Elsevier

Neuroscience Letters

Volume 592, 10 April 2015, Pages 1-5
Neuroscience Letters

Research article
Cortical processes associated with continuous balance control as revealed by EEG spectral power

https://doi.org/10.1016/j.neulet.2015.02.049Get rights and content

Highlights

  • This is the first study investigating cortical theta activity during continuous balance tasks varying in difficulty.

  • Higher demands on continuous balance control are associated with an increase in frontal and parietal midline theta power.

  • Fronto–central and centro–parietal theta power is correlated with balance performance.

Abstract

Balance is a crucial component in numerous every day activities such as locomotion. Previous research has reported distinct changes in cortical theta activity during transient balance instability. However, there remains little understanding of the neural mechanisms underlying continuous balance control. This study aimed to investigate cortical theta activity during varying difficulties of continuous balance tasks, as well as examining the relationship between theta activity and balance performance. 37 subjects completed nine balance tasks with different levels of surface stability and base of support. Throughout the balancing task, electroencephalogram (EEG) was recorded from 32 scalp locations. ICA-based artifact rejection was applied and spectral power was analyzed in the theta frequency band. Theta power increased in the frontal, central, and parietal regions of the cortex when balance tasks became more challenging. In addition, fronto–central and centro–parietal theta power correlated with balance performance. This study demonstrates the involvement of the cerebral cortex in maintaining upright posture during continuous balance tasks. Specifically, the results emphasize the important role of frontal and parietal theta oscillations in balance control.

Introduction

Recent research indicates the involvement of cortical structures during control of balance and posture [6], [13], [20]. Specifically, this research identified an important role of fronto–central cortical regions including the anterior cingulate cortex (ACC) which is well-known to be crucially involved in action monitoring and the detection of error signals [26]. In the context of balance control, Adkin et al. [1] defined the “error signal” as a discrepancy between expected and actual state of balance during transient balance perturbations. This is comparable to the so called “error-related negativity/error-negativity (ERN/EN)” potential [8] observed after incorrect responses during cognitive task performance. In fact, several studies reported increased fronto–central and/or ACC activity during the performance of a balance task that was attributed to the detection of balance instability [2], [10], [14]. fMRI studies reported an increase in ACC activity during successful recognition of unstable posture [22], [23]. Importantly, ACC activity did not significantly differ from baseline activity in unsuccessful trials, demonstrating the ACC’s involvement in detecting balance disturbances [22]. Electroencephalographic (EEG) studies on balance control by Slobounov et al. [20], [24] and Sipp et al. [19] confirmed these results by locating increased cortical activity in the ACC when standing on one leg and when walking on a balance beam, respectively. ACC activity during postural instability was further characterized by increased theta spectral power, indicating theta oscillatory activity to subserve error detection and processing during balance control.

In addition to the ACC, parietal cortical regions were also activated during recognition of postural instability and balance beam walking [19], [22]. In particular, the posterior parietal cortex (PPC) receives multimodal input from somatosensory, vestibular and visual systems. Thus, the PPC represents a key region for sensory information processing and sensorimotor transformation processes [16]. PPC contribution to balance control is indicated by the results of Adkin et al. [1], reporting not only fronto–central but also parietal distribution of the N1 perturbation evoked cortical response. In addition, Slobounov et al. [20] found also cortical activity in the PPC (BA7) during one leg stance as revealed by independent component analysis. This is in accordance with the results of Sipp et al. [19] providing a similar frontal and parietal spatial distribution of cortical activity when balance was disturbed during balance beam walking. Importantly, this was accompanied by increased theta activity in frontal and parietal cortical areas primarily located along the cortical midline. The authors suggested increased theta activity distributed over frontal and parietal regions reflects sensory information transfer from parietal areas to anterior cingulate regions involved in error detection and processing [19]. The cumulative pattern of the above described results emphasizes increased theta oscillatory activity including the fronto–central and parietal cortex to subserve balance control.

The functional significance of frontal and parietal involvement during balance control is further supported by longitudinal studies on the effects of balance training on neural structure [18], [25]. Gray matter volume increased in frontal and parietal cortical areas after six weeks of continuous balance training and this was correlated with improvements in balance performance [25].

While the latter study highlights the effectiveness of continuous balance tasks to induce adaptations in neural structure, there is a lack of research investigating the underlying functional neural correlates when exposed to continuous postural instability. Therefore, this study aimed to investigate cortical theta oscillations during continuous balance tasks varying in surface stability and base of support. It is expected that the error signal increases with increasing balance demands. As theta activity in frontal and parietal cortex was suggested to indicate error detection and processing [19], we hypothesized that frontal and parietal theta activity should be higher during balance control with reduced surface stability and/or base of support.

It was further hypothesized that frontal and parietal theta power should correlate with balance performance as the amount of error detection and processing should be lower in high balance performers who exhibit less platform oscillations.

Section snippets

Methods

39 healthy male university students participated in the study. In two subjects, the applied artefact detection algorithm prior to independent component analysis (ICA) detected artefacts in more than 80% of all segments within several balance conditions; therefore, the number of the remaining segments was considered as not sufficient for further analyses (please see below for details on EEG data preprocessing and analysis). The remaining 37 participants (age: 24.7 ± 3 years; body weight: 77.3 ± 8.1 

Results

Mean platform oscillations are illustrated in Fig. 1a. The ANOVA on platform oscillations revealed a significant main effect for SUS (F1,37 = 80.93, p < 0.001), BOS (F2,74 = 52.52, p < 0.001), as well as a SUS × BOS interaction (F2,74 = 49.97, p < 0.001). Platform oscillations were increased during SUS3 when compared to SUS2 and during unipedal stance (BOS2, BOS3) when compared to bipedal stance (BOS1). Post-hoc analysis of the significant SUS × BOS interaction further revealed that the increase in platform

Discussion

This study is the first to investigate cortical activity in the theta frequency band during continuous balance tasks varying in surface stability and base of support, and to correlate cortical theta activity with balance performance.

In line with our hypothesis, a significant increase in cortical theta power was found when balance task became more challenging. This observation is in agreement with previous research on transient balance perturbations showing that fronto–central theta oscillations

Conflict of interest

The authors declare that they have no conflict of interest.

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