Visual-vestibular interactions during vestibular compensation: role of the pretectal not in horizontal VOR recovery after hemilabyrinthectomy in rhesus monkey

Abstract

Damage to the vestibular labyrinth leads to profound nystagmus and vertigo. Over time, the vestibular-ocular system recovers in a process called vestibular compensation leading to reduced nystagmus and vertigo provided visual signals are available. Our study was directed at identifying sources of visual information that could play a role in vestibular compensation. Specifically, we investigated the role of the pretectal nucleus of the optic tract (NOT) in vestibular compensation after hemilabyrinthectomy (HL) in rhesus monkeys. We chose the NOT because this structure provides critical visual motion information for adaptive modification of the vestibular ocular reflex (VOR). We produced bilateral NOT lesions by injecting the excitotoxin ibotenic acid. We compared vestibular compensation after HL in NOT-lesioned and control animals with intact NOTs. We measured eye movements with an electromagnetic method employing scleral search coils. Measurements included slow-phase eye velocity during spontaneous nystagmus, per- and postrotatory nystagmus and the horizontal VOR (hVOR) gain (eye-velocity/head velocity) associated with per- and postrotatory and sinusoidal (0.2-2.0 Hz; 30-90 degrees/s) whole body oscillation around the earth-vertical axis. VOR gain was low (<0.5) for rotation toward the HL side. Our control animal evinced significant vestibular compensation with VOR gains approaching unity by 100 days post HL. In contrast, monkeys with bilateral lesions of the NOT never obtained this significant recovery with hVOR gains well below unity at 100 days and beyond. Therefore our studies demonstrate that the NOT is an essential source of visual signals for the process of vestibular compensation after HL.