The recovery of static vestibular function following peripheral vestibular lesions in mammals: the intrinsic mechanism hypothesis.

This theoretical paper describes the "intrinsic mechanism hypothesis," a new hypothesis of vestibular compensation, the behavioral recovery that follows unilateral deafferentation of the vestibular labyrinth (UVD). The most salient characteristic of vestibular compensation is the decrease in the severity of the static ocular motor and postural symptoms that follow UVD, associated with a recovery of resting activity in the ipsilateral vestibular nucleus complex (VNC). The speed of static compensation in some mammalian species (for example, cat) has suggested that reactive synaptogenesis is an unlikely explanation because it is too slow. Other, more rapid mechanisms, such as denervation supersensitivity, receptor-up-regulation, or increased neurotransmitter release, were reasonable possibilities. However, to date, each study that has addressed these possibilities has failed to find any change that could account for the recovery of VNC resting activity. The search for such "substitutive" mechanisms was based on the hypothesis that something other than the VNC neurons themselves would have to "replace" the missing resting activity that the ipsilateral vestibular nerve normally provides. However, brainstem slice studies demonstrate that, at least in vitro, VNC neurons do not need the vestibular nerve in order to generate resting activity. On the basis of these and other considerations, we suggest that following a brief calcium-induced diaschisis, VNC neurons ipsilateral to the UVD reactivate the intrinsic membrane properties that normally contribute to their resting activity in vivo, and that this recovery of resting activity accounts for static vestibular compensation.