Intensity coding in the auditory periphery of the cat: Responses of cochlear nerve and cochlear nucleus neurons to signals in the presence of bandstop masking noise

The dynamic range over which fine intensity discrimination is possible has been reported to be largely unaffected by limitation of the spread of neuronal activity to neighbouring frequency regions by bandstop noise masking.We have therefore examined the responses of cochlear nerve and nucleus neurons to tone and noise signals in the presence of a bandstop masking noise designed to be comparable to that employed in the psychophysical experiments. Under these conditions, the vast majority of cochlear nerve fibres were saturated by sound levels at which some 50% of our sample of cochlear nucleus neurons still responded to signal level differences. The extended dynamic ranges of these cochlear nucleus neurons was shown to be a result of activation, by the masking noise, of the lateral inhibitory side-bands ‘biassing’ the neuron's discharge. A small proportion of cochlear fibres, having low spontaneous discharge rates and showing strong two-tone suppression effects, demonstrated analogous but not so pronounced effects. It is unclear in what form information on the level of stimuli under these conditions is transmitted by the majority of apparently saturated cochlear nerve fibres, but several possible mechanisms are discussed.     

The Sharpening of cochlear frequency selectivity in the normal and abnormal cochlea

In the normal (anaesthetized) animal cochlea, the frequency threshold curves for single primary fibres are up to an order of magnitude sharper than the analogous functions derived from various reported measurements of the basilar membrane amplitude of vibration. This enhanced neural frequency selectivity is found in the same species and under conditions similar to those in which the mechanical measurements are taken. The sharpening process (at least near threshold) appears to be linear and is not dependent upon lateral inhibitory mechanisms. The variability of the neural frequency selectivity and its vulnerability to metabolic, chemical and pathological influences suggests the hypothesis that the sharpening is due to some form of ‘second filter’ subsequent to the relatively broadly tuned basilar membrane.

All fibres recorded from in the cochlear nerve in the normal cochlea show this enhanced frequency selectivity; in contrast, in pathological cochleas, all fibres, or a substantial proportion, have high-threshold, broadly tuned characteristics, approximating to those of the basilar membrane.

The frequency selectivity of normal cochlear fibres is adequate to account for the analogous psychophysical measures of hearing. It is proposed that loss of this normal frequency selectivity occurs in deafness of cochlear origin, accounting for widening of the critical band. A new hypothesis for recruitment is proposed on this basis.

Finally, invetigations of the cochlear nerve fibre frequency responses under conditions of hypoxia give grounds for the speculation that more than one mechanism is involved in the excitation of a single fibre, related to the separate functioning of the inner and outer hair cells.     

Physiological and psychophysical correlates of temporal processes in hearing

Discharges of auditory nerve fibers are synchronized to stimulus frequencies below 4-5 kHz. The phase-locking phenomenon has been studied in considerable detail in several animal species. Although strikingly close correspondences exist between phase-locking behavior in animals and human perceptual performance on certain tasks, there is still no clear evidence that the human brain actually bases perceptual decisions on temporally encoded frequency information. The alternative to temporal coding is rate-place coding, in which frequency is assigned on the basis of peaks in cochlear excitation patterns. This paper reviews pertinent physiological, psychophysical and modeling data in three classes of experiment whose results are explanable in terms of both rate-place and temporal processing of neural responses. The experiments deal with the pitch of complex tones, vowel identification, and pure-tone frequency discrimination. The data described here suggest that temporal models of frequency coding compete well with and in some cases offer a more parsimonious explanation of perceptual performance than rate-place codes do, particularly at low and middle frequencies. A potentially important implication of the analyses conducted here is that humans may not code frequency information in synchronized activity as well as other species. The data suggest that within limits the human ear is capable of using either temporal and rate-place frequency codes, and that the specific code employed by the perceptual processor is task-dependent.     

Review of the roles of temporal and place coding of frequency in speech discrimination.

Numerous studies have demonstrated that the frequency spectrum of sounds is represented in the neural code of single auditory nerve fibres both spatially and temporally, but few experiments have been designed to test which of these two representations of frequency is used in the discrimination of complex sounds such as speech and music. This paper reviews the roles of place and temporal coding of frequency in the nervous system as a basis for frequency discrimination of complex sounds such as those in speech. Animal studies based on frequency analysis in the cochlea have shown that the place code changes systematically as a function of sound intensity and therefore lacks the robustness required to explain pitch perception (in humans), which is nearly independent of sound intensity. Further indication that the place principle plays a minor role in discrimination of speech comes from observations that signs of impairment of the spectral analysis in the cochlea in some individuals are not associated with impairments in speech discrimination. The importance of temporal coding is supported by the observation that injuries to the auditory nerve, assumed to impair temporal coherence of the discharges of auditory nerve fibres, are associated with grave impairments in speech discrimination. These observations indicate that temporal coding of sounds is more important for discrimination of speech than place coding. The implications of these findings for the design of prostheses such as cochlear implants are discussed.     

Some aspects of temporal coding by single cochlear fibres from regions of cochlear hair cell degeneration in the guinea pig

Summary Some temporal coding properties of cochlear nerve fibres are investigated in kanamycin-treated guinea pigs (GPs) with various degrees of outer hair cell (OHC) degeneration. In particular, the phase locking ability of fibres from pathological cochleas, and also their adaptation properties are compared with the properties of normal cochlear fibres. No systematic effects of OHC loss on these properties have so far been found.These preliminary results therefore suggest (in so far as these animals can be regarded as models of sensorineural hearing loss of cochlear origin in man) that little deterioration should be expected in functions purely dependent upon faithful temporal coding of the stimulus waveform.     

Gamma-aminobutyric acidergic and glycinergic inputs shape coding of amplitude modulation in the chinchilla cochlear nucleus.

Amplitude modulation is a prominent acoustic feature of biologically relevant sounds, such as speech and animal vocalizations. Enhanced temporal coding of amplitude modulation signals is found in certain dorsal and posteroventral cochlear nucleus neurons when they are compared to auditory nerve. Although mechanisms underlying this improved temporal selectivity are not known, involvement of inhibition has been suggested. gamma-Aminobutyric acid- and glycine-mediated inhibition have been shown to shape the dorsal cochlear nucleus and posteroventral cochlear nucleus response properties to other acoustic stimuli. In the present study, responses to amplitude modulation tones were obtained from chinchilla dorsal cochlear nucleus and posteroventral cochlear nucleus neurons. The amplitude modulation carrier was set to the neuron's characteristic frequency and the modulating frequency varied from 10 Hz. Rate and temporal modulation transfer functions were compared across neurons. Bandpass temporal modulation transfer functions were observed in 74% of the neurons studied. Most cochlear nucleus neurons (90%) displayed flat or lowpass rate modulation transfer functions to amplitude modulation signals presented at 2540 dB (re: characteristic frequency threshold). The role of inhibition in shaping responses to amplitude modulation stimuli was examined using iontophoretic application of glycine or gamma-aminobutyric acidA receptor agonists and antagonists. Blockade of gamma-aminobutyric acidA or glycine receptors increased stimulus-evoked discharge rates for a majority of neurons tested. Synchronization to the envelope was reduced, particularly at low and middle modulating frequencies, with temporal modulation transfer functions becoming flattened and less bandpass in appearance. Application of glycine, gamma-aminobutyric acid or muscimol increased the modulation gain over the low- and mid-modulation frequencies and reduced the discharge rate across envelope frequencies for most neurons tested. These findings support the hypothesis that glycinergic and gamma-aminobutyric acidergic inputs onto certain dorsal cochlear nucleus and posteroventral cochlear nucleus neurons play a role in shaping responses to amplitude modulation stimuli and may be responsible for the reported preservation of amplitude modulation temporal coding in dorsal cochlear nucleus and posteroventral cochlear nucleus neurons at high stimulus intensities or in background noise.     

Temporal pitch in electric hearing

Both place and temporal codes in the peripheral auditory system contain pitch information, however, their actual use by the brain is unclear. Here pitch data are reported from users of the cochlear implant, which provides the ability to change the temporal code independently from the place code. With fixed electrode stimulation, both frequency discrimination and pitch estimate data show that the cochlear implant users can only discern differences in pitch for frequencies up to about 300 Hz. An integration model can predict pitch estimation from frequency discrimination, reinforcing Fechner's hypothesis relating sensation magnitude to stimulus discriminability. The present results suggest that 300 Hz is the upper boundary of the temporal code and that the absolute place information should be included in the present pitch models. They further suggest that future cochlear implants need to increase the number of independent electrodes to restore normal pitch range and resolution.     

Representation of voice pitch in discharge patterns of auditory-nerve fibers

Responses of populations of auditory-nerve fibers were measured for synthesized consonant-vowel stimuli. This paper explores the encoding of fundamental frequency (pitch) in these responses. Post-stimulus time (PST) histograms were computed from 25 ms segments of the spike trains. Discrete Fourier transforms with a 40 Hz resolution were computed from the histograms. Two representations of pitch are considered. The first representation is based on the pitch-related temporal properties of the speech signal. Histograms for individual units can show envelope modulations directly related to the pitch period. These modulations reflect the responses of these fibers to a number of stimulus harmonics near fiber CF. Responses of fibers near formant frequencies are dominated by a single large harmonic component, and thus show small or no pitch-related enveloped modulations. Envelope modulations are reduced in the presence of background noise. The second representation uses both temporal properties of auditory-nerve responses and cochlear place to encode the pitch-related harmonic structure of speech. As a measure of the response of the population of fibers to each harmonic of 40 Hz the magnitude of the component of the Fourier transform at that frequency was averaged across all fibers whose characteristic frequencies were within one-fourth octave of that harmonic. We call this measure the average localized synchronized rate (ALSR). The ALSR provides a good representation of stimulus spectrum, even in the presence of background noise. From the harmonic structure of the ALSR, we are able to extract the stimulus pitch frequency. The relationship of these two representations to pitch perception in both acoustic and electrical stimulation (via cochlear implants) is discussed.     

The sharpening of cochlear frequency selectivity in the normal and abnormal cochlea.

In the normal (anaesthetized) animal cochlea, the frequency threshold curves for single primary fibres are up to an order of magnitude sharper than the analogous function derived from various reported measurements of the basilar membrane amplitude of vibration. This enhanced neural frequency selectivity is found in the same species and under conditions similar to those in which the mechanical measurements are taken. The sharpening process (at least near threshold) appears to be linear and is not dependent upon lateral inhibitory mechanisms. The variability of the neural frequency selectivity and its vulnerability to metabolic, chemical and pathological influences suggests the hypothesis that the sharpening is due to some form of "second filter" subsequent to the relatively broadly tuned basilar membrane. All fibres recorded from in the cochlear nerve in the normal cochlea show this enhanced frequency selectivity; in contrast, in pathological cochleas, all fibres, or a substantial proportion, have high-threshold, broadly tuned characteristics, approximating to those of the basilar membrane.The frequency selectivity of normal cochlear fibres is adequate to account for the analogous psychophysical measures of hearing. It is proposed that loss of this normal frequency selectivity occurs in deafness of cochlear origin, accounting for widening of the critical band. A new hypothesis for recruitment is proposed on this basis.     

Encoding of alternating acoustical signals in the medial geniculate body of guinea pigs

In unanaesthetized guinea pigs 102 single units of the medial geniculate body were recorded under acoustical stimulation with alternating noise and tone impulses. The temporal parameters of the signals were chosen in close relation to psychoacoustical pulsation-threshold measurements. Most units showed a strong interaction between the responses of the non-simultaneously presented signal components (temporal suppression). The phasic part of each impulse-evoked response was more affected by the suppression than the tonic part. Thus, two regions of responsiveness could be verified: a region of pure tonic discharge and a region of tonic and phasic discharge. The borderline between both regions was defined as ‘on-threshold’.The temporal suppression effect of the discharge rate did depend on impulse duration, impulse shape, gap duration, and the levels of the signals components. The overall unit-response characteristic — especially the lack of temporal onset information — suggested a close relation between psychoacoustical pulsation threshold and physiological ‘on-threshold’.     

Indication of a relation between speech perception and temporal resolution for cochlear implantees.

In order to better understand the reasons for success or failure of a cochlear implant system for various patients, it appears necessary to analyze the patients' basic psychophysical capacities in relation to speech perception. Five patients with intracochlear multichannel Ineraid implants were studied in terms of their performance on temporal analysis in relation to their perception of consonants. For temporal analysis we measured the detection of a silent gap in noise and of an interval between two clicks. For consonant perception we established a confusion matrix based on 12 consonants presented in a vowel-consonant-vowel context using the vowel /a/. The results showed a correlation between temporal resolution for two successive clicks at the most basal cochlear electrode used, and the perception of place of articulation of consonants. This finding indicates that delivering fine temporal coding can be crucial for the success of an implant and that for a given subject, optimal capacity for temporal resolution may serve as a criterion for choosing a basal electrode.     

Digital speech processing for cochlear implants.

A rather general basic working hypothesis for cochlear implant research might be formulated as follows. Signal processing for cochlear implants should carefully select a subset of the total information contained in the sound signal and transform these elements into those physical stimulation parameters which can generate distinctive perceptions for the listener. Several new digital processing strategies have thus been implemented on a laboratory cochlear implant speech processor for the Nucleus 22-electrode system. One of the approaches (PES, pitch excited sampler) is based on the maximum peak channel vocoder concept whereby the spectral energy of a number of frequency bands is transformed into appropriate electrical stimulation parameters for up to 22 electrodes using a voice pitch synchronous pulse rate at any electrode. Another approach (CIS, continuous interleaved sampler) uses a maximally high pitch-independent stimulation pulse rate on a selected number of electrodes. As only one electrode can be stimulated at any instance of time, the rate of stimulation is limited by the required stimulus pulse widths (as determined individually for each subject) and some additional constraints and parameters which have to be optimized and fine tuned by psychophysical measurements. Evaluation experiments with 5 cochlear implant users resulted in significantly improved performance in consonant identification tests with the new processing strategies as compared with the subjects own wearable speech processors whereas improvements in vowel identification tasks were rarely observed. The pitch-synchronous coding (PES) resulted in worse performance compared to the coding without explicit pitch extraction (CIS).(ABSTRACT TRUNCATED AT 250 WORDS)     

Encoding of rapid amplitude fluctuations by cochlear-nerve fibres in the guinea-pig

Summary Responses of cochlear nerve fibres in the guinea-pig were measured to sinusoidally amplitude-modulated tones at fibre characteristic frequency. The modulation depth was ± 3 dB and the modulation rate was varied between 6.25 and 6400 Hz keeping the mean level of the tone constant. The resultant period histogram (locked to the modulation cycle) was used to determine the depth of modulated neural discharge. The functions showing the variation of discharge modulation with modulation frequency were, in general, low-pass. The cut-off of these functions appears to be primarily determined by the filtering properties of the fibres.Presented at the 18th Workshop on Inner Ear Biology in Montpellier/La Grande Motte, September 14–16, 1981     

Subcortical Neural Synchrony and Absolute Thresholds Predict Frequency Discrimination Independently

The neural mechanisms of pitch coding have been debated for more than a century. The two main mechanisms are coding based on the profiles of neural firing rates across auditory nerve fibers with different characteristic frequencies (place-rate coding), and coding based on the phase-locked temporal pattern of neural firing (temporal coding). Phase locking precision can be partly assessed by recording the frequency-following response (FFR), a scalp-recorded electrophysiological response that reflects synchronous activity in subcortical neurons. Although features of the FFR have been widely used as indices of pitch coding acuity, only a handful of studies have directly investigated the relation between the FFR and behavioral pitch judgments. Furthermore, the contribution of degraded neural synchrony (as indexed by the FFR) to the pitch perception impairments of older listeners and those with hearing loss is not well known. Here, the relation between the FFR and pure-tone frequency discrimination was investigated in listeners with a wide range of ages and absolute thresholds, to assess the respective contributions of subcortical neural synchrony and other age-related and hearing loss-related mechanisms to frequency discrimination performance. FFR measures of neural synchrony and absolute thresholds independently contributed to frequency discrimination performance. Age alone, i.e., once the effect of subcortical neural synchrony measures or absolute thresholds had been partialed out, did not contribute to frequency discrimination. Overall, the results suggest that frequency discrimination of pure tones may depend both on phase locking precision and on separate mechanisms affected in hearing loss.     

Some aspects of temporal coding by single cochlear fibres from regions of cochlear hair cell degeneration in the guinea pig.

Some temporal coding properties of cochlear nerve fibers are investigated in kanamycin-treated guinea pigs (GPs) with various degrees of outer hair cell (OHC) degeneration. In particular, the phase locking ability of fibres from pathological cochleas, and also their adaptation properties are compared with the properties of normal cochlear fibres. No systematic effects of OHC loss on these properties have so far been found. These preliminary results therefore suggest (in so far as these animals can be regarded as models of sensorineural hearing loss of cochlear origin in man) that little deterioration should be expected in functions purely dependent upon faithful temporal coding of the stimulus waveform.     

Neural temporal coding of low pitch. I. Human frequency-following responses to complex tones

The neural basis of low pitch was investigated in the present study by recording a brainstem potential from the scalp of human subjects during presentation of complex tones which evoke a variable sensation of pitch. The potential recorded, the frequency-following response (FFR), reflects the temporal discharge activity of auditory neurons in the upper brainstem pathway. It was used as an index of neural periodicity in order to determine the extent to which the low pitch of complex tones is encoded in the temporal discharge activity of auditory brainstem neurons. A tone composed of harmonics of a common fundamental produces a sensation of pitch equal to that of the 'missing' fundamental. Such signals generate brainstem potentials which are spectrally similar to FFR recorded in response to sinusoidal signals equal in frequency to the missing fundamental. Both types of signals generate FFR which are periodic, with a frequency similar to the perceived pitch of the stimuli. It is shown that the FFR to the missing fundamental is not the result of a distortion product by recording FFR to a complex signal in the presence of low-frequency bandpass noise. Neither is the FFR the result of neural synchronization to the waveform envelope modulation pattern. This was determined by recording FFR to inharmonic and quasi-frequency-modulated signals. It was also determined that the 'existence region' for FFR to the missing fundamental lies below 2 kHz and that the most favorable spectral region for FFR to complex tones is between 0.5 and 1.0 kHz. These results are consistent with the hypothesis that far-field-recorded FFR does reflect neural activity germane to the processing of low pitch and that such pitch-relevant activity is based on the temporal discharge patterns of neurons in the upper auditory brainstem pathway.     

A model proposing synaptic and extra-synaptic influences on the responses of cochlear nerve fibres

A unique property of sensory coding in the vertebrate auditory system is the existence of the classical form of excitatory centre-inhibitory surround in relative spike rate along the stimulus frequency dimension, in addition to a representation of temporal fine structure of high frequency periodic stimuli in the discharge pattern of primary afferent spike trains. We present a model which designates three factors that influence rate and temporal synchrony in spike responses; an excitatory factor, a suppressive factor and a synchronizing factor. The model proposes that an essential integration of bioelectric signals occurs in the primary afferent fibre. It is presumed that mean spike rate depends on mean level of membrane depolarization and synchronization depends on periodic modulation of membrane potential at the spike initiating zone. In the model, the excitatory factor is synaptically-mediated, excitatory post-synaptic potential (e.p.s.p.); the suppressive factor is negative DC polarization of the fibre membrane and the synchronizing factor is AC modulation of the fibre membrane potential. It is proposed that both the negatively-polarizing and high-frequency modulating signals are derived from extracellular current flow in the cochlea.     

Neural and Behavioral Sensitivity to Interaural Time Differences Using Amplitude Modulated Tones with Mismatched Carrier Frequencies

Bilateral cochlear implantation is intended to provide the advantages of binaural hearing, including sound localization and better speech recognition in noise. In most modern implants, temporal information is carried by the envelope of pulsatile stimulation, and thresholds to interaural time differences (ITDs) are generally high compared to those obtained in normal hearing observers. One factor thought to influence ITD sensitivity is the overlap of neural populations stimulated on each side. The present study investigated the effects of acoustically stimulating bilaterally mismatched neural populations in two related paradigms: rabbit neural recordings and human psychophysical testing. The neural coding of interaural envelope timing information was measured in recordings from neurons in the inferior colliculus of the unanesthetized rabbit. Binaural beat stimuli with a 1-Hz difference in modulation frequency were presented at the best modulation frequency and intensity as the carrier frequencies at each ear were varied. Some neurons encoded envelope ITDs with carrier frequency mismatches as great as several octaves. The synchronization strength was typically nonmonotonically related to intensity. Psychophysical data showed that human listeners could also make use of binaural envelope cues for carrier mismatches of up to 2–3 octaves. Thus, the physiological and psychophysical data were broadly consistent, and suggest that bilateral cochlear implants should provide information sufficient to detect envelope ITDs even in the face of bilateral mismatch in the neural populations responding to stimulation. However, the strongly nonmonotonic synchronization to envelope ITDs suggests that the limited dynamic range with electrical stimulation may be an important consideration for ITD encoding.     

Forward Masking in the Amplitude-Modulation Domain for Tone Carriers: Psychophysical Results and Physiological Correlates

Wojtczak and Viemeister (J Acoust Soc Am 118:3198–3210, 2005) demonstrated forward masking in the amplitude-modulation (AM) domain. The present study examined whether this effect has correlates in physiological responses to AM at the level of the auditory midbrain. The human psychophysical experiment used 40-Hz, 100% AM (masker AM) that was imposed on a 5.5-kHz carrier during the first 150 ms of its duration. The masker AM was followed by a 50-ms burst of AM of the same rate (signal AM) imposed on the same (uninterrupted) carrier, either immediately after the masker or with a delay. In the physiological experiment, single-unit extracellular recordings in the awake rabbit inferior colliculus (IC) were obtained for stimuli designed to be similar to the uninterrupted-carrier conditions used in the psychophysics. The masker AM was longer (500 ms compared with 150 ms in the psychophysical experiment), and the carrier and modulation rate were chosen based on each neuron’s audio- and envelope-frequency selectivity. Based on the average discharge rates of the responses or on the temporal correlation between neural responses to masked and unmasked stimuli, only a small subset of the population of IC cells exhibited suppression of signal AM following the masker. In contrast, changes in the discharge rates between the temporal segments of the carrier immediately preceding the signal AM and during the signal AM varied as a function of masker-signal delay with a trend that matched the psychophysical results. Unless the physiological observations were caused by species differences, they suggest that stages of processing higher than the IC must be considered to account for the AM-processing time constants measured perceptually in humans.     

Pitch perception and auditory stream segregation: implications for hearing loss and cochlear implants

Pitch is important for speech and music perception, and may also play a crucial role in our ability to segregate sounds that arrive from different sources. This article reviews some basic aspects of pitch coding in the normal auditory system and explores the implications for pitch perception in people with hearing impairments and cochlear implants. Data from normal-hearing listeners suggest that the low-frequency, low-numbered harmonics within complex tones are of prime importance in pitch perception and in the perceptual segregation of competing sounds. The poorer frequency selectivity experienced by many hearing-impaired listeners leads to less access to individual harmonics, and the coding schemes currently employed in cochlear implants provide little or no representation of individual harmonics. These deficits in the coding of harmonic sounds may underlie some of the difficulties experienced by people with hearing loss and cochlear implants, and may point to future areas where sound representation in auditory prostheses could be improved.