Classification of Rhythmic Cortical Activity Elicited by Whole-Body Balance Perturbations Suggests the Cortical Representation of Direction-Specific Changes in Postural Stability

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 lowintensity 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 participantspecific 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.

Mobile Brain Imaging to Examine Task-Related Cortical Correlates of Reactive Balance: A Systematic Review

“…This section included 8 studies that assessed changes in low-to-high frequency bands in response to unpredicted perturbations in stance ( n = 5) [ 49 , 77 , 79 , 81 , 82 , 83 , 85 ], walking ( n = 2) [ 86 , 88 ] and multiple tasks ( n = 1) [ 48 ] (stance and walking) ( Table 3 ). While a majority of these studies included young adults ( n = 5), one study examined cortical activations in healthy older adults [ 85 ] and two studies compared cortical activations in people with chronic cortical stroke [ 49 ] and chronic traumatic brain injury [ 83 ] with healthy counterparts. Studies analyzed changes in cortical frequencies including alpha (7.5–12.5 Hz), beta (13–30 Hz), gamma (40–100 Hz) and theta (4–8 Hz).…”

“…Pathological populations: Unpredicted perturbations only: Solis-Escalante et al [ 49 ] exposed people with chronic stroke and young adults to unpredicted stance perturbations via movable platform. This study reported perturbation direction-specific pictographic presentations of theta band activation patterns similar in both groups.…”

“…Studies have also indicated that physiological aging [ 32 , 33 , 34 , 35 , 36 ] and neurological impairment [ 37 , 38 , 39 , 40 ] are associated with alterations in compensatory stepping and impaired reactive balance control, which might be related to changes in cortical substrates. Evidence from studies using neuroimaging modalities supported these postulations from behavioral studies regarding possible cortical modulation of reactive balance responses [ 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 , 50 , 51 ]. In the past 2 decades, several neuroimaging modalities have been used by researchers to examine reactive balance control including magnetic resonance imaging (MRI) [ 52 , 53 , 54 ], functional MRI (fMRI) [ 55 , 56 ], positron emission tomography (PET) [ 57 , 58 ], electroencephalography (EEG) [ 41 , 42 , 59 , 60 , 61 , 62 , 63 ], and functional near-infrared spectroscopy (fNIRS) [ 50 , 51 , 64 , 65 ].…”

Toward passive BCI: asynchronous decoding of neural responses to direction- and angle-specific perturbations during a simulated cockpit scenario

“…Our results proved that the P2 component was laterized in the right hemisphere for right perturbations and vice versa, which is in conflict with previous studies and could be described by different EEG setups and analyzing procedures. Additionally, it was shown that the forward and backward perturbations can be decoded by using the spectral information (3–10 Hz) of brain signals in the frontocentral areas 58 . Our findings provide evidence that direction-specific instability was encoded across the fronto-centro-parietal region, which is in accordance with the reported study.…”

Assessment of Biomechanical Predictors of Occurrence of Low-Amplitude N1 Potentials Evoked by Naturally Occurring Postural Instabilities

“…Several studies [11,13,32] have attempted to identify an early cortical sign of postural instability. A negative potential (N1) generated over the fronto-central region, around 100-200 ms following naturally occurring instability while standing still [14] or following external perturbation of the support surface [6,7,9,10,17,19,21,22] has been suggested to indicate the involvement of higher-order processing in the form of detecting an error due to the difference between anticipated and actual postural states and signaling functional postural responses, if necessary [9,10,13,27,32]. These findings suggest that the occurrence of N1 would always indicate a presence of postural instability, regardless of its cause.…”