NEURONAL-ACTIVITY IN THE VESTIBULAR NUCLEI AFTER CONTRALATERAL OR BILATERAL LABYRINTHECTOMY IN THE ALERT GUINEA-PIG

In the guinea pig, a unilateral labyrinthectomy is followed by an init ial depression and a subsequent restoration of the spontaneous activit y in the neurons of the ipsilateral vestibular nuclei. In two previous works, we have established the time course of these changes in the al ert guinea pig using electrical stimulation as a search stimulus to se lect the analyzed neurons. The latter criterion was important to captu re the many ipsilateral neurons that are silent at rest during the imm ediate postlabyrinthectomy stage. Because it is known that a pathway o riginating from the vestibular nuclei on one side crosses the midline and functionally inhibits the activity of the vestibular nuclei on the other side, we investigated in the first part of this study the spiki ng behavior of the neurons in the vestibular nuclei contralateral to t he labyrinthectomy using the same procedure as that used for the ipsil ateral neurons. The spiking behavior of 976 neurons was studied during 4-h recording sessions in intact animals and 1 h, 1 day, 2 days, or 1 wk postlabyrinthectomy. Neurons selected according to the electrical activation criterion were classified further as type I (their firing r ate increased during ipsilateral rotation), type LI (their firing rate increased during contralateral rotation), or unresponsive. The restin g activity of type I neurons, which was 38.1 +/- 20.9 spikes/s (mean /-: SD) in the control state, increased statistically significantly 1 h after the lesion (53.3 +/- 29.1 spikes/s) and remained at this level 1 wk later (56.0 +/- 20.3 spikes/s). The sensitivity of type I units, which was 0.80 +/- 0.46 spikes/s per deg/s in the control population, decreased to 0.49 +/- 0.26 spikes/s per deg/s 1 h after the lesion an d remained at this level 1 wk later(0.50 +/- 0.39 spikes/s per deg/s). When all monosynaptically activated neurons (type I, type II, unrespo nsive) were pooled, the sensitivity to horizontal rotation fell from 0 .58 +/-: 0.51 spikes/s per deg/s in the control state to 0.15 +/- 0.25 spikes/s per deg/s 1 h after the lesion and to 0.20 +/- 0.32 spikes/s per deg/s 1 wk later. The major findings of the first part of this st udy in the alert guinea pig are thus in accord with those of Curthoys et al. and Smith and Curthoys in anesthetized guinea pigs. In the seco nd part of this work, we studied the spiking behavior of the neurons i n the vestibular nuclei after bilateral labyrinthectomy. After unilate ral labyrinthectomy, the resting discharge of the ipsilateral monosyna ptically activated vestibular neurons fell from 36.9 +/- 21 spikes/s ( basal activity) to 6.7 +/- 17.0 spikes/s 1 h after the lesion and then recovered, reaching 17.4 +/- 18.9 and 40.8 +/- 23.7 spikes/s 1 day an d 1 wk after the lesion, respectively. These observations raise the tw o following questions. What are the relative contributions of the loss of the excitatory influence from the ipsilateral labyrinth (destroyed ) and of the persistence of the inhibitory influence from the contrala teral labyrinth (intact) in the labyrinthectomy-induced depression of activity? And are the left-right asymmetries caused by a unilateral la byrinthectomy the driving force for restoration of activity? Here, we addressed these two questions by studying the spiking behavior of 473 second-order vestibular neurons in the alert guinea pig after a bilate ral labyrinthectomy. In the acute stage, 1 h after bilateral labyrinth ectomy, the resting discharge of the second-order vestibular neurons w as 16.2 +/- 22.4 spikes/s. From comparison with the results obtained i n the acute stage after a unilateral labyrinthectomy, we inferred that the ipsilateral excitatory influence was between two and three times more powerful than the contralateral inhibitory influence. After bilat eral labyrinthectomy as well as after unilateral labyrinthectomy, the resting activity of the second-order vestibular neurons returned to no rmal, reaching 20.8 +/- 23.1 spikes/s 1 day after the lesion and 38.6 +/- 21.1 spikes/s 1 wk after the lesion. From this fact, we concluded that the left-right asymmetries caused by a unilateral labyrinthectomy were not the error signals inducing the restoration of activity.