Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey

Abstract

Most vestibular nerve afferents can be classified as regularly or irregularly discharging. Two factors are theoretically identified as being potentially responsible for differences in discharge regularity. The first, ascribable to synaptic noise, is the variance (sigma v2) characterizing the transmembrane voltage fluctuations of the axon's spike trigger site, i.e., the place where impulses normally arise. The second factor is the slope (dmuv/dt) of the trigger site's postspike recovery function. Were (dmuv/dt) a major determinant of discharge regularity, the theory predicts that the more irregular the discharge of a unit, the greater should be its sensitivity to externally applied galvanic currents and the faster should be the postspike recovery of its electrical excitability. The predictions would not hold if differences in the discharge regularity between units largely reflected variations in sigma v. To test these predictions, the responses of vestibular nerve afferents to externally applied galvanic currents were studied in the barbiturate-anesthetized squirrel monkey. Current steps of 5-s duration and short (50 microsecond) shocks were delivered by way of the perilymphatic space of the vestibule. Results were similar regardless of which end organ an afferent innervated. The regularity of discharge of each unit was expressed by a normalized coefficient of variation (CV*). The galvanic sensitivity (beta p) of a unit, measured from its response to current steps, was linearly related to discharge regularity (CV*), there being approximately 20-fold variations in both variables across the afferent population. Various geometric factors--including fiber diameter, position of individual axons within the various nerve branches, and the configuration of unmyelinated processes within the sensory epithelium--are unlikely to have made a major contribution to the positive relation between beta P and CV*. The postspike recovery of electrical excitability was measured as response thresholds to shocks, synchronized to follow naturally occurring impulses at several different delays. Recovery in irregular units was more rapid than in regular units. Evidence is presented that externally applied currents acted at the spike trigger site rather than elsewhere in the sensory transduction process. We argue that the irregular discharge of some vestibular afferents offers no functional advantage in the encoding and transmission of sensory information. Rather, the irregularity of discharge is better viewed as a consequence of the enhanced sensitivity of these units to depolarizing influences, including afferent and efferent synaptic inputs.

Efferent Actions in the Chinchilla Vestibular Labyrinth

“…Responses, averaged for a 5-s, 50-l A cathodal current, are plotted against cv* in Figure 10E. As had been found previously (Goldberg et al 1984;Baird et al 1988), galvanic sensitivity was related to cv* by a power law. The exponent, b = 0.74 ± 0.09, was nearly identical to the pooled exponent, b = 0.68 ± 0.05, for the relations between efferent response magnitude and cv* (Fig.…”

“…The similarity in exponents suggests that the same mechanisms underlie the two relations with cv*. Galvanic sensitivity reflects the sensitivity of the spike encoder in the afferent terminal (Goldberg et al 1984;Smith and Goldberg 1986) and the same may be true for efferent-response magnitude.…”

“…Studies of the responses to externally applied galvanic currents (Goldberg et al 1984(Goldberg et al , a,1990bBaird et al 1988), as well as modeling studies (Smith and Goldberg 1986), imply that encoder sensitivity is related to discharge regularity. As shown in the present study, galvanic sensitivity and efferent response magnitude grow almost identically with cv* suggesting that both reflect variations in encoder sensitivity.…”

Acoustic Clicks Activate both the Canal and Otolith Vestibulo-Ocular Reflex Pathways in Behaving Monkeys

“…This may be justified by the conservative nature of the vestibular peripheral end organs. According to Murofushi et al (1995), the minimum latency of clickevoked vestibular afferent response was 0.4 ms in guinea pigs, which was very close to the 0.33 ms minimum latency of short electric pulse-evoked vestibular afferent response in squirrel monkeys (Goldberg et al 1984). The extreme short latency is one of the most prominent features of acoustic activation of the vestibular system, but we know little about how it occurs.…”

Ionic and neuromodulatory regulation of burst discharge controls frequency tuning

“…The CV provides a measure of the variability of spike discharge in response to step depolarizations and a CV of ≅1 is indicative of random firing (Poisson process with exponentially distributed ISIs (Bair et al, 1994;Softky and Koch, 1993)), while a CV≫1 is typically associated with burst discharge (Wilbur and Rinzel, 1983), allowing this measure to serve as a sensitive burst indicator. We note that, while the CV measure is sensitive to changes in firing rate, increases/decreases in firing rate have been shown to cause a decrease/ increase in CV (Goldberg et al, 1984).…”