Vestibular Perception and Action Employ Qualitatively Different Mechanisms: I

Acknowledgments: Authors thank Tom Bennett and Valerie Stallings for their technical contributions, Margaret Marsden and Patty Cunningham for their administrative assistance, and Drs. Lionel Zupan and Rick Lewis for commenting on early versions of the manuscript. Experiments were performed at the Legacy Neurotology Research Laboratory. ABSTRACT To investigate the neural mechanisms that humans use to process the ambiguous force measured by the otolith organs, we measured vestibulo-ocular reflexes (VORs) and perceptions of tilt and translation. One primary goal was to determine if the same, or different, mechanisms contribute to vestibular perception and action. We used motion paradigms that provided identical sinusoidal inter-aural otolith cues across a broad frequency range. We accomplished this by sinusoidally tilting (20˚, 0.005-0.7 Hz) subjects in roll about an earth-horizontal, head-centered, rotation axis (" Tilt ") or sinusoidally accelerating (3.3 m/s 2 , 0.005-0.7 Hz) subjects along their inter-aural axis (" Translation "). While identical inter-aural otolith cues were provided by these motion paradigms, the canal cues were substantially different, since roll rotations were present during Tilt but not during Translation. We found that perception was dependent on canal cues, since the reported perceptions of both roll tilt and inter-aural translation were substantially different during Translation and Tilt. These findings match internal model predictions that rotational cues from the canals influence the neural processing of otolith cues. We also found horizontal translational VORs at frequencies above 0.2 Hz during both Translation and Tilt. These responses were dependent on otolith cues and match simple filtering predictions that translational VORs include contributions via simple high-pass filtering of otolith cues. More generally, these findings demonstrate that internal models govern human vestibular " perception " across a broad range of frequencies and that simple high-pass filters contribute to human horizontal translational VORs (" action ") at frequencies above about 0.2 Hz.