Electroencephalographic markers of vestibular adaptation and heading perception

Abstract

Background When given a series of sinusoidal oscillations in which the two hemicycles have equal amplitude but asymmetric velocity, healthy subjects lose perception of the slower hemicycle (SHC), reporting a drift towards the faster hemicycle (FHC). This adaptive “neglect” is not reflected in the vestibular-ocular reflex, suggesting that the adaptation is higher-order. Our study aimed to define EEG markers of this perceptual shift. It was hypothesised that the adaptation would be reflected in modulation of parieto-occipital alpha and beta rhythms and strength of frontoparietal networks. Methods Twenty-five subjects underwent a series of whole-body symmetric or asymmetric oscillations. Subjects reported their perceived final head orientation using landmarks in the testing room; this was converted into total position error (TPE). Thirty-two channel EEG was recorded before, during, and after the adaptation period. Spectral power was calculated for the alpha, beta, delta, and theta frequency bands in discrete epochs (cycles) corresponding to each oscillation. Linear mixed models were used to determine a region-by-condition effect of the adaptation. Coherence was analysed using a network-based statistic. Main Findings TPE was significantly greater in the asymmetric condition, always in the direction of the FHC. VOR did not adapt across cycles. An initial desynchronisation was noted in the alpha band, followed by a rebound toward baseline values within a few cycles; this persisted into the post-adaptation period. Rate of alpha resynchronisation was accelerated and attenuated in prefrontal and occipital regions, respectively, for the asymmetric condition only. Functional connectivity networks, primarily comprised of frontoparietal connections, were identified in the beta and delta frequency bands; these networks were stronger during asymmetric stimulation. Conclusions These findings show that the adaptive “neglect” induced by asymmetric vestibular stimulation is associated with modulation of alpha rhythms and frontoparietal networks. The novel results presented here further our understanding of vestibular adaptation during heading perception.