Plastic changes underlying vestibular compensation in the guinea-pig persist in isolated, in vitro whole brain preparations

Vestibular compensation for the postural and oculomotor deficits induced by unilateral labyrinthectomy is a model of post-lesional plasticity in the c entral nervous system. Just after the removal of one labyrinth, the deaffer ented, ipsilateral vestibular nucleus neurons are almost silent, and the di scharge of the contralateral vestibular nucleus neurons is increased. The a ssociated static disorders disappear in a few days, as normal activity is r estored in both vestibular nuclei. In this study, we searched for traces of vestibular compensation in isolated whole brains taken from adult guinea-p igs. The electrophysiological responses evoked in control brains were compa red to those evoked in brains taken from animals that had previously been l abyrinthectomized. Guineapigs compensated for an initial labyrinthectomy wi thin three days, in vivo, subsequent deafferentation of vestibular nucleus neurons on the intact side triggered "Bechterew's phenomenon": a new postur al and oculomotor syndrome appeared, similar to the one induced by the firs t lesion, but directed to the newly deafferented side. These disturbances w ould be caused by the new imbalance between the discharges of neurons in th e two vestibular nuclei triggered by the second deafferentation. Experiment s were designed to search for a similar imbalance in vitro in brains taken from labyrinthectomized animals, where the intact vestibular nerve is cut d uring the dissection. Isolated whole brains were obtained from young guinea -pigs at various times (one to seven days) following an initial labyrinthec tomy. An imbalance between the resting activities of medial vestibular nucl eus neurons on both sides of the brainstem was revealed in brains taken mor e chan three days after the lesion: their discharge was higher on the compe nsated, initially lesioned side than on the newly deafferented side. In som e cases, an oscillatory pattern of discharge, reminiscent of the spontaneou s nystagmus associated in vivo with Bechterew's syndrome, appeared in both abducens nerves. These data demonstrate that most of the changes underlying vestibular compensation persist, and can thus be investigated in the isola ted whole brain preparation. Brains removed only one day after the lesion displayed normal commissural r esponses and symmetric spinal inputs to vestibular nucleus neurons. However , an unusually large proportion of the neurons recorded on both sides of th e preparation had very irregular spontaneous discharge rates. These data su ggest that the first stages of vestibular compensation might be associated with transient changes in the membrane properties of vestibular nucleus neu rons. Brains taken from compensated animals displayed a significant, bilate ral decrease of the inhibitory commissural responses evoked in the medial v estibular nucleus by single-shock. stimulation of the contralateral vestibu lar nerve. The sensitivity of abducens motoneurons on the initially lesione d, compensated side to synaptic activation from the contralesional vestibul ar nucleus neurons was also decreased. Both changes may explain the long-te rm, bilateral decrease of vestibular-related reflexes observed following un ilateral labyrinthectomy. Spinal inputs to vestibular nucleus neurons becam e progressively asymmetric: their efficacy was increased on the lesioned si de and decreased on the intact one. This last modification may support a fu nctional substitution of the deficient, vestibular-related synergies involv ed in gaze and posture stabilization by neck-related reflexes. (C) 1999 IBR O. Published by Elsevier Science Ltd.