Envelope statistics of self-motion signals experienced by human subjects during everyday activities: Implications for vestibular processing

• Published in: PloS one Vol. 12; no. 6; p. e0178664
• Main Authors: Carriot, Jérome, Jamali, Mohsen, Cullen, Kathleen E., Chacron, Maurice J.
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 02.06.2017; Public Library of Science (PLoS)
• Subjects: Activities of Daily Living; Adaptation; Adult; Afferent Pathways - physiology; Analysis; Biology and Life Sciences; Brain; Coding; Constraints; Deviation; Engineering and Technology; Envelopes; External stimuli; Female; Filtration; Head Movements - physiology; Human body; Human motion; Human subjects; Humans; Invariance; Male; Mathematical models; Models, Neurological; Motion Perception - physiology; Motion sickness; Movement - physiology; Neural coding; Neurons; Neurosciences; Physical Sciences; Physiology; Power law; Proprioception - physiology; Rotation; Scale invariance; Signal processing; Spectra; Spectrum Analysis; Statistics; Statistics (Data); Stimuli; Studies; Temporal variations; Translation; Translations; Variance; Velocity; Vestibular system; Young Adult; United States; Canada; Montreal Quebec Canada
• DOI: 10.1371/journal.pone.0178664
• ISSN: 1932-6203

There is accumulating evidence that the brain's neural coding strategies are constrained by natural stimulus statistics. Here we investigated the statistics of the time varying envelope (i.e. a second-order stimulus attribute that is related to variance) of rotational and translational self-motion signals experienced by human subjects during everyday activities. We found that envelopes can reach large values across all six motion dimensions (~450 deg/s for rotations and ~4 G for translations). Unlike results obtained in other sensory modalities, the spectral power of envelope signals decreased slowly for low (< 2 Hz) and more sharply for high (>2 Hz) temporal frequencies and thus was not well-fit by a power law. We next compared the spectral properties of envelope signals resulting from active and passive self-motion, as well as those resulting from signals obtained when the subject is absent (i.e. external stimuli). Our data suggest that different mechanisms underlie deviation from scale invariance in rotational and translational self-motion envelopes. Specifically, active self-motion and filtering by the human body cause deviation from scale invariance primarily for translational and rotational envelope signals, respectively. Finally, we used well-established models in order to predict the responses of peripheral vestibular afferents to natural envelope stimuli. We found that irregular afferents responded more strongly to envelopes than their regular counterparts. Our findings have important consequences for understanding the coding strategies used by the vestibular system to process natural second-order self-motion signals.