Extracellular recording techniques were used in the chinchilla to study the discharge properties of utricular afferents, including their discharge regularity, background discharge, and responses to both externally applied galvanic currents and centrifugal forces. A normalized coefficient of variation (CV*), independent of discharge rate, was used to classify units as regularly (CV* < 0.10), intermediate (0.10 ≤ CV* ≤ 0.20), or irregularly discharging (CV* > 0.20). In some circumstances, it was useful to recognize a group of very regularly discharging afferents (CV* < 0.05). The CV* ranged from < 0.020 to > 0.60. Regular units outnumbered irregular units by an ~3:1 ratio. The distribution of CV*s was bimodal: there was a major peak at CV* = 0.03 and a minor peak at CV* = 0.3. Background rates were measured with the head in a horizontal position. Those of regular units usually fell between 40 and 80 spikes/s (mean: 54 spikes/s); those of irregular units were more broadly distributed (mean: 47 spikes/s). Units were categorized in terms of the tilt directions resulting in increased discharge. There is a broad distribution of excitatory tilt directions with some units excited by ipsilateral rolls, others by controlateral rolls, some by nose-up pitches, and still others by nose-down pitches. In the chinchilla, there are almost equal numbers of units excited by ipsilateral or contralateral tilts. This is in contrast to previous findings in the cat and squirrel monkey, where the former units predominate by a 3:1 ratio. The difference can be related to the fact that medial zone of the macula, where units excited by ipsilateral tilts reside, makes up a smaller proportion of the sensory epithelium in the chinchilla than in the monkey. Galvanic sensitivity (β*) and discharge regularity (CV*) were related by a power law, β* = (CV*)b, with an exponent, b = 0.70. Responses to sinusoidal centrifugal forces in the frequency range, f, between DC and 2 Hz were characterized by their gains (g(f)) and phases (Φ(f)), taken with respect to peak linear force. Response linearity was studied by varying the amplitude of a 0.1-Hz sinusoid from 0.05 to 0.4 g. Nonlinear distortion was small (~10%), as was the variation of gain (±10%) and phase (±5°) with amplitude. Response dynamics vary with discharge regularity. Very regular units are tonic. Their gains are typically 50 spikes·s-1/g and almost constant (±10%) over the entire frequency range. Phases hover near zero with small (5°) phase leads at low frequencies and slightly larger (10°) phase lags at high frequencies. Irregular units are more phasic. Their gains increase -5 to 20-fold with frequency from a typical g(DC) of 25 spikes·s-1/g to a typical g(2Hz) of 250 spikes·s-1/g; phase leads of 25-40° are seen between 0.01 and 2 Hz. Gains and phases were fit by a transfer function, H = H(M)·H(V)·H(A), consisting of three terms thought to represent the mechanics of the otolithic membrane (H(M)), the transduction processes interposed between the mechanics and the postsynaptic spike encoder (H(V)), and the adaptive properties of the encoder (H(A)). H(A) has been previously measured with externally applied galvanic sine waves. It is similar for all afferents and results in a small, nearly constant phase lead between 0.01 and 2 Hz and a gain that gradually increases with frequency. H(M), which was deduced by assuming that H(V)= 1 for very regular units, introduces a gradual and progressive gain decrement and a corresponding phase lag that can be stimulated by a distributed relaxation model. H(V) was the only term to vary between units. It was mimicked by a two-term, fractional-lead operator with an exponent, k(V). At frequencies above an upper corner frequency of ~0.2 Hz, the operator introduces a phase lead that approaches 90°·2k(V) and a gain that increases as f(2k(v)). There is a systematic increase in the exponent from k(V) ~ 0 for the most regular units to k(V) ~ 0.3 for the most irregular units. Gains (g(2Hz)) for regular units increase linearly with CV* from ~25 spikes·s-1/g (CV* = 0.020) to ~ 125 spikes·s-1/g (CV* = 0.10). g(2Hz) for irregular units averages ~ 250 spikes·s-1/g and is unrelated to CV*. Unlike the situation previously described in the cristae, a separate group of low-gain irregular afferents was not evident among utricular fibers. Fibers innervating the anterolateral (AL) macula have especially thick axons and unusually large numbers of calyx endings. Despite this, their discharge properties are similar to those of units supplying other macular zones.
