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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.

This review considers whether the vestibular system includes separate populations of sensory axons innervating individual organs and giving rise to distinct central pathways. There is a variability in the discharge properties of afferents supplying each organ. Discharge regularity provides a marker for this diversity since fibers which differ in this way also differ in many other properties. Postspike recovery of excitability determines the discharge regularity of an afferent and its sensitivity to depolarizing inputs. Sensitivity is small in regularly discharging afferents and large in irregularly discharging afferents. The enhanced sensitivity of irregular fibers explains their larger responses to sensory inputs, to efferent activation, and to externally applied galvanic currents, but not their distinctive response dynamics. Morphophysiological studies show that regular and irregular afferents innervate overlapping regions of the vestibular nuclei. Intracellular recordings of EPSPs reveal that some secondary vestibular neurons receive a restricted input from regular or irregular afferents, but that most such neurons receive a mixed input from both kinds of afferents. Anodal currents delivered to the labyrinth can result in a selective and reversible silencing of irregular afferents. Such a functional ablation can provide estimates of the relative contributions of regular and irregular inputs to a central neuron's discharge. From such estimates it is concluded that secondary neurons need not resemble their afferent inputs in discharge regularity or response dynamics. Several suggestions are made as to the potentially distinctive contributions made by regular and irregular afferents: (1) Reflecting their response dynamics, regular and irregular afferents could compensate for differences in the dynamic loads of various reflexes or of individual reflexes in different parts of their frequency range; (2) The gating of irregular inputs to secondary VOR neurons could modify the operation of reflexes under varying behavioral circumstances; (3) Two-dimensional sensitivity can arise from the convergence onto secondary neurons of otolith inputs differing in their directional properties and response dynamics; (4) Calyx afferents have relatively low gains when compared with irregular dimorphic afferents. This could serve to expand the stimulus range over which the response of calyx afferents remains linear, while at the same time preserving the other features peculiar to irregular afferents. Among those features are phasic response dynamics and large responses to efferent activation; (5) Because of the convergence of several afferents onto each secondary neuron, information transmission to the latter depends on the gain of individual afferents, but not on their discharge regularity.

1. The response to static tilts was studied in peripheral otolith neurons in the barbiturate-anesthetized squirrel monkey (Saimiri sciureus). Each unit was characterized by a functional polarization vector, which defines the axis of greatest sensitivity. A circumstantial criterion was used to assign units to the inferior (IN) or superior (SN) vestibular nerves. The former neurons should innervate the sacculus, the latter mainly the utriculus. Confirming pasting experiments, the polarization vectors for SN units lay near the plane of the utricular macula, those for IN units near the plane of the saccular macula. The polarization vectors for IN units were compared in two groups of animals. In one group, the vestibular nerve was intact; in the other, the superior nerve was sectioned. No differences were found and this, together with other observations, demonstrate that the sacculas in mammals functions mainly (if not solely) as an equilibrium organ. 2. The resting discharge of otolith neurons averages some 60 spikes/s, the sensitivity some 30-40 spikes/s-g. IN units tend to have slightly lower sensitivities than do SN units. IN units with upwardly directed (+Z) vectors have substantially higher resting discharges than do units with downwardly directed (-Z) vectors. The +Z units are also characterized by more linear force-response relations. 3. There is a strong positive relation between the resting discharge and sensitivity of units characterized by regular steady-state discharge patterns. A weaker, but statistically significant, relation is demonstrable for irregular units. It is suggested that the relation seen in regular units is the result of the neurons differing from one anothrer in terms of a receptor bias, a transduction gain, or both. Only the mechanism based on transduction gain is thought to be operative among the population of irregular units. 4. Centrifugal-force trapezoids were used to study the response adaptation to prolonged stimulation. Adaptation was more conspicious in irregular units and was characterized by perstimulus response declines and poststimulus secondary responses. For regular units, adaptive properties were similar during excitatory and inhibitory responses. For irregular units, response declines were larger during excitatory stimuli, secondary responses larger following inhibitory stimuli. Typically, response declines were most rapid at the start of the force plateau. A few units, all of them irregular, exhibited a delayed adaptation with response declines beginning only after a constant force had been maintained for 10-20 s. 5. Excitatory responses of regular units are almost always larger than inhibitory responses. This is so during both the dynamic and static portions of force trapezoids. A similar asymmetry is seen in the dynamic response of irregular units; static response asymmetries of the latter units are more variable.

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