Efferent-mediated fluctuations in vestibular nerve discharge: a novel, positive-feedback mechanism of efferent control.

We compared the background discharge of vestibular nerve afferents in barbiturate-anesthetized and unanesthetized, decerebrate chinchillas. Based on their interspike-interval statistics, units were categorized as regular, intermediate, or irregular. Background discharge rates were higher in irregular units from decerebrates compared to anesthetized preparations; no such difference was observed for regular or intermediate units. Large fluctuations in discharge rate were confined to intermediate and irregular units in decerebrates, but were not seen at all in anesthetized animals. The most prominent examples of fluctuations consisted of oscillations with periods exceeding 500 s and peak-to-peak amplitudes as large as 300 spikes/s. Several observations show that the fluctuations are mediated by the efferent vestibular system (EVS): (1) they are abolished when the vestibular nerve is cut proximal to the recording electrode; (2) their amplitude is correlated with the size of efferent-mediated rotational responses in individual units; and (3) they occur even when vital signs are stable. Previous studies had provided evidence that the EVS involves positive feedback: vestibular nerve afferents and EVS neurons excite one another. To study how oscillations could be produced, we developed a nonlinear model of positive feedback in which afferent feed-forward discharge was nonlinearly related to its inputs from hair cells and the EVS, while these inputs declined (adapted) as discharge was prolonged. Provided that the gain of the efferent feedback loop was sufficiently large, the model showed oscillations similar to those observed experimentally. Although large fluctuations in afferent discharge are unlikely to occur under physiological circumstances, positive feedback may be a normal feature that can amplify the influence of the EVS.