Excitation and suppression of primary auditory fibres in the pigeon

Spike potentials were recorded from single fibres in the auditory nerve of the pigeon. In fibres with recognizable responses to sound, spontaneous activity and properties of responses to tonal stimuli were studied in quiet background conditions. Mean spontaneous rate in the sample of fibres was 35 spikes/s. Tuning of spike response to tones was manifest as a single peak in rate at each sound pressure level (SPL) in the frequency-intensity plane. The majority of fibres showed only excitation of spike rate above spontaneous rate. Post stimulus time histograms (PSTs) in such cases were typical of excitatory responses, previously described in birds and mammals showing pronounced adaptation and post-stimulus suppression of spike rate. In most cases of excitation-only responses, however, slopes of rate functions depended on stimulus frequency. Close to characteristic frequency (CF), slopes tended to decrease with increasing SPL, whereas away from CF, slopes tended to increase with SPL. In a minority of excitation-only responses, slopes of rate functions were parallel. In some fibres, tones adjacent to the response area caused overt suppression of spontaneous firing. For these fibres, the slopes of rate functions were more-strongly frequency-dependent, being negative at low SPL when rate suppression occurred. Suppression of spontaneous activity at low SPL was non-monotonic and quite different from suppression of spike rate at stimulus intensities above rat saturation. In PSTs of suppressed spontaneous activity, rebound occurred at the termination of the tone. The results clarify previous observations of suppression of primary auditory responses in birds. We conclude that responses in the majority of auditory fibres in the pigeon are the product of opposing excitatory and suppressive influences in the cochlea, generated by single tones in quite.     

Timing of spike discharges in cat auditory cortex neurons: implications for encoding of stimulus periodicity

Neurons at more central stations in the central auditory pathway show progressively poorer responses to high-frequency stimulus periodicities. This has been attributed to the relatively poorer spike timing in forebrain auditory neurons. This study directly examined the timing of spikes evoked by brief tone pulses which were varied in peak level and repetition rate. The experiments revealed that at tone repetition rates which produced progressively poorer entrainment, the timing of spike discharges remained sufficiently precise to support entrained responses. The fact that responses were poor indicates that imprecision in spike timing may not be the only factor limiting the encoding of temporal frequency. The data are discussed in relation to evidence on the temporal tuning of central neurons seen in studies using continuous amplitude modulations.     

Electrical stimulation of the auditory nerve. III. Response initiation sites and temporal fine structure

Latency, temporal dispersion and input-output characteristics of auditory nerve fiber responses to electrical pulse trains in normal and chronically deafened cat ears were classified and tentatively associated with sites where activity is initiated. Spikes occurred in one or more of four discrete time ranges whose endpoints overlapped partially. A responses had latencies <0.44 ms, exhibited asymptotic temporal dispersion of 8–12 μs and possessed an average dynamic range of 1.2 dB for 200 pulses/s (pps) pulse trains. They likely originated from central processes of spiral ganglion cells. B₁ and B₂ responses (0.45–0.9 ms, 25–40 μs, 1.9 dB) likely stemmed from activity at myelinated and unmyelinated peripheral processes, respectively. C responses (0.9–1.2 ms, >100 μs) likely originated from direct stimulation of inner hair cells, and D responses (>1.1 ms, >100 μs, >8 dB) arose from propagating traveling waves possibly caused by electrically induced motion of outer hair cells. C and D responses were recorded only in acoustically responsive ears. Mean latencies of spikes in all time ranges usually decreased with intensity, and activity at two or even three discrete latencies was often observed in the same spike train. Latency shifts from one discrete time range to another often occurred as intensity increased. Some shifts could be attributed to responses to the opposite-polarity phase of the biphasic pulse. In these cases, temporal dispersion and dynamic range were approximately equal for activity at each latency. A second type of latency shift was also often observed, in which responses at each latency exhibited dissimilar temporal dispersion and dynamic range. This behavior was attributed to a centralward shift in the spike initiation site and it occurred for monophasic as well as biphasic signals. Several fibers exhibited dual latency activity with a 40–90 μs time difference between response peaks. This may have stemmed from spike initiation at nodes on either side of the cell body. Increasing the stimulus pulse rate to 800–1000 pps produced small increases in temporal dispersion and proportionate increases in asymptotic discharge rate and dynamic range, but thresholds did not improve and slopes of rate-intensity functions (in spikes/s/dB) did not change. Responses to high-rate stimuli also exhibited discrete latency increases when discharge rates exceeded 300–400 spikes/s. Spike by spike latencies in these cases depended strongly on the discharge history. Implications for high-rate speech processing strategies are discussed.     

Response Characteristics in the Apex of the Gerbil Cochlea Studied Through Auditory Nerve Recordings

In this study, we analyze the processing of low-frequency sounds in the cochlear apex through responses of auditory nerve fibers (ANFs) that innervate the apex. Single tones and irregularly spaced tone complexes were used to evoke ANF responses in Mongolian gerbil. The spike arrival times were analyzed in terms of phase locking, peripheral frequency selectivity, group delays, and the nonlinear effects of sound pressure level (SPL). Phase locking to single tones was similar to that in cat. Vector strength was maximal for stimulus frequencies around 500 Hz, decreased above 1 kHz, and became insignificant above 4 to 5 kHz. We used the responses to tone complexes to determine amplitude and phase curves of ANFs having a characteristic frequency (CF) below 5 kHz. With increasing CF, amplitude curves gradually changed from broadly tuned and asymmetric with a steep low-frequency flank to more sharply tuned and asymmetric with a steep high-frequency flank. Over the same CF range, phase curves gradually changed from a concave-upward shape to a concave-downward shape. Phase curves consisted of two or three approximately straight segments. Group delay was analyzed separately for these segments. Generally, the largest group delay was observed near CF. With increasing SPL, most amplitude curves broadened, sometimes accompanied by a downward shift of best frequency, and group delay changed along the entire range of stimulus frequencies. We observed considerable across-ANF variation in the effects of SPL on both amplitude and phase. Overall, our data suggest that mechanical responses in the apex of the cochlea are considerably nonlinear and that these nonlinearities are of a different character than those known from the base of the cochlea.     

Temporal response patterns of auditory nerve fibers to electrical stimulation in deafened squirrel monkeys

Electroneural response patterns of single auditory-nerve neurons were studied in aminoglycoside-deafened squirrel monkeys. The electrical stimuli were delivered through bipolar electrodes implanted in the scala tympani. The effects of pulse width, shape, frequency, and intensity on neural adaptation, phase locking, and spectral content were evaluated. Our results did not demonstrate the characteristic adaptation seen in auditory-nerve neurons in response to acoustic stimulation. Phase locking to a broad stimulus pulse (3200 microseconds/phase) was found to a very restricted phase angle of the electrical stimulus which was broader for square wave than for sine wave stimulation. The latency of the phase locked response varied inversely with stimulus intensity with greater variation for square wave stimulation than for sine wave stimulation. Auditory neurons were capable of a very high degree of phase locking to a 200-microseconds/phase pulse presented at 156 pulses per second (PPS) and to the first pulse of a 2500-Hz pulse burst. Phase locking was much poorer for the subsequent 200-microseconds/phase pulses comprising the 2500-Hz pulse burst where the neuron's response was determined by its relative recovery status. These findings can be explained by an interaction between the neuron's relative refractory status and its integration of charge over the stimulatory half cycle of the electrical stimulus. These two factors also appear to determine the interspike interval of the neural response. This interval decreased monotonically with increasing stimulus intensity. The neural spike rate (150-500 Hz) producing this interval increased with intensity and may be a source of periodicity information which the central auditory nervous system could interpret as pitch. This may account for the proportional relationship between pitch and stimulus intensity seen in some cochlear implant patients. Our study demonstrates that auditory-nerve neurons comply with basic neurophysiological principles in their responses to electrical stimulation. These principles should be incorporated into the cochlear prosthesis stimulator if more normal neural response patterns are desired in the cochlear prosthesis patient.     

A model of frequency discrimination with optimal processing of auditory nerve spike intervals

This paper investigates phase-lock coding of frequency in the auditory system. One objective with the current model was to construct an optimal central estimation mechanism able to extract frequency directly from spike trains. The model bases estimates of the stimulus frequency on inter-spike intervals of spike trains phase-locked to a pure tone stimulus. Phase-locking is the tendency of spikes to cluster around multiples of the stimulus period. It is assumed that these clusters have Gaussian distributions with variance that depends on the amount of phase-locking. Inter-spike intervals are then noisy measurements of the actual period of the stimulus waveform. The problem of estimating frequency from inter-spike intervals can be solved optimally with a Kalman filter. It is shown that the number of inter-spike intervals observed in the stimulus interval determines frequency discrimination at low frequencies, while the variance of spike clusters dominates at higher frequencies. Timing information in spike intervals is sufficient to account for human frequency discrimination performance up to 5000 Hz. When spikes are available on each stimulus cycle, the model can accurately predict frequency discrimination thresholds as a function of frequency, intensity and duration.     

Phase-locked responses to low frequency tones in the medial geniculate body

Over 2500 extracellular single unit recordings were obtained from the medial geniculate body (MGB) of cats anaesthetized with nitrous oxide. Three out of four units were activated by tone bursts, most of them presenting a transient ‘on’ response. Only about 10% of the units showed a sustained excitatory ‘through’ response. Some of these neurons, when activated by low-frequency tone bursts, had discharge synchronized with the phase of the tonal stimulus. Such phase-locked units were principally found in the pars lateralls, but also in the pars magnocellularis and pars ovoidea of the MGB. Significant phase-locking (vector strength R ? 0.5) was observed up to 1000 Hz. About 20% of all units, responding in a sustained fashion to tone bursts below that frequency, were phase-locked. Monaural stimulation led to a shift of the mean phase angle compared to that measured when the tone bursts were delivered simultaneously to both ears. Implications of these experimental results on the synaptic jitter and the information processing through the auditory pathways are discussed.     

Induced suppression in spike responses to tone-on-noise stimuli in the auditory nerve of the pigeon

Spike potentials were recorded from single, afferent fibres in the pigeon auditory nerve. Pure-tone stimuli were presented in quiet and in combination with wide band noise. Presented alone, tones produced tuned response areas; noise generally drove spike rate to well above the spontaneous rate measured in quiet. When presented in combination with noise, tones up to 75 dB SPL at frequencies far from the fibre's response area had no effect on the noise-driven spike rate. As the tone frequency was shifted towards the response area, from above or below CF, suppression of the noise-driven spike rate became stronger until the tone reached the edge of the response area. Suppression of the noise-driven rate was directly proportional to the level of the tone. Within the area of response to the tone, tone-driven spike rates generally were unchanged or variably decreased (occasionally slightly increased) by tone-on-noise stimulation, depending on the relation of the tone frequency to CF and the level of the tone relative to that of the noise. Tuning properties were unaffected. It is suggested that in the pigeon, the suppression of driven spike rate during presentation of combination stimuli, which is common to all fibres, depends on the same mechanism as the suppression of spontaneous firing by tones that is observed in a proportion of fibres (Temchin, A.N. (1988), J. Comp. Physiol. A 163, 99-115; Hill et al., (1989) Hear. Res. 39, 37-48).     

Relationship between tone burst discharge pattern and spontaneous firing rate of auditory nerve fibres in the guinea pig.

A detailed investigation was carried out of the response of single auditory nerve fibres in the guinea pig to tone bursts. Comparisons were made between the shapes of peri-stimulus-time histograms (PSTHs) of low and high characteristic frequency (CF) fibres grouped according to their spontaneous firing rates (SR). Both low and high CF fibres of high spontaneous rate (greater than 18 spikes/s) exhibited marked rapid adaptation in their PSTH's which became most pronounced at high stimulus intensities. The ratio of onset-to-adapted firing estimated from PSTH data in these fibres increased monotonically as a function of adapted firing rate. The behaviour of fibres with the lowest spontaneous rates (less than 0.5 spikes/s) was markedly different, particularly in fibres from low CF regions. In general, these low-SR fibres showed slower adaptation than high-SR fibres, and a less pronounced onset peak. This was most striking in low CF fibres. Furthermore, the ratio of onset-to-adapted firing rate tended to decrease with increasing stimulus intensity in both low and high CF fibres with low spontaneous firing rates. Low-SR fibres also showed the highest maximum discharge rates to tone burst stimuli. Fibres with medium spontaneous rates between 0.5 and 18 spikes/s displayed intermediate characteristics in their PSTH's. Recent data in the chinchilla (Relkin and Doucet, 1991), suggest that these differences may arise in part from differences in inter-stimulus recovery processes in the different spontaneous rate groups.     

Responses of inferior colliculus neurons to SAM tones located in inhibitory response areas

In order to examine the effect of inhibition on processing auditory temporal information, responses of single neurons in the inferior colliculus of the chinchilla to sinusoidally amplitude-modulated (SAM) tones alone and the presence of a steady-state tone were obtained. The carrier frequency of the SAM tone was either the characteristic frequency (CF) or a frequency in the inhibitory response area of a studied neuron. When the carrier frequency was set to the neuron’s CF, neurons responded in synchrony to the SAM-tone envelope, as expected. When the carrier frequency was set to a frequency at which pure tones produced inhibition, SAM tones elicited little or no response, also as expected. However, when the same SAM tone was paired with a pure tone whose frequency was set to the neuron’s CF, responses synchronized to the SAM tone envelope were obtained. These modulated responses were typically one-half cycle out-of-phase with the response to the SAM tone at CF, suggesting that they arose from cyclic inhibition and release from inhibition by the SAM tone. The results demonstrate that the representation of temporal information by inferior colliculus neurons is influenced by temporally-patterned inhibition arising from locations remote from CF.     

Neural coding of repetitive clicks in the medial geniculate body of cat

The activity of 418 medial geniculate body (MGB) units was studied in response to repetitive acoustic pulses in 35 nitrous oxide anaesthetized cats. The proportion of MGB neurons insensitive to repetitive clicks was close to 30%. On the basis of their pattern of discharge, the responsive units were divided into three categories. The majority of them (71%), classified as ‘lockers’, showed discharges precisely time-locked to the individual clicks of the train. A few units (8%), called ‘groupers’, had discharges loosely synchronized to low-rate repetitive clicks. When the spikes were not synchronized, the cell had transient or sustained responses for a limited frequency range and was classified as a ‘special responder’ (21%). Responses of ‘lockers’ were time-locked up to a limiting rate, which varied between 10 and 800 Hz; half of the ‘lockers’ had a limiting rate of locking equal to or higher than 100 Hz. The degree of entrainment, defined as the probability that each click evokes at least one spike, regularly decreases for increasing rates; on the other hand, the precision of locking increases with frequency. The time jitter observed at 100 Hz might be as small as 0.2 ms and was 1.2 ms on average. The population of ‘lockers’ can mark with precision the transients of complex sounds and has response properties still compatible with a temporal coding of the fundamental frequency of most animal vocalizations.     

Setting complex tasks to single units in the avian auditory forebrain. I: Processing of complex artificial stimuli.

In the auditory forebrain (field L) of the European starling (Sturnus vulgaris), single unit responses were recorded for a wide range of complex stimuli, comprising different forms of amplitude and frequency modulation. About two-third of the units locked to sinusoidal modulation regardless of whether frequency (SFM) or amplitude (SAM) was modulated. On average, however, frequency led to stronger synchronization. Both the proportion of phase locking and its mean strength showed a low-pass dependence on modulation frequency. The lower efficiency of amplitude modulation is also visible in unit responses when SAM is combined with (random) frequency modulation. For the assessment of response strength and its comparison across the tested repertoire of complex stimuli, a new index (REX) is introduced which primarily weighs similarity of the spike trains in identically repeated stimulus runs. Applied to a set of 311 field L neurons, also this approach discloses the two stimulus classes lacking frequency modulation (pure tone and SAM) as the least effective. A new measure for response latency, the Effective Response Delay (ERD), based on the spike-triggered analysis of responses to randomly frequency-modulated sounds (RFM), reflects physiological delays better than conventional latency. So, ERD correction of SAM and SFM Period Histograms allowed to disclose response effective stimulus ranges independent of modulation frequency.     

Human frequency-following response: representation of tonal sweeps

Auditory nerve single-unit population studies have demonstrated that phase locking plays a dominant role in the neural encoding of steady-state speech sounds. Recently, we have reported that the phase-locked activity underlying the human frequency-following response (FFR) could also encode the first two formants of several tonal approximations of steady-state vowels. Since auditory nerve single-unit population studies have also demonstrated that phase locking is used to represent time-varying speech-like sounds, it was reasoned that the phase-locked neural activity underlying the human FFR, likewise, is dynamic enough to represent time-varying sounds. FFRs to a rising and a falling tone were obtained from 8 normal-hearing adults at 95, 85, 75 and 65 dB nHL. Results clearly demonstrated that the human FFR does indeed follow the trajectory of the rising and falling tones. Also, amplitude changes in the FFR supported the view that neural phase locking decreases with increasing frequency. Finally, the relatively smaller FFR amplitude for the falling tone compared to its rising counterpart lends further support to the notion that rising tones produce greater neural synchrony than falling tones. These results indicate that the human FFR may be used to evaluate encoding of time-varying speech sounds like diphthongs and certain consonant-vowel syllables.     

The responses of single units in the inferior colliculus of the guinea pig to damped and ramped sinusoids

Temporal asymmetry can have a pronounced effect on the perception of a sinusoid. For instance, if a sinusoid is amplitude modulated by a decaying exponential that restarts every 50 ms, (a damped sinusoid) listeners report a two-component percept: a tonal component corresponding to the carrier and a drumming component corresponding to the envelope modulation period. When the amplitude modulation is reversed in time (a ramped sinusoid) the perception changes markedly; the tonal component increases while the drumming component decreases. The long-term Fourier energy spectra are identical for damped and ramped sinusoids with the same exponential half-life. Modelling studies suggest that this perceptual asymmetry must occur central to the peripheral stages of auditory processing (Patterson and Irino, 1998). To test this hypothesis, we have recorded the responses of single units in the inferior colliculus of the anaesthetised guinea pig. We divided single units into three groups: onset, on-sustained and sustained, based on their temporal adaptation properties to suprathreshold tone bursts at the unit's best frequency. The asymmetry observed in the neural responses of single units was quantified in two ways: a simple total spike count measure and a ratio of the tallest bin of the modulation period histogram to the total number of spikes. Responses were more diverse than those observed with similar stimuli in a previous study in the ventral cochlear nucleus (Pressnitzer et al., 2000). The main results were: (1) The shape of the responses of on-sustained units to ramped sinusoids resembled the shape of the responses to damped sinusoids. This is in contrast to the response shapes in the VCN, which were always similar to the stimulating sinusoid. (2) Units classified as onsets often responded only to the damped stimuli. (3) All units display significant asymmetry in discharge rate for at least one of the half-lives tested and 20% showed significant response asymmetry over all of the half-lives tested. (4) A summary population measure of temporal asymmetry based on total spike count reveals the same pattern of results as that obtained psychophysically using the same stimuli (Patterson, 1994a).     

Statistical Analyses of Temporal Information in Auditory Brainstem Responses to Tones in Noise: Correlation Index and Spike-distance Metric

Gai and Carney (J Neurophysiol 96:2451-2464, 2006) previously explored the detection of tones in noise based on responses in the anteroventral cochlear nucleus; that study focused on temporal information in discharge reliability and analyses of neural responses related to the fine structure or envelope of the stimulus. Two additional temporal approaches, the correlation index (Joris et al., Hearing Res 216-217:19-30, 2006) and the spike-distance metric (Victor and Purpura, J Neurophysiol 76:1310-1326, 1996; Netw Comput Neural Syst 8:127-164, 1997), are tested in the present study. Trends in the correlation index as a function of stimulus level are similar to those of the synchronization coefficient (also called the vector strength) when the tone is presented alone. However, the present study found that trends in the correlation index did not agree with those of the synchronization coefficient for tones presented with relatively high-level background noise. Instead, trends in the correlation index generally agreed with those of the temporal reliability metric discussed in Gai and Carney (J Neurophysiol 96:2451-2464, 2006); that is, the correlation index decreased with increased tone level in the presence of relatively high-level background noise. The spike-distance metric, which was based on absolute spike times or on interspike intervals, was compared to the temporal measures described above, which were generally based on relative spike times. The results confirm that the spike-distance metric is not an optimal temporal metric. In addition, absolute spike times of primary-like responses generally contained much less temporal information than absolute spike times of chopper response types. The present study highlights the importance of relative spike-timing information as characterized by traditional and novel temporal measures.     

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.     

Responses elicited from medial superior olivary neurons by stimuli associated with binaural masking and unmasking

The responses of binaural neurons of the medial superior olive were measured as a function of interaural temporal differences for tones and as a function of signal-to-noise ratio under homophasic and antiphasic masking conditions. The degree of neural response synchrony to the frequency of the signal was related to the degree of behavioral detectability of the signal in the homophasic, but not the antiphasic masking condition. For the antiphasic condition, a decrease in discharge rate resulted from the addition of the signal to the noise, similar to the decrease which occurred when interaural temporal differences were introduced in the tonal stimuli. The results are compatible with a model in which interaural temporal-difference information arriving over monaural afferents in the form of synchronized impulses is mapped into a place code by a neural coincidence-detection device. Several differences were noted between the responses to tones found in the present experiment and those reported by others. These differences were attributed mainly to differences among the experimental procedures in use among the various reporting laboratories.     

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.     

Auditory Cortical Images of Tones and Noise Bands

We examined the representation of stimulus center frequencies by the distribution of cortical activity. Recordings were made from the primary auditory cortex (area A1) of ketamine-anesthetized guinea pigs. Cortical images of tones and noise bands were visualized as the simultaneously recorded spike activity of neurons at 16 sites along the tonotopic gradient of cortical frequency representation. The cortical image of a pure tone showed a restricted focus of activity along the tonotopic gradient. As the stimulus frequency was increased, the location of the activation focus shifted from rostral to caudal. When cochlear activation was broadened by increasing the stimulus level or bandwidth, the cortical image broadened. An artificial neural network algorithm was used to quantify the accuracy of center-frequency representation by small populations of cortical neurons. The artificial neural network identified stimulus center frequency based on single-trial spike counts at as few as ten sites. The performance of the artificial neural network under various conditions of stimulus level and bandwidth suggests that the accuracy of representation of center frequency is largely insensitive to changes in the width of cortical images.