Electroencephalographic response to transient adaptation of vestibular perception

Abstract

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 response is not reflected in the vestibular-ocular reflex, suggesting that the adaptation is of higher order. This study aimed to define EEG correlates of this adaptive response. Twenty-five subjects underwent a series of symmetric or asymmetric oscillations and reported their perceived head orientation at the end using landmarks in the testing room; this was converted into total position error (TPE). Thirty-two channel EEG was recorded before, during and after adaptation. Spectral power and coherence were calculated for the alpha, beta, delta and theta frequency bands. Linear mixed models were used to determine a region-by-condition effect of the adaptation. TPE was significantly greater in the asymmetric condition and reported error was always in the direction of the FHC. Regardless of condition, alpha desynchronised in response to stimulation, then rebounded back toward baseline values. This pattern was accelerated and attenuated in the prefrontal and occipital regions, respectively, in the asymmetric condition. Functional connectivity networks were identified in the beta and delta frequency bands; these networks, primarily comprising frontoparietal connections, were more coherent during asymmetric stimulation. These findings suggest that the temporary vestibulo-perceptual 'neglect' induced by asymmetric vestibular stimulation may be mediated by alpha rhythms and frontoparietal attentional networks. The results presented further our understanding of brain rhythms and cortical networks involved in vestibular perception and adaptation. KEY POINTS: Whole-body asymmetric sinusoidal oscillations, which consist of hemicycles with equal amplitude but differing velocities, can induce transient 'neglect' of the slower hemicycle in the vestibular perception of healthy subjects. In this study, we aimed to elucidate EEG correlates of this 'neglect', thereby identifying a cortical role in vestibular perception and adaptation. We identified a desynchronisation-resynchronisation response in the alpha frequency band (8-14 Hz) that was accelerated in the prefrontal region and attenuated in the occipital region when exposed to asymmetric, as compared to symmetric, rotations. We additionally identified functional connectivity networks in the beta (14-30 Hz) and delta (1-4 Hz) frequency bands consisting primarily of frontoparietal connections. These results suggest a prominent role of alpha rhythms and frontoparietal attentional networks in vestibular perception and adaptation.

Keywords: EEG; adaptation; alpha frequency; asymmetric rotation; frontoparietal; vestibular perception.