Natural statistics of human head orientation constrain models of vestibular processing

Abstract

Head orientation relative to gravity determines how gravity-dependent environmental structure is sampled by the visual system, as well as how gravity itself is sampled by the vestibular system. Therefore, both visual and vestibular sensory processing should be shaped by the statistics of head orientation relative to gravity. Here we report the statistics of human head orientation during unconstrained natural activities in humans for the first time, and we explore implications for models of vestibular processing. We find that the distribution of head pitch is more variable than head roll and that the head pitch distribution is asymmetrical with an over-representation of downward head pitch, consistent with ground-looking behavior. We further suggest that pitch and roll distributions can be used as empirical priors in a Bayesian framework to explain previously measured biases in perception of both roll and pitch. Gravitational and inertial acceleration stimulate the otoliths in an equivalent manner, so we also analyze the dynamics of human head orientation to better understand how knowledge of these dynamics can constrain solutions to the problem of gravitoinertial ambiguity. Gravitational acceleration dominates at low frequencies and inertial acceleration dominates at higher frequencies. The change in relative power of gravitational and inertial components as a function of frequency places empirical constraints on dynamic models of vestibular processing, including both frequency segregation and probabilistic internal model accounts. We conclude with a discussion of methodological considerations and scientific and applied domains that will benefit from continued measurement and analysis of natural head movements moving forward.