Spontaneous Rate Auditory Nerve Fibers Research Articles

The Relative and Combined Effects of Noise Exposure and Aging on Auditory Peripheral Neural Deafferentation: A Narrative Review.

Animal studies have shown that noise exposure and aging cause a reduction in the number of synapses between low and medium spontaneous rate auditory nerve fibers and inner hair cells before outer hair cell deterioration. This noise-induced and age-related cochlear synaptopathy (CS) is hypothesized to compromise speech recognition at moderate-to-high suprathreshold levels in humans. This paper evaluates the evidence on the relative and combined effects of noise exposure and aging on CS, in both animals and humans, using histopathological and proxy measures. In animal studies, noise exposure seems to result in a higher proportion of CS (up to 70% synapse loss) compared to aging (up to 48% synapse loss). Following noise exposure, older animals, depending on their species, seem to either exhibit significant or little further synapse loss compared to their younger counterparts. In humans, temporal bone studies suggest a possible age- and noise-related auditory nerve fiber loss. Based on the animal data obtained from different species, we predict that noise exposure may accelerate age-related CS to at least some extent in humans. In animals, noise-induced and age-related CS in separation have been consistently associated with a decreased amplitude of wave 1 of the auditory brainstem response, reduced middle ear muscle reflex strength, and degraded temporal processing as demonstrated by lower amplitudes of the envelope following response. In humans, the individual effects of noise exposure and aging do not seem to translate clearly into deficits in electrophysiological, middle ear muscle reflex, and behavioral measures of CS. Moreover, the evidence on the combined effects of noise exposure and aging on peripheral neural deafferentation in humans using electrophysiological and behavioral measures is even more sparse and inconclusive. Further research is necessary to establish the individual and combined effects of CS in humans using temporal bone, objective, and behavioral measures.

Input-output curves of low and high spontaneous rate auditory nerve fibers are exponential near threshold

Input-output (IO) properties of cochlear transduction are frequently determined by analyzing the average discharge rates of auditory nerve fibers (ANFs) in response to relatively long tonal stimulation. The ANFs in cats have spontaneous discharge rates (SRs) that are bimodally distributed, peaking at low (<0.5 spikes/s) and high (∼60 spikes/s) rates, and rate-level characteristics differ depending upon SR. In an effort to assess the instantaneous IO properties of ANFs having different SRs, static IO-curves were constructed from period histograms based on phase-locking of spikes to the stimulus waveform. These curves provide information unavailable in conventional average rate-level curves. We find that all IO curves follow an exponential trajectory. It is argued that the exponential behavior represents the transduction in the IHC and that the difference among ANFs having different SRs is predominantly a difference in gain attributed most likely to synaptic drive. © 2018 The authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)

Evidence of “hidden hearing loss” following noise exposures that produce robust TTS and ABR wave-I amplitude reductions

In animals, noise exposures that produce robust temporary threshold shifts (TTS) can produce immediate damage to afferent synapses and long-term degeneration of low spontaneous rate auditory nerve fibers. This synaptopathic damage has been shown to correlate with reduced auditory brainstem response (ABR) wave-I amplitudes at suprathreshold levels. The perceptual consequences of this “synaptopathy” remain unknown but have been suggested to include compromised hearing performance in competing background noise. Here, we used a modified startle inhibition paradigm to evaluate whether noise exposures that produce robust TTS and ABR wave-I reduction but not permanent threshold shift (PTS) reduced hearing-in-noise performance. Animals exposed to 109 dB SPL octave band noise showed TTS >30 dB 24-h post noise and modest but persistent ABR wave-I reduction 2 weeks post noise despite full recovery of ABR thresholds. Hearing-in-noise performance was negatively affected by the noise exposure. However, the effect was observed only at the poorest signal to noise ratio and was frequency specific. Although TTS >30 dB 24-h post noise was a predictor of functional deficits, there was no relationship between the degree of ABR wave-I reduction and degree of functional impairment.

Hidden hearing loss and computational models of the auditory pathway: Predicting speech intelligibility decline

Recent animal studies have shown that noise exposures cause a permanent loss of low spontaneous rate auditory nerve fibers (ANFs) and reduction of auditory brainstem response wave-I amplitudes (Kujawa and Liberman, 2009). This phenomenon is thought to create difficulties understanding speech in noise in humans, although there is currently no established clinical technique to measure cochlear synaptopathy. The goal of this research is to utilize computational models of the auditory periphery and auditory cortex to study the effect of low spontaneous rate ANF loss on the cortical representation of speech intelligibility in noise. The auditory-periphery model of Zilany et al. (2009, 2014) is used to make predictions of auditory nerve responses to speech stimuli in noise. The resulting cochlear neurogram, a spectrogram-like output based on ANF outputs, is then used as a foundation for two different but related cortical representations of speech: the Spectro-Temporal Modulation Index (STMI; Elihali et al., 200...

Parallel pathways at the auditory periphery

We should consider the possibility that Low- and High- spontaneous rate (SR) auditory nerve fibers (ANFs) [1] constitute two different parallel pathways at the auditory periphery. The present study used a computational model of the auditory periphery [2] to demonstrate that Low- and High- SR ANFs have contrasting response properties. Anatomical studies suggest that Low- and High- SR ANF types have separate innervation sites (Figure ​(Figure1A)1A) on the same inner hair cell; lower-SR fibers synapse on the modiolar side and high-SR fibers synapse on the pillar side [3]. My hypothesis, prior to modeling the tuning curves (Figure ​(Figure1B),1B), was that Low Spontaneous Rate (Low-SR) fibers have a higher threshold for simulation and thus will have demonstrably sharper frequency selectivity than High-SR fibers. The results of the simulation support this framework; Low-SR ANFs were shown to have sharper frequency tuning (Figure ​(Figure1B)1B) than High-SR ANFs throughout a range of characteristic frequencies (CFs). While Low-SR ANFs have sharper frequency selectivity (Figure ​(Figure1B),1B), High-SR ANFs have finer temporal resolution, as the rate of change of the mean firing rate in High-SR ANFs was well above that of Low-SR fibers in the simulation (Figure ​(Figure1C).1C). It would seem that Low-SR and Medium-SR fibers (i.e. Lower-SR fibers) are optimized for “place theory” frequency coding and High-SR fibers are optimized for “volley-theory” synchronous phase locking. Future modeling efforts might maintain the integrity of these two parallel pathways, optimized for fine spectral (Lower-SR) and fine temporal (High-SR) resolution, by separating rather than summing their respective outputs. Figure 1 Innervation sites (A), tuning curves (B) and temporal response properties for Low- and High- SR ANFs

The sharp frequency selectivity of low- and medium- spontaneous rate auditory nerve fibers might allow for rate-place coding up to 5 kilohertz

One feature that might differentiate the three types of spontaneous rate (SR) auditory nerve fibers (ANFs) is the sharpness of frequency tuning at comparable sound pressure levels. My hypothesis, prior to modeling the tuning curves for each fiber type, was that low-SR fibers have a higher threshold for stimulation and thus have sharper frequency selectivity than medium-SR fibers, which in turn have sharper frequency selectivity than high-SR fibers. The results of the simulation support this framework. I used the Zilany et al. (2014) model of the auditory periphery and the cochlear tuning parameters from Shera et al. (2002) to generate tuning curves and neurogram raster plots for each of the three fiber types. The results of the simulation suggest that the sharp frequency selectivity of low-SR and medium-SR ANFs might allow for resolved rate-place coding up to 5 kHz. At frequencies below 1500 Hz, high-SR fibers were seen to have very different response properties than low-SR and medium-SR fibers. It is conceivable that the different fiber types constitute parallel pathways and mediate two different coding schemes. We should consider whether these sharply tuned low-SR and medium-SR ANFs, while fewer in number than High-SR ANFs, might be especially important for rate-place frequency coding.

Physiological and psychophysical assessments of the dynamic range of vowel representations in the auditory periphery

This review summarizes our work on the neural encoding of steady-state vowels. As in previous studies from our laboratory, the speech code is described in terms of average discharge rates for populations of neurons in the auditory nerve and ventral cochlear nucleus of barbiturate anesthetized cats. Our current analyses extend these population measures with new statistical models and signal detection methods to facilitate quantitative comparisons of the effects of stimulus level on vowel formant representations. These measures are applied to low and high spontaneous rate auditory-nerve fibers, and four of the principal response types of the ventral cochlear nucleus. The perceptual significance of the speech code is examined by relating neural response patterns to the behavioral performance of cats in vowel formant discrimination tasks. In combination, these physiological and psychophysical assessments suggest that vowel-coding mechanisms based on discharge rates in the auditory periphery are sufficient to support the dynamic range of speech perception.

The Functional Role of Excitatory and Inhibitory Interactions in Chopper Cells of the Anteroventral Cochlear Nucleus

Chopper cells in the anteroventral cochlear nucleus of the cat maintain a robust rate-place representation of vowel spectra over a broad range of stimulus levels. This representation resembles that of low threshold, high spontaneous rate primary auditory nerve fibers at low stimulus levels, and that of high threshold, low spontaneous rate auditory-nerve fibers at high stimulus levels. This has led to the hypothesis that chopper cells in the anteroventral cochlear nucleus selectively process inputs from different spontaneous rate populations of primary auditory-nerve fibers at different stimulus levels. We present a computational model, making use of shunting inhibition, for how this level dependent processing may be performed within the chopper cell dendritic tree. We show that this model (1) implements level-dependent selective processing, (2) reproduces detailed features of real chopper cell post-stimulus-time histograms, and (3) reproduces nonmonotonic rate versus level functions in response to single tones measured.

Neural encoding of single-formant stimuli in the cat. II. Responses of anteroventral cochlear nucleus units.

1. We have studied responses of anteroventral cochlear nucleus (AVCN) units to single-formant stimuli (SFS), in an effort to make quantitative comparisons with responses observed in auditory-nerve fibers (ANFs) to the same stimuli (Wang and Sachs 1993) and to reveal some of the signal processing mechanisms at the AVCN. Single-unit recordings and subsequent analyses were performed on each type of commonly recorded units, namely primarylike (Pri), primarylike with notch (PN), sustained chopper (ChS), transient chopper (ChT), and onset chopper (OnC), as well as a few onset (On) units, from the AVCN in anesthetized cats. The responses were obtained at a wide range of sound levels and at a frequency range of 1-10 kHz. Modulation in the envelopes of discharge patterns was quantified by a measure called modulation depth. 2. At moderate to high sound levels, most AVCN units were found to have enhanced modulation depth compared with that of ANFs, although the degree of enhancement varies among different types. All AVCN units, except Pri type, showed an enhancement in modulation depth over that of the highest of ANFs at moderate to high sound levels in the order of (from the highest to the lowest) On, OnC, ChT/PN, and ChS. Specifically, 1) modulation depth in Pri units was comparable to that of high spontaneous rate (SR) ANFs at low sound levels and to that of low/medium SR ANFs at high sound levels (in dB SPL). When sound level was normalized by unit threshold, Pri units, on average, exhibited only limited enhancement in envelope modulation at high sound levels (> 80 dB re threshold); 2) PN units showed substantially enhanced modulation depth over that of all SR groups of ANFs at moderate to high sound levels in dB SPL or dB re threshold scales; 3) significant enhancement in modulation depth was seen in both ChS and ChT units, with a slightly higher modulation depth in ChT type across sound levels (in dB SPL or dB re threshold); 4) modulation depth of OnC units was higher than those of primary-like (Pri and PN) and chopper (ChS and ChT) units at a wide range of sound levels; 5) responses from a limited sample of On units showed the highest modulation depth among all types of AVCN units. 3. Detailed analysis revealed that the enhanced modulation depth in the responses of AVCN units is the result of increased envelope peak height and decreased envelope minimum, relative to those of ANFs.(ABSTRACT TRUNCATED AT 400 WORDS)

Responses of DCN-PVCN neurons and auditory nerve fibers in unanesthetized decerebrate cats to AM and pure tones: Analysis with autocorrelation/power-spectrum

We investigated amplitude-modulated (AM) tone encoding behavior of dorsal and posteroventral cochlear-nucleus (DCN and PVCN) neurons and auditory nerve (AN) fibers in decerebrate unanesthetized cats. Some of the modulation transfer functions (MTFs) were narrowly-tuned band-pass functions; these included responses at moderate and high stimulus levels of DCN pause/build-type-III neurons and the following types of DCN and PVCN chopper neurons: chop-S and/or chop-type-I/III. Other MTFs were broad low-pass or complex functions. Chop-T neurons of the DCN and PVCN tended to exhibit low-pass or flat MTFs. The band-pass MTF neurons exhibited intrinsic oscillations (IOs) in responses to AM or pure tones. The IOs, which were detected in autocorrelation functions and power spectra, were closely correlated (r = 0.863) with the best envelope frequency (BEF). All of the AN fibers showed broad low-pass MTFs with some showing a rudimentary peak in the MTF. The MTFs of DCN-PVCN neurons and AN fibers showed, respectively: (1) BEFs ranging 50–500 Hz, and 400–1300 Hz; (2) upper cut-off frequencies ranging 200–1200 Hz, and 1600–3200 Hz. At stimulus levels of 60–85 dB SPL, maximum modulation gains were as high as 12 dB for DCN-PVCN neurons but were limited to below about 0 dB for AN fibers. The median dynamic ranges of DCN and PVCN neurons (51 and 42 dB, respectively) were substantially wider than those of the low and high spontaneous rate AN fibers (30 and 31 dB, respectively). The observation of higher modulation gain, wider dynamic range, and more narrowly-tuned MTF of DCN-PVCN neurons than AN fibers supports the concept that the capabilities to encode dynamic signals are enhanced in DCN-PVCN neurons compared with AN fibers.

Excitatory/inhibitory response types in the cochlear nucleus: relationships to discharge patterns and responses to electrical stimulation of the auditory nerve.

We have studied the response properties of single units in the cochlear nucleus of unanesthetized decerebrate cats. The purpose of the study was to compare the properties of cochlear nucleus units as described in two commonly used classification schemes. Units were first classified according to their receptive-field properties based on the relative prominence of excitatory and inhibitory responses to tones and noise. Units were then classified on the basis of their discharge patterns to short tone bursts at their best frequencies (BFs). Our results show that systematic relationships exist between the receptive-field properties and discharge patterns of cochlear nucleus units. Type I units give only excitatory responses to tones and noise. They are characterized by primary-like and chopper discharge patterns. Some units in the anteroventral cochlear nucleus have prepotentials in their spike waveforms. Prepotential units most often show primary-like discharge patterns, but prepotential units characterized by nonprimary-like discharge patterns are also found. Most prepotential units lack detectable inhibitory sidebands (type I), but two of the nonprimary-like prepotential units encountered in this study had inhibitory sidebands (type III). Type III units also give excitatory responses to BF tones, but they have inhibitory sidebands. Most type III units give chopper discharge patterns, and these units can be recorded throughout the cochlear nucleus. Some type III units in the dorsal cochlear nucleus give complex discharge patterns that can be described as a composite of the pauser pattern and other patterns. The complexity of these responses seems to increase as the amount of inhibition at BF increases. Type I/III units give excitatory responses to tones and noise, but have little or no spontaneous activity so they cannot be tested directly for inhibitory responses. Type I/III units typically show chopper discharge patterns. One group of type I/III units have rate-level functions with sloping saturation, suggesting that these may receive a predominance of input from low spontaneous rate auditory nerve fibers. Type II units are nonspontaneous and give excitatory responses to tones, but give weak or no responses to noise. While type II units are homogeneous as a group in terms of their response maps. BF rate-level functions, and responses to noise, they show a variety of discharge patterns in response to short tone bursts at BF.(ABSTRACT TRUNCATED AT 400 WORDS)

Phase-locked response to low-frequency tones in single auditory nerve fibers of the squirrel monkey.

Phase-locked response to low-frequency tones in single auditory nerve fibers of the squirrel monkey.