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

Bilateral otolith contribution to spatial coding in the vestibular system.

Recent work on the coding of spatial information in central otolith neurons has significantly advanced our knowledge of signal transformation from head-fixed otolith coordinates to space-centered coordinates during motion. In this review, emphasis is placed on the neural mechanisms by which signals generated at the bilateral labyrinths are recognized as gravity-dependent spatial information and in turn as substrate for otolithic reflexes. We first focus on the spatiotemporal neuronal response patterns (i.e. one- and two-dimensional neurons) to pure otolith stimulation, as assessed by single unit recording from the vestibular nucleus in labyrinth-intact animals. These spatiotemporal features are also analyzed in association with other electrophysiological properties to evaluate their role in the central construction of a spatial frame of reference in the otolith system. Data derived from animals with elimination of inputs from one labyrinth then provide evidence that during vestibular stimulation signals arising from a single utricle are operative at the level of both the ipsilateral and contralateral vestibular nuclei. Hemilabyrinthectomy also revealed neural asymmetries in spontaneous activity, response dynamics and spatial coding behavior between neuronal subpopulations on the two sides and as a result suggested a segregation of otolith signals reaching the ipsilateral and contralateral vestibular nuclei. Recent studies have confirmed and extended previous observations that the recovery of resting activity within the vestibular nuclear complex during vestibular compensation is related to changes in both intrinsic membrane properties and capacities to respond to extracellular factors. The bilateral imbalance provides the basis for deranged spatial coding and motor deficits accompanying hemilabyrinthectomy. Taken together, these experimental findings indicate that in the normal state converging inputs from bilateral vestibular labyrinths are essential to spatiotemporal signal transformation at the central otolith neurons during low-frequency head movements. Copyright 2002 National Science Council, ROC and S. Karger AG, Basellink_to_subscribed_fulltex