Post-lesional plasticity in the central nervous system of the guinea-pig: a "top-down" adaptation process?

Vestibular compensation for the postural and oculomotor deficits following unilateral labyrinthectomy is a model of functional plasticity in the brain of adult vertebrates. The mechanisms involved in this recovery are still controversial. The post-lesional lack of vestibular input might be compensated by changes in the efficacy of the remaining sensory inputs involved in gaze and posture stabilization. However, the compensation process could also rapidly become independent of these external cues, and thus be detectable in vitro in preparations obtained from lesioned animals. In agreement with this hypothesis, we have shown recently that prominent traces of the compensation process appeared three days after the lesion on in vitro isolated brains taken from labyrinthectomized guinea-pigs, where the connectivity of the central vestibular-related networks is preserved. We report here that, one week after the lesion, a slight increase in the intrinsic, spontaneous activity of the deafferented, central vestibular neurons was found in brainstem slices. This increase became stronger in slices taken after one month of compensation, and was associated at this stage with a significant decrease in the intrinsic activity of the vestibular neurons on the contralesional side. Vestibular compensation could thus follow a "top-down" strategy: it would first rely on the external cues given by the intact sensory systems, then on an internal reorganization of the vestibular-related networks, and finally on changes in the intrinsic properties of the vestibular neurons themselves. Similar strategies may be used by the mammalian brain to compensate for other types of deafferentations or environmental changes.