Tonotopic Distribution of Short-Term Adaptation Properties in the Cochlear Nerve of Normal and Acoustically Overexposed Chicks

Abstract

Cochlear nerve adaptation is thought to result, at least partially, from the depletion of neurotransmitter stores in hair cells. Recently, neurotransmitter vesicle pools have been identified in chick tall hair cells that might play a role in adaptation. In order to understand better the relationship between adaptation and neurotransmitter release dynamics, short-term adaptation was characterized by using peristimulus time histograms of single-unit activity in the chick cochlear nerve. The adaptation function resulting from 100-ms pure tone stimuli presented at the characteristic frequency, +20 dB relative to threshold, was well described as a single exponential decay process with an average time constant of 18.6 T 0.8 ms (mean T SEM). The number of spikes contributed by the adapting part of the response increased tonotopically for characteristic frequencies up to õ0.8 kHz. Comparison of the adaptation data with known physiological and anatomical hair cell properties suggests that depletion of the readily releasable pool is the basis of short-term adaptation in the chick. With this idea in mind, short-term adaptation was used as a proxy for assessing tall hair cell synaptic function following intense acoustic stimulation. After 48 h of exposure to an intense pure tone, the time constant of short-term adaptation was unaltered, whereas the number of spikes in the adapting component was increased at characteristic frequencies at and above the exposure frequency. These data suggest that the rate of readily releasable pool emptying is unaltered, but the neurotransmitter content of the pool is increased, by exposure to intense sound. The results imply that an increase in readily releasable pool size might be a compensatory mechanism ensuring the strength of the hair cell afferent synapse in the face of ongoing acoustic stress.

Adaptation Reduces Spike-Count Reliability, But Not Spike-Timing Precision, of Auditory Nerve Responses

“…As CF increased, adaptation also increased, as measured by a decrease in with duration of stimulation. This was consistent with previous findings (Crumling and Saunders, 2007). The adapted spike-count variance, , was only slightly higher than the initial and was not significantly different at the lowest frequency range (Fig.…”

“…9A). Interestingly, at progressively lower frequencies, the time course of spike-rate adaptation slows (Crumling and Saunders, 2007). Thus, over 35 ms, there is a smaller change in the mean spike count (Fig.…”

“…In chick auditory nerve, the average time constant of adaptation is 19 ms, but is much more pronounced in higher CF cells (Fig. 1, compare A, B with C, D), where the time constants of adaptation can be four times faster (Crumling and Saunders, 2007).…”

“…In response to a constant stimulus, the firing rate of a cochlear neuron rapidly decreases to a maintained firing rate over a time course of tens of milliseconds (Kiang, 1965;Westerman and Smith, 1984;Crumling and Saunders, 2007). This rapid form of adaptation is likely mediated by exhaustion of release-ready synaptic vesicles in the cochlear hair cell (Furukawa et al, 1978;Moser and Beutner, 2000;Spassova et al, 2004).…”

Rapid Neural Adaptation to Sound Level Statistics

“…Previous studies have demonstrated that the time course of spike rate adaptation of auditory nerve fibers (ANFs) during pure tone bursts is related to neural CF (Westerman and Smith, 1985;Crumling and Saunders, 2007). A similar relationship was observed in the adaptation to sound level statistics examined in the current study.…”