Statistics of the Vestibular Input Experienced during Natural Self-Motion: Implications for Neural Processing

• Published in: The Journal of neuroscience Vol. 34; no. 24; pp. 8347 - 8357
• Main Authors: Carriot, J., Jamali, M., Chacron, M. J., Cullen, K. E.
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 11.06.2014
• Subjects: Adult; Efferent Pathways - physiology; Female; Head Movements; Humans; Male; Models, Biological; Motion; Motion Perception - physiology; Physical Stimulation; Proprioception - physiology; Psychophysics; Reflex, Vestibulo-Ocular - physiology; Spectrum Analysis; Vestibule, Labyrinth - physiology; Young Adult; natural stimuli; preneuronal processing; power law
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.0692-14.2014

It is widely believed that sensory systems are optimized for processing stimuli occurring in the natural environment. However, it remains unknown whether this principle applies to the vestibular system, which contributes to essential brain functions ranging from the most automatic reflexes to spatial perception and motor coordination. Here we quantified, for the first time, the statistics of natural vestibular inputs experienced by freely moving human subjects during typical everyday activities. Although previous studies have found that the power spectra of natural signals across sensory modalities decay as a power law (i.e., as 1/f(α)), we found that this did not apply to natural vestibular stimuli. Instead, power decreased slowly at lower and more rapidly at higher frequencies for all motion dimensions. We further establish that this unique stimulus structure is the result of active motion as well as passive biomechanical filtering occurring before any neural processing. Notably, the transition frequency (i.e., frequency at which power starts to decrease rapidly) was lower when subjects passively experienced sensory stimulation than when they actively controlled stimulation through their own movement. In contrast to signals measured at the head, the spectral content of externally generated (i.e., passive) environmental motion did follow a power law. Specifically, transformations caused by both motor control and biomechanics shape the statistics of natural vestibular stimuli before neural processing. We suggest that the unique structure of natural vestibular stimuli will have important consequences on the neural coding strategies used by this essential sensory system to represent self-motion in everyday life.