Aberrant three-dimensional estimates of head motion and orientation are generated by the brain when the vestibular...

Vertigo, defined as an abnormal perception of motion, is debilitating for millions of people, but the underlying mechanisms are not fully understood. It often arises from changes in the peripheral vestibular organs, which sense three-dimensional angular rotation, translational acceleration, and gravity. Researchers have predicted the characteristics of these complex misperceptions based solely on peripheral vestibular physiology and anatomy, but surprisingly, the actual misperceptions of motion and orientation in patients are different from these predictions. It has therefore been suggested that processing of aberrant vestibular inputs in the brain may be responsible for introducing additional complexity. We studied how central interactions between otolithic gravity cues and erroneous semicircular canal cues caused by unilateral peripheral vestibular loss of function could result in three-dimensional misestimates of head rotation, translation, and tilt relative to gravity. Our broad hypothesis is that vertigo arises from an interaction between abnormal peripheral vestibular signals and central processing that includes internal models of physical relationships. We studied this hypothesis using a computational model of central processing. The model predicted misestimates of tilt, translation, and rotation that depended on head orientation. Specifically, estimates of translation were the largest and rotations were the smallest when the abnormal canal input was about an axis perpendicular to gravitational cues, and the opposite was observed when conflict was minimal. These predictions match head-orientation-dependent vertigo and nystagmus in patients with unilateral loss of function. Our results, therefore, provide a quantitative approach to understanding central vestibular processing and the clinical symptoms it generates with peripheral dysfunction.