Gravito-inertial ambiguity resolved through head stabilization

It has been frequently observed that humans and animals spontaneously stabilize their heads with respect to the gravitational vertical during body movements even in the absence of vision. The interpretations of this intriguing behaviour have so far not included the need, for survival, to robustly estimate verticality. Here we use a mechanistic model of the head/otolith organ to analyse the possibility for this system to render verticality 'observable', a fundamental prerequisite to the determination of the angular position and acceleration of the head from idiothetic, inertial measurements. The intrinsically nonlinear head-vestibular dynamics is shown to generally lack observability unless the head is stabilized in orientation by feedback. Thus, our study supports the hypothesis that a central function of the physiologically costly head stabilization strategy is to enable an organism to estimate the gravitational vertical and head acceleration during locomotion. Moreover, our result exhibits a rare peculiarity of certain nonlinear systems to fortuitously alter their observability properties when feedback is applied.