Abstract

Postural responses that effectively recover balance following unexpected postural changes need to be tailored to the characteristics of the postural change. We hypothesized that cortical dynamics involved in top-down regulation of postural responses carry information about directional postural changes (i.e., sway) imposed by sudden perturbations to standing balance (i.e., support surface translations). To test our hypothesis, we evaluated the single-trial classification of perturbation-induced directional changes in postural stability from high-density EEG. We analyzed EEG recordings from six young able-bodied individuals and three older individuals with chronic hemiparetic stroke, which were acquired while individuals reacted to low-intensity balance perturbations. Using common spatial patterns for feature extraction and linear discriminant analysis or support vector machines for classification, we achieved classification accuracies above random level (p < 0.05; cross-validated) for the classification of four different sway directions (one vs. the rest scheme). Screening of spectral features (3-50 Hz) revealed that the highest classification performance occurred when low-frequency (3-10 Hz) spectral features were used. Strikingly, the participant-specific classification results were qualitatively similar between young able-bodied individuals and older individuals with chronic hemiparetic stroke. Our findings demonstrate that low-frequency spectral components, corresponding to the cortical theta rhythm, carry direction-specific information about changes in postural stability. Our work presents a new perspective on the cortical representation of postural stability and the possible role of the theta rhythm in the modulation of (directional) reactive balance responses. Importantly, our work provides preliminary evidence that the cortical encoding of direction-specific changes in postural stability is present in chronic hemiparetic stroke.

Highlights

  • H UMAN standing balance and upright posture are maintained through interactions of hierarchically organized and highly interconnected neural ensembles distributed across the central nervous system (CNS), including the cerebral cortex [1], [2]

  • Our finding demonstrates an association between the low-frequency cortical rhythms and the cortical representation of postural stability; presumably for the appropriate selection and/or modulation of direction-specific postural responses

  • The scalp topographies associated with the spectral features leading to the highest classification performance suggest a role of the fronto-central theta rhythm in the cortical representation of postural stability

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Summary

Introduction

H UMAN standing balance and upright posture are maintained through interactions of hierarchically organized and highly interconnected neural ensembles distributed across the central nervous system (CNS), including the cerebral cortex [1], [2]. The cortical responses to balance perturbations appear in the electroencephalogram (EEG) between 30 and 400 ms after perturbation onset, with a broad scalp distribution and a rich spectral composition [4]–[6]. The cortical responses may reflect concurrent cognitive and sensorimotor processes related to the integration of the multisensory input (visual, vestibular, and proprioceptive) associated with sudden postural changes [7], [8] and to the detection of a mismatch between expected and current postural stability, as a form of error detection [9], [10] or sensorimotor conflict [4]. Soon after perturbation onset, a transient enhancement of the theta (3-7 Hz) rhythm appears in frontal, central, parietal, and occipital cortical areas, irrespective of the sensory modality of the perturbation (visual or physical perturbations; [4]) or the subsequent postural response (stepping or maintaining both feet in place; [5]). A similar pattern has been observed during a balance beam walking task during the double support phase of the gait cycle directly preceding the loss of

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