we examined beta rebound and other components of electroencephalogram (EEG) activity during perturbed upright stance to investigate supraspinal contributions to postural stabilization. Particularly, we aimed to clarify the timing and duration of beta rebound within a non-sustained, but long-lasting postural recovery process that occurs more slowly compared to upper extremities. To this end, EEG signals were acquired from nine healthy young adults in response to a brief support-surface perturbation, together with the center of pressure, the center of mass and electromyogram (EMG) activities of ankle muscles. Event-related potentials (ERPs) and event-related spectral perturbations were computed from EEG data using the perturbation-onset as a triggering event. After short-latency (<0.3 s) ERPs, our results showed a decrease in high-beta band oscillations (event-related desynchronization), which was followed by a significant increase (event-related synchronization) in the same band, as well as a decrease in theta band oscillations. Unlike during upper extremity motor tasks, the beta rebound in this case was initiated before the postural recovery was completed, and sustained for as long as 3 s with small EMG responses for the first half period, followed by no excessive EMG activities for the second half period. We speculate that those novel characteristics of beta rebound might be caused by slow postural dynamics along a stable manifold of the unstable saddle-type upright equilibrium of the postural control system without active feedback control, but with active monitoring of the postural state, in the framework of the intermittent control.

Discrete cortical control during quiet stance revealed by desynchronization and rebound of beta oscillations

“…Only the CoP data in AP direction was used for our study. Positions of the left and the right ankle joints were measured by a three-dimensional optical motion capture system (SMART-DX, BTS Bioengineering, Milan, Italy) with a sampling frequency of 300 Hz, using light reflection markers attached on the lateral malleolus [11]. Electromyography (EMG) signals were recorded from the ankle muscles of both the left and the right legs, including the soleus, medial gastrocnemius (MG), tibialis anterior, rectus femoris and biceps femoris muscles.…”

“…All EEG signals were sampled at a sampling frequency of 2048 Hz and stored on a computer for post-processing. Data sampling of CoP, the ankle positions, EMG and EEG were started simultaneously by an identical start-trigger, where the ankle positions and EMG were sampled synchronously using a stroboscope-related clock of the motion capture system [11].…”

“…Measuring cortical neural activity during postural control tasks using electroencephalogram (EEG) can approach such mechanisms. In our previous study, we examined postural responses to an impulsive backward support-surface perturbation during quiet stance and associated EEG, and identified novel brain activities [11]. Particularly, after an appearance of short latency and large amplitude synchronizations at a wide range of frequency bands in a window of a few hundred milliseconds from the perturbation [12][13][14][15][16][17], the beta-band event-related desynchronization (beta-ERD) and the subsequent long-lasting beta-band eventrelated synchronization (beta-ERS) occurred for a few seconds, respectively, during the forward fall response and the backward recovery response to the perturbation.…”

Brain Processes Involved in Motor Planning Are a Dominant Factor for Inducing Event-Related Desynchronization

“…For example, BCI has been used to detect motor intention from brain activity and control medical/assistive devices such as exoskeleton or electrical stimulation to intentionally move paralyzed limbs (Tacchino et al, 2017 ; Bai et al, 2020 ). A widely used feature of brain signals to detect the motor intention is event-related desynchronization/synchronization (ERD/S) (Pfurtscheller and Lopes da Silva, 1999 ; Pfurtscheller, 2001 ), where ERD is a relative spectral power attenuation of electroencephalogram (EEG) during motor execution and motor imagery (Ron-Angevin et al, 2011 ; Formaggio et al, 2013 ), while ERS is a relative spectral power increase like a rebound mainly after the motor execution (Nakamura et al, 2021 ). Pioneering work by Takahashi et al ( 2012 ) revealed that increasing the strength of functional electrical stimulation (FES) in response to the detection of ERD enabled the paralyzed ankle to bend spontaneously after the intervention, whereas the FES alone cannot induce such motor recovery of the stroke patients.…”

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“…For example, BCI has been used to detect motor intention from brain activity and control medical/assistive devices such as exoskeleton or electrical stimulation to intentionally move paralyzed limbs (Tacchino et al, 2017;Bai et al, 2020). A widely used feature of brain signals to detect the motor intention is event-related desynchronization/synchronization (ERD/S) (Pfurtscheller and Lopes da Silva, 1999;Pfurtscheller, 2001), where ERD is a relative spectral power attenuation of electroencephalogram (EEG) during motor execution and motor imagery (Ron-Angevin et al, 2011;Formaggio et al, 2013), while ERS is a relative spectral power increase like a rebound mainly after the motor execution (Nakamura et al, 2021). Pioneering work by Takahashi et al (2012) revealed that increasing the strength of functional electrical stimulation (FES) in response to the detection of ERD enabled the paralyzed ankle to bend spontaneously after the intervention, whereas the FES alone cannot induce such motor recovery of the stroke patients.…”