Noise and vestibular perception of passive self-motion

Abstract

Noise defined as random disturbances is ubiquitous in both the external environment and the nervous system. Depending on the context, noise can degrade or improve information processing and performance. In all cases, it contributes to neural systems dynamics. We review some effects of various sources of noise on the neural processing of self-motion signals at different stages of the vestibular pathways and the resulting perceptual responses. Hair cells in the inner ear reduce the impact of noise by means of mechanical and neural filtering. Hair cells synapse on regular and irregular afferents. Variability of discharge (noise) is low in regular afferents and high in irregular units. The high variability of irregular units provides information about the envelope of naturalistic head motion stimuli. A subset of neurons in the vestibular nuclei and thalamus are optimally tuned to noisy motion stimuli that reproduce the statistics of naturalistic head movements. In the thalamus, variability of neural discharge increases with increasing motion amplitude but saturates at high amplitudes, accounting for behavioral violation of Weber’s law. In general, the precision of individual vestibular neurons in encoding head motion is worse than the perceptual precision measured behaviorally. However, the global precision predicted by neural population codes matches the high behavioral precision. The latter is estimated by means of psychometric functions for detection or discrimination of whole-body displacements. Vestibular motion thresholds (inverse of precision) reflect the contribution of intrinsic and extrinsic noise to perception. Vestibular motion thresholds tend to deteriorate progressively after the age of 40 years, possibly due to oxidative stress resulting from high discharge rates and metabolic loads of vestibular afferents. In the elderly, vestibular thresholds correlate with postural stability: the higher the threshold, the greater is the postural imbalance and risk of falling. Experimental application of optimal levels of either galvanic noise or whole-body oscillations can ameliorate vestibular function with a mechanism reminiscent of stochastic resonance. Assessment of vestibular thresholds is diagnostic in several types of vestibulopathies, and vestibular stimulation might be useful in vestibular rehabilitation.

Head-centric computing for vestibular stimulation under head-free conditions

“…Our approach lends itself to vestibular tests that require head-free conditions, either because head-restraints are not recommended or because the test involves voluntary or reflex head movements during the platform motion stimuli. Head-free testing is especially relevant in the light of the growing interest in the exploration of the vestibular function under ecological conditions ( Carriot et al, 2014 ; Diaz-Artiles and Karmali, 2021 ; La Scaleia et al, 2023 ; Lacquaniti et al, 2023 ). Indeed, it is now known that the vestibular system performs best when faced with naturalistic inputs, such as those encountered during head-free conditions ( Cullen, 2019 ; Carriot et al, 2022 ; Sinnott et al, 2023 ).…”

“…These methods range from galvanic or caloric vestibular stimulation to passive full-body accelerations. These last methods allow more naturalistic vestibular stimulation to the extent that they simulate the conditions of everyday life ( Lacquaniti et al, 2023 ). Since other sources of sensory information in addition to the vestibular ones potentially contribute to passive self-motion perception, appropriate measures are generally taken to minimize non-vestibular cues, for instance by masking visual and auditory cues and by minimizing somatosensory cues.…”