DISSOCIATIONS BETWEEN BEHAVIORAL RECOVERY AND RESTORATION OF VESTIBULAR ACTIVITY IN THE UNILABYRINTHECTOMIZED GUINEA-PIG

1. In the guinea-pig, a unilateral labyrinthectomy induces postural di sturbances and an ocular nystagmus which abate or disappear over time. These behavioural changes are accompanied by an initial collapse and a subsequent restoration of the spontaneous activity in the neurones o f the ipsilateral vestibular nuclei. Recently, it has been shown that the vestibular neuronal activity remained collapsed over at least 10 h whereas its restoration was complete 1 week after the lesion. The aim s of this study were to determine when restoration of spontaneous acti vity in the partially deafferented vestibular neurones started and to compare the time courses of the behavioural and neuronal recoveries in guinea-pigs that had undergone a unilateral labyrinthectomy. 2. Neuro nal discharge measurements were made using chronic extracellular recor ding of single unit activity. After a left labyrinthectomy, electrodes were placed on the site of the destroyed labyrinth to enable stimulat ion of the left vestibular nerve. Behavioural measurements included ch ronic recording of eye movements by the scleral search coil technique. After a left labyrinthectomy, lateral deviation of the head, twisting of the head, and eye velocity of the slow phases of the nystagmus wer e measured. 3. The neuronal activity of the rostral part of the vestib ular nuclear complex on tile lesioned side was recorded in alert guine a-pigs over 4 h recording sessions between 12 and 72 h after the lesio n. 4. The criterion used to select vestibular neurones for analysis wa s their recruitment by an electric shock on tile vestibular nerve, In addition, in order to explore a uniform population, we focused on neur ones recruited at monosynaptic latencies (0.85-1.15 ms). 5. For each r ecording period, the mean resting rate was calculated animal by animal and the grand mean of these individual resting rate means was calcula ted. Previously, a deline in the grand mean resting rate from 35.8 +/- 6.0 spikes s(-1) (control state) to 7.1 +/- 4.2 spikes s(-1) during t he first 4 h after labyrinthectomy had been shown. In the present stud y, the first sign of recovery was observed during the 12-16 h recordin g period when the resting rate grand mean increased to 16.3 +/- 3.9 sp ikes s(-1). This grand mean activity did not change significantly duri ng the following 12 h. Thereafter, restoration of neuronal activity im proved and was complete 1 week after the lesion. 6. Although the abate ment of the vestibular symptoms roughly paralleled the restoration of neuronal activity in the vestibular nuclei, some discrepancies between the time courses of both phenomena emerged. An important step in post ural recovery (the animals managed to stand up) and a major part of th e abatement of the nystagmus occurred before tile recovery of vestibul ar neuronal activity. In addition, lateral deviation of the head disap peared while restoration of the neuronal activity was incomplete, but significant head twisting was still evident when vestibular resting ra tes had recovered completely. 7. We conclude that restoration of neuro nal activity in the ipsilateral vestibular nuclei starts 12 h after th e lesion and that restoration of neuronal activity in the ipsilateral vestibular nuclei is not the only mechanism underlying behavioural ves tibular compensation.