VISUAL SENSORY SUBSTITUTION IN VESTIBULAR COMPENSATION - NEURONAL SUBSTRATES IN THE ALERT CAT

The purpose of this study was to investigate adaptive changes in the a ctivity of vestibular nuclei neurons unilaterally deprived of their pr imary afferent inputs when influenced by visual motion cues. These neu ronal changes might account for the established role that vision plays in the compensation for posture-kinetic deficits after the loss of ve stibular inputs. Neuronal recordings were made in alert, non-paralysed cats that had undergone unilateral vestibular nerve sections. The uni t responses collected in both Deiters' nuclei were compared to those p reviously recorded in intact cats. We analysed the extracellular activ ity of Deiters' nucleus neurons, as well as the optokinetic reflex (OK R) evoked during sinusoidal translation of a whole-field optokinetic s timulus in the vertical plane. In intact cats, we found the unit firin g rate closely correlated with the visual surround translation velocit y, and the relationship between the discharge rate and the motion freq uency was tuned around an optimal frequency. The maxi mum firing rate modulation was generally below the 0.25 Hz stimulus frequency; unit re sponses were weak or even absent above 0.25 Hz. From the 4th day to th e end of the 3rd week after ipsilateral deafferentation, a majority of cells was found to display maximum discharge modulation during vertic al visual stimulation at 0.50 Hz, and even at 0.75 Hz, indicating that the frequency bandwidth of the visually induced responses of deaffere nted vestibular nuclei neurons had been extended. Consequently, the fr equency-dependent attenuation in the sensitivity of vestibular neurons to visual inputs was much less pronounced. After the first 3 weeks po stlesion, the unit response characteristics were very similar to those observed prior to the deafferentation. On the nucleus contralateral t o the neurectomy, the maximum modulation of most cells was tuned to th e low frequencies of optokinetic stimulation, as also seen prior to th e lesion. We found, however, a subgroup of cells displaying well-devel oped responses above 0.50 Hz. Under all experimental conditions, the n euronal response phase still remained closely correlated with the moti on velocity of the vertical sinusoidal visual pattern. We hypothesize that Deiters' neurons deprived of their primary afferents may transien tly acquire the ability to code fast head movements on the basis of vi sual messages, thus compensating, at least partially, for the loss of dynamic vestibular inputs during the early stages of the recovery proc ess. Since the overall vertical OKR gain was not significantly altered within the 0.0125 Hz-1 Hz range of stimulation after the unilateral n eurectomy, it can be postulated that the increased sensitivity of deaf ferented vestibular neurons to visual motion cues was accounted for by plasticity mechanisms operating within the deafferented Deiters' nucl eus. The neuroplasticity mechanisms underlying this rapid and temporar y increase in neuronal sensitivity are discussed.