title: The increased sensitivity of irregular peripheral canal and otolith vestibular afferents optimizes their encoding of natural stimuli.
abstract: Efficient processing of incoming sensory input is essential for an organism's survival. A growing body of evidence suggests that sensory systems have developed coding strategies that are constrained by the statistics of the natural environment. Consequently, it is necessary to first characterize neural responses to natural stimuli to uncover the coding strategies used by a given sensory system. Here we report for the first time the statistics of vestibular rotational and translational stimuli experienced by rhesus monkeys during natural (e.g., walking, grooming) behaviors. We find that these stimuli can reach intensities as high as 1500 deg/s and 8 G. Recordings from afferents during naturalistic rotational and linear motion further revealed strongly nonlinear responses in the form of rectification and saturation, which could not be accurately predicted by traditional linear models of vestibular processing. Accordingly, we used linear-nonlinear cascade models and found that these could accurately predict responses to naturalistic stimuli. Finally, we tested whether the statistics of natural vestibular signals constrain the neural coding strategies used by peripheral afferents. We found that both irregular otolith and semicircular canal afferents, because of their higher sensitivities, were more optimized for processing natural vestibular stimuli as compared with their regular counterparts. Our results therefore provide the first evidence supporting the hypothesis that the neural coding strategies used by the vestibular system are matched to the statistics of natural stimuli.
authors: Department Physics and.
authors: Adam D
authors: AD
authors: Schneider
authors: Department Physiology, McGill University, Montreal, Quebec, H3A 0G4, Canada.
authors: Mohsen
authors: M
authors: Jamali
authors: Department Physiology, McGill University, Montreal, Quebec, H3A 0G4, Canada.
authors: Jerome
authors: J
authors: Carriot
authors: Department Physics and Department Physiology, McGill University, Montreal, Quebec, H3A 0G4, Canada.
authors: Maurice J
authors: http://orcid.org/0000-0002-3032-452X
authors: MJ
authors: Chacron
authors: Department Physiology, McGill University, Montreal, Quebec, H3A 0G4, Canada kathleen.cullen@mcgill.ca.
authors: Kathleen E
authors: http://orcid.org/0000-0002-9348-0933
authors: KE
authors: Cullen
mesh_terms: D000200:Action Potentials / Q000502:physiology; D000818:Animals; D001306:Auditory Pathways / Q000502:physiology*; D006112:Gravitation; D019416:Head Movements / Q000502:physiology*; D016014:Linear Models; D008252:Macaca fascicularis; D008297:Male; D016011:Normal Distribution; D010037:Otolithic Membrane / Q000502:physiology*; D012399:Rotation; D014722:Vestibule, Labyrinth / Q000502:physiology*
keywords: natural stimuli; optimal coding; sensitivity; vestibular afferent