Bilateral Vestibular Loss Leads to Active Destabilization of Balance During Voluntary Head Turns in the Standing Cat

Abstract

The purpose of this study was to determine the source of postural instability in labyrinthectomized cats during lateral head turns. Cats were trained to maintain the head in a forward orientation and then perform a rapid, large-amplitude head turn to left or right in yaw, while standing freely on a force platform. Head turns were biomechanically complex with the primary movement in the yaw plane accompanied by an ipsilateral ear-down roll and nose-down pitch. Cats used a strategy of pushing off by activating extensors of the contralateral forelimb while using all four limbs to produce a rotational moment of force about the vertical axis. After bilateral labyrinthectomy, the initial components of the head turn and accompanying postural responses were hypermetric, but otherwise similar to those produced before the lesion. However, near the time of peak yaw velocity, the lesioned cats produced an unexpected burst in extensors of the contralateral limbs that thrust the body to the ipsilateral side, leading to falls. This postural error was in the frontal (roll) plane, even though the primary movement was a rotation in the horizontal (yaw) plane. The response error decreased in amplitude with compensation but did not disappear. We conclude that lack of vestibular input results in active destabilization of balance during voluntary head movement. We postulate that the postural imbalance arises from the misperception that the trunk was rolling contralaterally, based on signals from neck proprioceptors in the absence of vestibular inputs.