Hypothesis for shared central processing of canal and otolith signals

A common goal of the translational vestibuloocular reflex (TVOR) and the rotational vestibuloocular reflex (RVOR) is to stabilize visual targets on the retinae during head movement. However, these reflexes differ significantly in their dynamic characteristics at both sensory and motor levels, implying a requirement for different central processing of canal and otolith signals. Semicircular canal afferents carry a signal proportional to angular head velocity, whereas primary otolith afferents modulate approximately in phase with linear head acceleration. Behaviorally, the RVOR exhibits a robust response down to approximately 0.01 Hz, yet the TVOR is only significant above approximately 0.5 Hz. Several hypotheses were proposed to address central processing in the TVOR pathways. All rely on a central filtering process that precedes a "neural integrator" shared with the RVOR. We propose an alternative hypothesis for the convergence of canal and otolith signals that does not impose the requirement for additional low-pass filters for the TVOR. The approach is demonstrated using an anatomically based, simple model structure that reproduces the general dynamic characteristics of the RVOR and TVOR at both ocular and central levels. Differential dynamic processing of otolith and canal signals is achieved by virtue of the location at which sensory information enters a shared but distributed neural integrator. As a result, only the RVOR is provided with compensation for the eye plant. Hence canal and otolith signals share a common central integrator, as in previous hypotheses. However, we propose that the required additional filtering of otolith signals is provided by the eye plant.