Primary Auditory Nerve Fibers Research Articles

Suppression tuning of spontaneous otoacoustic emissions in the barn owl (Tyto alba)

Spontaneous otoacoustic emissions (SOAEs) have been observed in a variety of different vertebrates, including humans and barn owls (Tyto alba). The underlying mechanisms producing the SOAEs and the meaning of their characteristics regarding the frequency selectivity of an individual and species are, however, still under debate. In the present study, we measured SOAE spectra in lightly anesthetized barn owls and suppressed their amplitudes by presenting pure tones at different frequencies and sound levels. Suppression effects were quantified by deriving suppression tuning curves (STCs) with a criterion of 2 dB suppression. SOAEs were found in 100% of ears (n = 14), with an average of 12.7 SOAEs per ear. Across the whole SOAE frequency range of 3.4–10.2 kHz, the distances between neighboring SOAEs were relatively uniform, with a median distance of 430 Hz. The majority (87.6%) of SOAEs were recorded at frequencies that fall within the barn owl’s auditory fovea (5–10 kHz). The STCs were V-shaped and sharply tuned, similar to STCs from humans and other species. Between 5 and 10 kHz, the median Q10dB value of STC was 4.87 and was thus lower than that of owl single-unit neural data. There was no evidence for secondary STC side lobes, as seen in humans. The best thresholds of the STCs varied from 7.0 to 57.5 dB SPL and correlated with SOAE level, such that smaller SOAEs tended to require a higher sound level to be suppressed. While similar, the frequency-threshold curves of auditory-nerve fibers and STCs of SOAEs differ in some respects in their tuning characteristics indicating that SOAE suppression tuning in the barn owl may not directly reflect neural tuning in primary auditory nerve fibers.

The side of cochlear implantation and speech intelligibility in pediatric and adult cochlear implantees

Abstract A cochlear implant (CI) is an auditory prosthesis that stimulates the primary auditory nerve fibers electrically to elicit sound perception in individuals with severe-to-profound sensorineural hearing impairments. Speech intelligibility is a joint product of a speaker and a listener and can provide a close approximation of an individual’s everyday communication status, and cochlear implants can facilitate the development of speech and language skills in prelingually deaf patients. The aim of this work was to study whether there is an advantage of one ear in the improvement of speech intelligibility in pediatric and adult cochlear-implanted patients. A cross-sectional study to assess the speech intelligibility of right and left cochlear-implanted patients. The study included 50 cochlear-implanted patients (24 male and 26 female): 25 of the patients were prelingual and 25 were postlingual. Twenty-six of the patients were implanted on the right ear and 24 were implanted on the left ear. Speech intelligibility assessment was conducted using the Arabic Speech Intelligibility test. This Arabic Speech Intelligibility test is meant to be an objective measure as the examiner does not have to evaluate how a word was said. The results revealed that there was no significant difference between the speech intelligibility percentage regarding the onset of deafness (prelingual or postlingual), the sex and the duration of therapy, but there was a significant difference between the speech intelligibility percentage in right-ear-implanted and left-ear-implanted patients, with marked advantage for the implanted right ear. Right-ear cochlear implantation has an advantage over left-ear implantation regarding the speech intelligibility. Hence, in case of bilateral profound deafness of the same degree with no anatomical complications in either of the ears, it is recommended to choose the right ear for cochlear implantation.

The Reduced Cochlear Output and the Failure to Adapt the Central Auditory Response Causes Tinnitus in Noise Exposed Rats

Tinnitus is proposed to be caused by decreased central input from the cochlea, followed by increased spontaneous and evoked subcortical activity that is interpreted as compensation for increased responsiveness of central auditory circuits. We compared equally noise exposed rats separated into groups with and without tinnitus for differences in brain responsiveness relative to the degree of deafferentation in the periphery. We analyzed (1) the number of CtBP2/RIBEYE-positive particles in ribbon synapses of the inner hair cell (IHC) as a measure for deafferentation; (2) the fine structure of the amplitudes of auditory brainstem responses (ABR) reflecting differences in sound responses following decreased auditory nerve activity and (3) the expression of the activity-regulated gene Arc in the auditory cortex (AC) to identify long-lasting central activity following sensory deprivation. Following moderate trauma, 30% of animals exhibited tinnitus, similar to the tinnitus prevalence among hearing impaired humans. Although both tinnitus and no-tinnitus animals exhibited a reduced ABR wave I amplitude (generated by primary auditory nerve fibers), IHCs ribbon loss and high-frequency hearing impairment was more severe in tinnitus animals, associated with significantly reduced amplitudes of the more centrally generated wave IV and V and less intense staining of Arc mRNA and protein in the AC. The observed severe IHCs ribbon loss, the minimal restoration of ABR wave size, and reduced cortical Arc expression suggest that tinnitus is linked to a failure to adapt central circuits to reduced cochlear input.

Tinnitus with a Normal Audiogram: Physiological Evidence for Hidden Hearing Loss and Computational Model

Ever since Pliny the Elder coined the term tinnitus, the perception of sound in the absence of an external sound source has remained enigmatic. Traditional theories assume that tinnitus is triggered by cochlear damage, but many tinnitus patients present with a normal audiogram, i.e., with no direct signs of cochlear damage. Here, we report that in human subjects with tinnitus and a normal audiogram, auditory brainstem responses show a significantly reduced amplitude of the wave I potential (generated by primary auditory nerve fibers) but normal amplitudes of the more centrally generated wave V. This provides direct physiological evidence of "hidden hearing loss" that manifests as reduced neural output from the cochlea, and consequent renormalization of neuronal response magnitude within the brainstem. Employing an established computational model, we demonstrate how tinnitus could arise from a homeostatic response of neurons in the central auditory system to reduced auditory nerve input in the absence of elevated hearing thresholds.

Tuning and timing of excitation and inhibition in primary auditory nerve fibers

Information about the tuning and timing of excitation, adaptation and suppression in an auditory primary afferent axon can be obtained from the second-order Wiener kernel. Through the process of singular-value decomposition, this information can be extracted from the kernel and displayed graphically in separate two-dimensional images for excitation and inhibition 1 1 In this paper, we use the term inhibition to include all of those phenomena (such as adaptation and rate suppression) that result in reduction of instantaneous spike rate in a primary auditory afferent axon; it does not imply involvement of inhibitory synapses. We use excitation to include all of those phenomena that result in increase of instantaneous spike rate. . For low- to mid-frequency units, the images typically include checkerboard patterns. For all units they may include patterns of parallel diagonal lines. The former represent non-linearities in the phase-locked (ac) response of the unit; the latter reflect non-linear envelope-following (dc) responses. Examples of detailed interpretation are presented for three amphibian-papillar units from the American bullfrog. The second-order Wiener kernel itself is derived from second-order reverse correlation between spikes and a continuous, non-repeating, broad-band white-noise stimulus.

Serotonin projection patterns to the cochlear nucleus

The cochlear nucleus is well known as an obligatory relay center for primary auditory nerve fibers. Perhaps not so well known is the neural input to the cochlear nucleus from cells containing serotonin that reside near the midline in the midbrain raphe region. Although the specific locations of the main, if not sole, sources of serotonin within the dorsal cochlear nucleus subdivision are known to be the dorsal and median raphe nuclei, sources of serotonin located within other cochlear nucleus subdivisions are not currently known. Anterograde tract tracing was used to label fibers originating from the dorsal and median raphe nuclei while fluorescence immunohistochemistry was used to simultaneously label specific serotonin fibers in cat. Biotinylated dextran amine was injected into the dorsal and median raphe nuclei and was visualized with Texas Red, while serotonin was visualized with fluorescein. Thus, double-labeled fibers were unequivocally identified as serotoninergic and originating from one of the labeled neurons within the dorsal and median raphe nuclei. Double-labeled fiber segments, typically of fine caliber with oval varicosities, were observed in many areas of the cochlear nucleus. They were found in the molecular layer of the dorsal cochlear nucleus, in the small cell cap region, and in the granule cell and external regions of the cochlear nuclei, bilaterally, of all cats. However, the density of these double-labeled fiber segments varied considerably depending upon the exact region in which they were found. Fiber segments were most dense in the dorsal cochlear nucleus (especially in the molecular layer) and the large spherical cell area of the anteroventral cochlear nucleus; they were moderately dense in the small cell cap region; and fiber segments were least dense in the octopus and multipolar cell regions of the posteroventral cochlear nucleus. Because of the presence of labeled fiber segments in subdivisions of the cochlear nucleus other than the dorsal cochlear nucleus, we concluded that the serotoninergic projection pattern to the cochlear nucleus is divergent and non-specific. Double-labeled fiber segments were also present, but sparse, in the superior olive, localized mainly in periolivary regions; this indicated that the divergence of dorsal and median raphe neurons that extends throughout regions of the cochlear nucleus also extended well beyond the cochlear nucleus to include at least the superior olivary complex as well.

The responses of single units in the ventral cochlear nucleus of the guinea pig to damped and ramped sinusoids

Human listeners hear an asymmetry in the perception of damped and ramped sinusoids; the partial loudness of the envelope component is greater than the partial loudness of the carrier component for damped sinusoids. Here we show that an asymmetry also occurs in the physiological responses of most units in the ventral cochlear nucleus to these same sounds. The activity elicited by damped sinusoids is mainly restricted to the beginning of each envelope period, which is not the case for ramped sinusoids. This can be quantified by computing the ratio of the tallest bin of the modulation period histogram to the total number of spikes (the peak-to-total ratio, p/ t). Damped sinusoids produce a higher p/ t than ramped sinusoids, which demonstrates physiological temporal asymmetry. It is also the case that ramped sinusoids typically elicit more spikes than damped sinusoids. The physiological asymmetry occurs where the perceptual asymmetry is present. It is maximal at modulation half-lives of 4 and 16 ms, greatly reduced at 1 ms and absent at 64 ms. Different unit types exhibit differing degrees of temporal asymmetry. Onset units produce the greatest p/ t asymmetry, primary-like units produce the least asymmetry and chopper units are in-between. With regard to total spike count, the maximal asymmetry occurs with chopper units. If primary-like units are assumed to reflect the activity in primary auditory nerve fibres, then there is enhancement of temporal asymmetry in the ventral cochlear nucleus by both onset and chopper units.

The influence of stochastic behavior on the human threshold of hearing

The inner hair cells in the cochlea perform the crucial task of transforming mechanical sound signals into electrical activity. The cochlear nerve fibers code this information and convey it to the brain for further processing. This study investigates the performance of the system inner hair cell – primary auditory afferent nerve fibers at the physical limit of the mechano-electrical transduction for the human auditory frequency range. The Brownian motion of the hair cell’s receptive organelle, the hair bundle, does not blunt the sensitivity, but in fact enlarges – especially in frequency regions which are most important for the perception of music and speech – via the mechanism of nonlinear stochastic resonance (SR) the dynamical range of the mechano-electrical transduction by at least one order of magnitude. The coding efficiency of small sinusoidal hair bundle deflections shows basic properties of the human hearing threshold curve for pure tones and corresponds to experimental results of noise-induced tuning curves in mechano-receptors in the rat foot. Furthermore, the model explains how altered coding efficiency contributes to pathological changes in the spiking pattern which arise from morphological changes in the hair bundle structure (e.g., in noise-induced sensorineural hearing loss of cochlear origin).

Dissecting the frog inner ear with Gaussian noise. I. Application of high-order Wiener-kernel analysis

Wiener kernel analysis was used to characterize the auditory pathway from tympanic membrane to single primary auditory nerve fibers in the European edible frog, Rana esculenta. Nerve fiber signals were recorded in response to white Gaussian noise. By cross-correlating the noise stimulus and the nerve fiber response, we computed (1) the full second-order Wiener kernel, and (2) the diagonals of the zeroth- to fourth-order Wiener kernels. These diagonals are usually referred to as polynomial correlation functions. The measured Wiener kernels were fitted with a ‘sandwich’ model. A new fitting procedure was used to compute the response characteristics of (1) the first filter, (2) the static nonlinearity, and (3) the second filter, which form the functional components of the model. The first filter is a bandpass filter. In the majority of low frequency fibers, with best excitatory frequency (BEF) < 800 Hz, this filter was tuned to two frequencies. This dual tuning mechanism gives rise to ‘off-diagonal’ components in the second-order Wiener kernel. The static nonlinearity resembles a rectifier, and is dominated by second-order (quadratic) nonlinearity. As a function of BEF, the shape of the nonlinearity changes systematically. Finally, the last filter in the model was a low pass filter. Across fibers, its cutoff frequency ƒ −3 dB ranged from 106 to 434 Hz.

Dissecting the frog inner ear with Gaussian noise. II. Temperature dependence of inner ear function

The temperature dependence of the response of single primary auditory nerve fibers ( n = 31) was investigated in the European edible frog, Rana esculenta (seven ears). Nerve fiber responses were analyzed with Wiener kernel analysis and polynomial correlation. The responses were described with a cascade model, consisting of a linear bandpass filter, a static nonlinearity, and a linear lowpass filter. From the computed Wiener kernels and the polynomial correlation functions, the characteristics of the three model components were obtained. With increasing temperature (1) tuning of the first filter increased in the majority ( n = 16) of amphibian papilla fibers (best excitatory frequency, BEF < 1 kHz, n = 21) but remained unchanged in the majority ( n = 10) of basilar papilla fibers (BEF > 1 kHz, n = 11), (2) the gain of the first filter remained unchanged, (3) the shape of nonlinear 10 function remained unchanged, (4) the combined gain of the static nonlinearity and the second filter usually increased, but displayed considerable scatter across fibers (from −0.7 dB/†C to 3 dB/†C), and (5) the cutoff frequency of the second lowpass filter increases, with average 0.13 oct/°C. The immunity of the shape of the nonlinearity is considered evidence of a temperature independent gating mechanism in the transduction channels. The temperature dependence of the second filter may have resulted from a decrease of the hair cell membrane resistance, but may also reflect changes in subsequent staging of nerve fiber excitation.

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.

Wiener kernel analysis of inner ear function in the American bullfrog

The response of 17 primary auditory nerve fibers in the American bullfrog (Rana catesbeiana) to acoustic noise stimulation of the tympanic membrane was recorded. For each fiber, the first- and second-order Wiener kernels, k1 (tau 1) and k2 (tau 1, tau 2), were computed by cross correlation of the stimulus and the response. The kernels revealed amplitude and phase characteristics of auditory filters of both phase-locking and non-phase-locking fibers. Wiener kernels of high- and midfrequency fibers (best frequency, BF > 500 Hz), implied a simple sandwich model, consisting of a cascade of a linear bandpass filter, a static nonlinearity, a linear low-pass filter, and a spike generator. The bandpass filter was at least of order 7, and had a linear phase response, for both the high- and the midfrequency fibers. Averaged across fibers, filter order 2, and cutoff frequency 451 Hz for the second filter in the model was observed. The responses of low-frequency fibers (BF < 500 Hz) could not be fit with the sandwich model, because the Fourier transform K2 (f1,f2) of the second-order Wiener kernel showed significant components at off-diagonal frequencies f1 not equal to +/- f2. The presence of these off-diagonal components shows that, in addition to the phase and gain characteristics of auditory filters, the Wiener kernel analysis reveals nonlinear two-tone interactions.

Auditory nerve terminals in the cochlear nucleus magnocellularis: Differences between low and high frequencies

Primary auditory nerve fibers were labelled in the barn owl by localized horseradish peroxidase (HRP) injections into the cochlear nucleus angularis. They were followed to their terminal sites in the hearing organ (basilar papilla), confirming that they were auditory, and to the cochlear nucleus magnocellularis. The terminal sites of low-frequency fibers within nucleus magnocellularis always included an area previously described as the lagenar part, i.e., an area receiving primary input which is probably only vestibular. Furthermore, a number of differences were recognized between these low-frequency (up to 0.64 kHz) and the high-frequency (1.8 kHz and above) auditory nerve projections to nucleus magnocellularis. Most importantly, the collaterals given off by low-frequency fibers into the nucleus typically showed multiple terminal branching, with both en passant and terminal bouton-like swellings. High-frequency fiber collaterals, in contrast, terminated unbranched in a single endbulb of Held. Nucleus magnocellularis is the first station in a brainstem auditory pathway processing stimulus timing information, coded through neuronal phase locking. The prominent difference in terminal shape found between its low- and high-frequency input fibers is interpreted as reflecting different requirements of the absolute temporal precision for significant phase locking. Terminals in the shape of endbulbs of Held are probably a specialization to improve the temporal precision of synaptic transmission, allowing phase locking to higher frequencies.

Spectral characteristics and synchrony in primary auditory-nerve fibers in response to pure-tone acoustic stimuli

Under pure-tone stimulation, the spectrum of the period histogram recorded from primary auditory-nerve fibers at low and medium frequencies contains components at DC, at the applied tone frequency (the fundamental), and at a small number of harmonics of the tone frequency. The magnitudes and phases of these spectral components are examined. The spectral magnitudes of the fundamental and various harmonic components generally bear a fixed proportionality to each other over a broad range of signal conditions and nerve-fiber characteristics. This implies that the shape of the underlying rectified wave remains essentially unchanged over a broad range of stimulus intensities. For high-frequency stimuli, the fundamental and harmonic components are substantially attenuated. We provide a theoretical basis for the decrease of the spectralcomponent magnitudes with increasing harmonic number. For low-frequency pure-tone signals, the decrease is caused principally by the uncertainty in the position of neural-event occurrences within the half-wave-rectified period histogram. The lower the stimulus frequency, the greater this time uncertainty and therefore the lower the frequency at which the spectral components begin to diminish. For high-frequency pure-tone signals, on the other hand, the decrease is caused principally by the frequency rolloff associated with nervespike time jitter (it is then called loss of phase locking or loss of synchrony). Since some of this jitter arises from noise in the auditory nerve, it can be minimized by using peak detection rather than level detection. Using a specially designed microcomputer that measures the times at which the peaks of the action potentials occur, we have demonstrated the presence of phase locking to tone frequencies as high as 18 kHz. The traditional view that phase locking is always lost above 6 kHz is clearly not valid. This indicates that the placeversus-periodicity dichotomy in auditory theory requires reexaraination.

Shapes of rate-versus-level functions of primary auditory nerve fibres: Test of the basilar membrane mechanical hypothesis

Rate-versus level functions (RI functions) for characteristic frequency (CF) stimulation were measured from primary auditory nerve fibres from different spontaneous rate categories in the guinea pig cochlea. Attention was focussed on those fibres that showed clear breakpoints in their RI functions (sloping-saturation fibres). A statistical curve fitting procedure to an empirical equation was used to provide a quantitative estimate of the breakpoint position in individual fibres. It was found that, within the limits of reliability of the curve fitting procedure, the breakpoint position was the same in fibres from the same CF regions in any given animal. This result is consistent with the notion that the breakpoint position is determined by global basilar membrane mechanics and not by processes private to each nerve fibre. However, a subgroup of fibres not easily classifiable as sloping-saturation, showed features of their RI functions suggesting that factors other than basilar membrane mechanics could lead to fibre-to-fibre differences in rate-versus-level behaviour.

Activity patterns of primary auditory-nerve fibres in chickens: Development of fundamental properties

We have examined the activity patterns of single auditory-nerve fibres in the chicken and tested for possible changes during post-hatching development. For this purpose, we recorded from fibres in the cochlear ganglion of chickens of two age groups (about P2 and P21) and investigated their spontaneous and sound-evoked activity patterns under nembutal-chloralhydrate anaesthesia. The spontaneous activity of primary auditory neurones was irregular, the average rates were between 20.5 (P2) and 23 (P21) spikes/s. Many low-frequency fibres from both age groups showed preferred intervals in their spontaneous activity. Tuning characteristics, including the range of characteristic frequencies, the presence of primary and two-tone suppression, the slopes of tuning-curve flanks and Q 10 dB values were similar to those previously reported for the starling and were statistically indistinguishable between the two age groups. However, there was a difference in fibre thresholds at the highest frequencies. Systematic differences were also present between the two age groups with regard to some characteristics of the rate-intensity functions. These data indicate that whereas the tuning properties of primary auditory fibres of the chicken cochlea are mature as early as post-hatching day 2, the intensity functions are not.

Rate-versus-level functions of primary auditory nerve fibres: Evidence for square law behaviour of all fibre categories in the guinea pig

Detailed measurements of rate-versus-level (RI) functions close to threshold were made from single primary auditory nerve fibres in the guinea pig cochlea. For all fibres, a simple square law provided the best statistical fit to the data near threshold, regardless of spontaneous firing rate of the fibre. In no case was a better fit obtained with an exponent greater than 2. We conclude that a simple square law is an accurate description of the underlying synaptic drive to all primary auditory nerve fibres. For fibres with very low spontaneous firing rates the best square law fit near threshold frequently led to the formal mathematical estimate of a negative firing rate as the asymptotic value of the spontaneous firing rate. The ‘negative spontaneous rate’ of low spontaneous rate fibres derived from curve fitting can be conceptualized by postulating that for sound pressures well below threshold in these fibres the underlying synaptic drive lies below a threshold value at a site determining actio potential generation.

Changes in cochlear sensitivity do not alter relative thresholds of different spontaneous rate categories of primary auditory nerve fibres

The CF thresholds of three different spontaneous firing rate categories of single auditory nerve fibres were measured in guinea pigs with widely differing cochlear sensitivities. The CF thresholds for all fibres were compared to the CAP thresholds at the same frequencies. The relationship between single fibre CF threshold and CAP thresholds for the three different fibre categories remained unchanged despite the very wide range of absolute CAP thresholds. The widely ranging CAP thresholds in these animals were probably due to varying degrees of outer hair cell pathology and these data therefore support the notion that in normal animals, the origin of differences in threshold between fibres with different spontaneous rates, lies in the properties of the inner hair cells and/or their synapses with afferent dendrites.

Classification of the temporal discharge patterns of single auditory neurons in the dorsal medullary nucleus of the northern leopard frog

1. The dorsal medullary nucleus (DMN) of frogs is the presumed homolog of the mammalian cochlear nucleus (CN). Like the CN, the DMN is the sole target of centrally projecting primary auditory-nerve fibers and the first central auditory-processing center. To study the transformation of acoustic information in the DMN, we have utilized relatively simple stimuli--tone bursts--to detail the temporal discharge patterns of DMN neurons that can be compared with those shown by auditory-nerve fibers. 2. Based on the shape of poststimulus time (PSTH) and interspike interval (ISIH) histograms, we observed six distinctive discharge patterns to tone bursts presented at the best excitatory frequency (BEF), 10 dB above threshold. Four of these (primary-like type 1-4) resembled discharge patterns seen at the level of the auditory nerve, whereas two (phasic and phasic burst) were only observed in the DMN. 3. At stimulus levels of 20-30 dB above BEF threshold several phasic neurons became tonic responders, whereas several primary-like type-2 cells gave "pauser" discharges. The response patterns of the remaining cells were intensity independent. 4. We further showed that many of the single-unit discharge patterns were related to other neuronal response properties; specifically, spontaneous firing rate, intensity-rate functions, threshold, latency, BEF, and sharpness of tuning (Q10). 5. The implications of our findings are discussed with respect to 1) the transformation of acoustic information as it is passed from the auditory nerve to the DMN, and 2) the functional organization of the DMN.

Peripheral auditory processing in the bobtail lizard Tiliqua rugosa

Primary auditory-nerve fibres of the bobtail lizard have asymmetrical, V-shaped frequency-threshold tuning curves. Fibre characteristic frequencies (CF) ranged from 0.2 to 4.5 kHz. The tuning sharpness and the thresholds of both low- and high-CF fibres were hypoxia-sensitive, the loss of sensitivity being greatest at CF. Only the low-CF group of fibres showed two-tone rate suppression. In those fibres, two-tone rate suppression was only found with suppressor frequencies above CF, but not below CF