Recovery from prior stimulation. I: Relationship to spontaneous firing rates of primary auditory neurons

doi:10.1016/0378-5955(91)90106-J

Hearing Research

Volume 55, Issue 2, October 1991, Pages 215-222

https://doi.org/10.1016/0378-5955(91)90106-J Get rights and content

Abstract

Recovery of neural thresholds following a forward masker was measured for auditory neurons in anesthetized chinchillas. We find that recovery of forward-masked thresholds is slower for low spontaneous-rate neurons compared to high spontaneous-rate neurons. In addition, we studied the dependence of the shape of PST histograms on the time between repetitions of a tone-burst. We find that for low spontaneous-rate neurons, peak onset responses increase in magnitude over a longer range of interstimulus intervals compared to high spontaneous-rate neurons. Both results are consistent with the conclusion that low spontaneous-rate neurons take longer to recover from prior stimulation compared to high spontaneous-rate neurons. We suggest applications of this finding in psychophysical experiments to investigate the role of low spontaneous-rate neurons in intensity coding.

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Several approaches have been used to describe the rate-level functions of auditory-nerve fibers (ANFs). One approach uses descriptive models that can be fitted easily to data. Another derives rate-level functions from comprehensive physiological models of auditory peripheral processing. Here, we seek to identify the minimal set of components needed to provide a physiologically plausible account of rate-level functions. Our model consists of a first-order Boltzmann mechanoelectrical transducer function relating the instantaneous stimulus pressure to an instantaneous output, followed by a lowpass filter that eliminates the AC component, followed by an exponential synaptic transfer function relating the DC component to the mean spike rate. This is perhaps the simplest physiologically plausible model capable of accounting for rate-level functions under the assumption that the model parameters for a given ANF and stimulus frequency are level-independent. We find that the model typically accounts well for rate-level functions from cat ANFs for all stimulus frequencies. More complicated model variants having saturating synaptic transfer functions do not perform significantly better, implying the system operates far away from synaptic saturation. Rate saturation in the model is caused by saturation of the DC component of the filter output (e.g., the receptor potential), which in turn is due to the saturation of the transducer function. The maximum mean spike rate is approximately constant across ANFs, such that the slope parameter of the exponential synaptic transfer function decreases with increasing spontaneous rate. If the synaptic parameters for a given ANF are assumed to be constant across stimulus frequencies, then frequency- and level-dependent input nonlinearities are derived that are qualitatively similar to those reported in the literature. Contrary to assumptions in the literature, such nonlinearities are obtained even for ANFs having high spontaneous rates. Finally, spike-rate adaptation is examined and found to be accounted for by a decrease in the slope parameter of the synaptic transfer function over time following stimulus onset.
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Citation Excerpt :
In contrast, for ISIs of around 300 ms the probability for a spike to occur was well above two times the probability for a spike to occur in the adapted phase. Thus, the appropriate duration of the silent gap for a reset of the primacy effect found in our study roughly corresponds to the duration of the ISIs necessary to regain a pronounced initial peak in the firing rate of the LSR auditory nerve neurons in the study by Relkin and Doucet (1991). As the size of the initial peak in the firing rate of the LSR fibers at the onset of a sound increased with increasing ISI, these findings are also compatible with the observed effect of increasing primacy effects on the second sound part with increasing ISIs.
Human loudness judgments of time-varying sounds show a non-uniform temporal weighting pattern with increased weights at the beginning of a sound. Four experiments were conducted to investigate whether this primacy effect reoccurs after a silent gap of an appropriate duration that is inserted into a level-fluctuating sound. In three of the experiments, contiguous sounds as well as sounds containing silent gaps of different durations were presented. The temporal loudness weights were compared between the sounds that contained a gap and the sounds without a gap. The data showed that with increasing gap duration an increasingly pronounced primacy effect reoccurred on the second sound part in the sense that a) the weights assigned to the first segments after the gap were increased compared to the conditions without a gap, and that b) the following weights again showed a decrease over time. This effect was statistically significant for gap durations of 350 ms and above. To investigate whether an attenuation in level can lead to the same results as a silent gap, segments in the middle part of a sound were attenuated in the fourth experiment, and the resulting weights were compared to conditions in which the middle segments were unattenuated or where a 700 ms silent gap was presented instead of the middle segments. An attenuation of 15 dB resulted in a significant reoccurrence of the primacy effect, although the effect was more pronounced for an attenuation of 30 dB and the silent gap. The results are discussed in the light of auditory nerve responses, masking effects on intensity resolution, and assumptions based on evidence integration processes.
Effects of lifetime noise exposure on the middle-age human auditory brainstem response, tinnitus and speech-in-noise intelligibility
2018, Hearing Research
Recent animal studies have shown that the synapses between inner hair cells and the dendrites of the spiral ganglion cells they innervate are the elements in the cochlea most vulnerable to excessive noise exposure. Particularly in rodents, several studies have concluded that exposure to high level octave-band noise for 2 h leads to an irreversible loss of around 50% of synaptic ribbons, leaving audiometric hearing thresholds unaltered. Cochlear synaptopathy following noise exposure is hypothesized to degrade the neural encoding of sounds at the subcortical level, which would help explain certain listening-in-noise difficulties reported by some subjects with otherwise ‘normal’ hearing. In response to this peripheral damage, increased gain of central stages of the auditory system has been observed across several species of mammals, particularly in association with tinnitus. The auditory brainstem response (ABR) wave I amplitude and waves I-V amplitude ratio have been suggested as non-invasive indicators of cochlear synaptopathy and central gain activation respectively, but the evidence for these hearing disorders in humans is inconclusive. In this study, we evaluated the influence of lifetime noise exposure (LNE) on the human ABR and on speech-in-noise intelligibility performance in a large cohort of adults aged 29 to 55. Despite large inter-subject variability, results showed a moderate, but statistically significant, negative correlation between the ABR wave I amplitude and LNE, consistent with cochlear synaptopathy. The results also showed (a) that central gain mechanisms observed in animal studies might also occur in humans, in which higher stages of the auditory pathway appear to compensate for reduced input from the cochlea; (b) that tinnitus was associated with activation of central gain mechanisms; (c) that relevant cognitive and subcortical factors influence speech-in-noise intelligibility, in particular, longer ABR waves I-V interpeak latencies were associated with poorer performance in understanding speech in noise when central gain mechanisms were active; and (d) absence of a significant relationship between LNE and tinnitus, central gain activation or speech-in-noise performance. Although this study supports the possible existence of cochlear synaptopathy in humans, the great degree of variability, the lack of uniformity in central gain activation and the significant involvement of attention in speech-in-noise performance suggests that noise-induced cochlear synaptopathy is, at most, one of several factors that play a role in humans' speech-in-noise performance.
Evidence of noise-induced subclinical hearing loss using auditory brainstem responses and objective measures of noise exposure in humans
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Citation Excerpt :
Synaptic inefficiency could arise from a number of sources, including a selective depopulation of low-spontaneous rate nerve fibers (low-SR), inefficient neurotransmitter release, and/or myelinopathy. Low-SR auditory nerve fibers, which have been found to be more vulnerable to noise-induced damage than high-spontaneous rate fibers (Furman et al., 2013; Liberman and Liberman, 2015), have longer recovery times following adaptation than high-SR fibers (Relkin and Doucet, 1991; Relkin et al., 1995) and their characteristic adaptation properties are evident for human and non-human species in the amplitude of the compound action potential (CAP) (Murnane et al., 1998; Relkin et al., 1995), an analog of ABR wave I. This literature on the CAP sets up the prediction that the selective loss of low-SR nerve fibers that follows cochlear synaptopathy would lead to impaired temporal processing.
Exposure to loud sound places the auditory system at considerable risk, especially when the exposure is routine. The current study examined the impact of routine auditory overexposure in young human adults with clinically-normal audiometric thresholds by measuring the auditory brainstem response (ABR), an electrophysiological measure of peripheral and central auditory processing. Sound exposure was measured objectively with body-worn noise dosimeters over a week. Participants were divided into low-exposure and high-exposure groups, with the low-exposure group having an average daily noise exposure dose of ∼11% of the recommended exposure limit compared to the high-exposure group average of nearly 500%. Compared to the low-exposure group, the high-exposure group had delayed ABRs to suprathreshold click stimuli and this prolongation was evident at ABR waves I and III but strongest for V. When peripheral differences were corrected using the I-V interpeak latency, the high-exposure group showed greater taxation at faster stimulus presentation rates than the low-exposure group, suggestive of neural conduction inefficiencies within central auditory structures. Our findings are consistent with the hypothesis that auditory overexposure affects peripheral and central auditory structures even before changes are evident on standard audiometry. We discuss our findings within the context of the larger debate on the mechanisms and manifestations of subclinical hearing loss.

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Recovery from prior stimulation. I: Relationship to spontaneous firing rates of primary auditory neurons

Abstract

Hear. Res.

Hear. Res.

J. Phon.

Hear. Res.

Hear. Res.

Relationship between the dynamic range of cochlear nerve fibres and their spontaneous activity

Exptl. Brain Res.

Level discrimination as a function of level for tones from 0.25 to 16 kHz

J. Acoust. Soc. Am.

Possible role of low and medium spontaneous rate cochlear nerve fibers in the encoding of waveform periodicity

Forward masking as a function of frequency, masker level, and signal delay

J. Acoust. Soc. Am.

Discharge Patterns of Single Fibers in the Cat's Auditory Nerve

A population study of auditory-nerve fibers in unanesthetized decerebrate cats: Responses to pure tones

J. Acoust. Soc. Am.

A population study of cochlear nerve fibers: Comparison of spatial distributions of average-rate and phase-locking measures of responses to single tones

J. Neurophysiol.