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1.  Coding of Electric Pulse Trains Presented through Cochlear Implants in the Auditory Midbrain of Awake Rabbit: Comparison with Anesthetized Preparations 
The Journal of Neuroscience  2014;34(1):218-231.
Cochlear implant (CI) listeners show limits at high frequencies in tasks involving temporal processing such as rate pitch and interaural time difference discrimination. Similar limits have been observed in neural responses to electric stimulation in animals with CI; however, the upper limit of temporal coding of electric pulse train stimuli in the inferior colliculus (IC) of anesthetized animals is lower than the perceptual limit. We hypothesize that the upper limit of temporal neural coding has been underestimated in previous studies due to the confound of anesthesia. To test this hypothesis, we developed a chronic, awake rabbit preparation for single-unit studies of IC neurons with electric stimulation through CI. Stimuli were periodic trains of biphasic pulses with rates varying from 20 to 1280 pulses per second. We found that IC neurons in awake rabbits showed higher spontaneous activity and greater sustained responses, both excitatory and suppressive, at high pulse rates. Maximum pulse rates that elicited synchronized responses were approximately two times higher in awake rabbits than in earlier studies with anesthetized animals. Here, we demonstrate directly that anesthesia is a major factor underlying these differences by monitoring the responses of single units in one rabbit before and after injection of an ultra-short-acting barbiturate. In general, the physiological rate limits of IC neurons in the awake rabbit are more consistent with the psychophysical limits in human CI subjects compared with limits from anesthetized animals.
PMCID: PMC3866485  PMID: 24381283
anesthesia; cochlear implant; inferior colliculus; temporal coding
2.  Congenital and Prolonged Adult-Onset Deafness Cause Distinct Degradations in Neural ITD Coding with Bilateral Cochlear Implants 
Bilateral cochlear implant (CI) users perform poorly on tasks involving interaural time differences (ITD), which are critical for sound localization and speech reception in noise by normal-hearing listeners. ITD perception with bilateral CI is influenced by age at onset of deafness and duration of deafness. We previously showed that ITD coding in the auditory midbrain is degraded in congenitally deaf white cats (DWC) compared to acutely deafened cats (ADC) with normal auditory development (Hancock et al., J. Neurosci, 30:14068). To determine the relative importance of early onset of deafness and prolonged duration of deafness for abnormal ITD coding in DWC, we recorded from single units in the inferior colliculus of cats deafened as adults 6 months prior to experimentation (long-term deafened cats, LTDC) and compared neural ITD coding between the three deafness models. The incidence of ITD-sensitive neurons was similar in both groups with normal auditory development (LTDC and ADC), but significantly diminished in DWC. In contrast, both groups that experienced prolonged deafness (LTDC and DWC) had broad distributions of best ITDs around the midline, unlike the more focused distributions biased toward contralateral-leading ITDs present in both ADC and normal-hearing animals. The lack of contralateral bias in LTDC and DWC results in reduced sensitivity to changes in ITD within the natural range. The finding that early onset of deafness more severely degrades neural ITD coding than prolonged duration of deafness argues for the importance of fitting deaf children with sound processors that provide reliable ITD cues at an early age.
PMCID: PMC3642270  PMID: 23462803
binaural hearing; congenital deafness; inferior colliculus; cochlear implants; ITD
3.  Decoding Sound Source Location and Separation Using Neural Population Activity Patterns 
The Journal of Neuroscience  2013;33(40):15837-15847.
The strategies by which the central nervous system decodes the properties of sensory stimuli, such as sound source location, from the responses of a population of neurons are a matter of debate. We show, using the average firing rates of neurons in the inferior colliculus (IC) of awake rabbits, that prevailing decoding models of sound localization (summed population activity and the population vector) fail to localize sources accurately due to heterogeneity in azimuth tuning across the population. In contrast, a maximum-likelihood decoder operating on the pattern of activity across the population of neurons in one IC accurately localized sound sources in the contralateral hemifield, consistent with lesion studies, and did so with a precision consistent with rabbit psychophysical performance. The pattern decoder also predicts behavior in response to incongruent localization cues consistent with the long-standing “duplex” theory of sound localization. We further show that the pattern decoder accurately distinguishes two concurrent, spatially separated sources from a single source, consistent with human behavior. Decoder detection of small amounts of source separation directly in front is due to neural sensitivity to the interaural decorrelation of sound, at both low and high frequencies. The distinct patterns of IC activity between single and separated sound sources thereby provide a neural correlate for the ability to segregate and localize sources in everyday, multisource environments.
PMCID: PMC3787502  PMID: 24089491
4.  Better Temporal Neural Coding with Cochlear Implants in Awake Animals 
Both the performance of cochlear implant (CI) listeners and the responses of auditory neurons show limits in temporal processing at high frequencies. However, the upper limit of temporal coding of pulse train stimuli in the inferior colliculus (IC) of anesthetized animals appears to be lower than that observed in corresponding perceptual tasks. We hypothesize that the neural rate limits have been underestimated due to the effect of anesthesia. To test this hypothesis, we developed a chronic, awake rabbit preparation for recording responses of single IC neurons to CI stimulation without the confound of anesthesia, and compared these data with earlier recordings from the IC of anesthetized cats. Stimuli were periodic trains of biphasic pulses with rates varying from 20 to 1280 pulses per second (pps). We found that the maximum pulse rates that elicited sustained firing and phase-locked responses were 2–3 times higher in the IC of awake rabbits than in anesthetized cats. Moreover, about 25% of IC neurons in awake rabbit showed sustained responses to periodic pulse trains at much higher pulse rates (> 1000 pps) than observed in anesthetized animals. Similar differences were observed in single units whose responses to pulse trains were monitored while the animal was given an injection of an ultra short-acting anesthetic. In general, the physiological rate limits of IC neurons in awake rabbit are more consistent with the psychophysical limits in human CI subjects compared to the data from anesthetized animals.
PMCID: PMC3726256  PMID: 23716241
cochlear implants; temporal coding; inferior colliculus; anesthesia
5.  Neural correlates of the perception of sound source separation 
As two sound sources become spatially separated in the horizontal plane, the binaural cues used for sound localization become distorted from their values for each sound in isolation. Because firing rates of most neurons in the inferior colliculus (IC) are sensitive to these binaural cues, we hypothesized that these neurons would be sensitive to source separation. We examined changes in the target azimuth tuning functions of IC neurons in unanesthetized rabbits caused by the concurrent presentation of an interferer at a fixed spatial location. Both target and interferer were broadband noise bursts, uncorrelated with each other. Signal detection analysis of firing rates of individual IC neurons shows that responses are correlated with psychophysical performance on segregation of spatially-separated sources. The analysis also highlights the role of neural sensitivity to interaural time differences of cochlea-induced envelopes in performing this task. Psychophysical performance on source segregation was also compared to the performance of two contrasting maximum-likelihood classifiers operating on the firing rates of the population of IC neurons. The “population-pattern” classifier had access to the firing rates of every neuron in the population, while the “two-channel” classifier operated on the summed firing rates from each side of the brain. Unlike the two-channel classifier, the population-pattern classifier could segregate the sources accurately, suggesting that some of the information contained in the heterogeneity of azimuth tuning functions across IC neurons is used to segregate sources.
PMCID: PMC3729225  PMID: 23716231
interaural time difference; interaural level difference; interaural correlation; sound localization; neural decoding; inferior colliculus; rabbit
6.  A point process model for auditory neurons considering both their intrinsic dynamics and the spectro-temporal properties of an extrinsic signal 
We propose a point process model of spiking activity from auditory neurons. The model takes account of the neuron’s intrinsic dynamics as well as the spectro-temporal properties of an input stimulus. A discrete Volterra expansion is used to derive the form of the conditional intensity function. The Volterra expansion models the neuron’s baseline spike rate, its intrinsic dynamics - spiking history - and the stimulus effect which in this case is the analog of the spectro-temporal receptive field (STRF). We performed the model fitting efficiently in a generalized linear model framework using ridge regression to address properly this ill-posed maximum likelihood estimation problem. The model provides an excellent fit to spiking activity from 55 auditory nerve neurons. The STRF-like representation estimated jointly with the neuron’s intrinsic dynamics may offer more accurate characterizations of neural activity in the auditory system than current ones based solely on the STRF.
PMCID: PMC3118674  PMID: 21317068
Spike train model; point process; spectro-temporal receptive field; generalized linear model; auditory system
7.  Neural coding of ITD with bilateral cochlear implants: Effects of congenital deafness 
Human bilateral cochlear implant users do poorly on tasks involving interaural time differences (ITD), a cue which provides important benefits to the normal hearing, especially in challenging acoustic environments. Yet the precision of neural ITD coding in acutely-deafened, bilaterally-implanted cats is essentially normal (Smith and Delgutte, J. Neurosci. 27:6740–6750). One explanation for this discrepancy is that the extended periods of binaural deprivation typically experienced by cochlear implant users degrades neural ITD sensitivity, either by impeding normal maturation of the neural circuitry or by altering it later in life. To test this hypothesis, we recorded from single units in inferior colliculus (IC) of two groups of bilaterally-implanted, anesthetized cats that contrast maximally in binaural experience: acutely-deafened cats, which had normal binaural hearing until experimentation, and congenitally deaf white cats, which received no auditory inputs until the experiment. Rate responses of only half as many neurons showed significant ITD sensitivity to low-rate pulse trains in congenitally deaf cats compared to acutely deafened cats. For neurons that were ITD sensitive, ITD tuning was broader and best ITDs were more variable in congenitally deaf cats, leading to poorer ITD coding within the naturally-occurring range. A signal detection model constrained by the observed physiology supports the idea that the degraded neural ITD coding resulting from deprivation of binaural experience contributes to poor ITD discrimination by human implantees.
PMCID: PMC3025489  PMID: 20962228
binaural hearing; electric stimulation; congenital deafness; cochlear implant; inferior colliculus; ITD
8.  Spatio-Temporal Representation of the Pitch of Harmonic Complex Tones in the Auditory Nerve 
The pitch of harmonic complex tones plays an important role in speech and music perception and the analysis of auditory scenes, yet traditional rate-place and temporal models for pitch processing provide only an incomplete description of the psychophysical data. In order to test physiologically a model based on spatio-temporal pitch cues created by the cochlear traveling wave (Shamma, J Acoust Soc Am 78: 1622–1632), we recorded from single fibers in the auditory nerve of anesthetized cat in response to harmonic complex tones with missing fundamentals and equal-amplitude harmonics. We used the principle of scaling invariance in cochlear mechanics to infer the spatiotemporal response pattern to a given stimulus from a series of measurements made in a single fiber as a function of fundamental frequency F0. We found that spatio-temporal cues to resolved harmonics are available for F0s between 350 Hz and 1100 Hz and that these cues are more robust than traditional rate-place cues at high stimulus levels. The lower F0-limit is determined by the limited frequency selectivity of the cochlea, while the upper limit is caused by the degradation of phase-locking to the stimulus fine structure at high frequencies. The spatio-temporal representation is consistent with the upper F0-limit to the perception of the pitch of complex tones with a missing fundamental, and its effectiveness does not depend on the relative phase between resolved harmonics. The spatio-temporal representation is thus consistent with key trends in human psychophysics.
PMCID: PMC2957107  PMID: 20861376
pitch; harmonic complex tone; spatio-temporal coding; rate coding; cochlear scaling invariance; auditory nerve; resolved harmonics
9.  Effects of reverberation on the directional sensitivity of auditory neurons across the tonotopic axis: Influences of ITD and ILD 
In reverberant environments, acoustic reflections interfere with the direct sound arriving at a listener’s ears, distorting the binaural cues for sound localization. We investigated the effects of reverberation on the directional sensitivity of single neurons in the inferior colliculus (IC) of unanesthetized rabbits. We find that reverberation degrades the directional sensitivity of single neurons, although the amount of degradation depends on the characteristic frequency (CF) and the type of binaural cues available. When interaural time differences (ITD) are the only available directional cue, low-CF cells sensitive to ITD in the waveform fine time structure maintain better directional sensitivity in reverberation than high-CF cells sensitive to ITD in the envelope induced by cochlear filtering. On the other hand, when both ITD and interaural level difference (ILD) cues are available, directional sensitivity in reverberation is comparable throughout the tonotopic axis of the IC. This result suggests that, at high frequencies, ILDs provide better directional information than envelope ITDs, emphasizing the importance of the ILD-processing pathway for sound localization in reverberation.
PMCID: PMC2896784  PMID: 20534831
directional sensitivity; interaural level difference; inferior colliculus; interaural time difference; reverberation; sound localization
10.  Dynamic Range Adaptation to Sound Level Statistics in the Auditory Nerve 
The auditory system operates over a vast range of sound pressure levels (100–120 dB) with nearly constant discrimination ability across most of the range, well exceeding the dynamic range of most auditory neurons (20–40 dB). Dean et al. (Nat. Neurosci. 8:1684, 2005) have reported that the dynamic range of midbrain auditory neurons adapts to the distribution of sound levels in a continuous, dynamic stimulus by shifting towards the most frequently occurring level. Here we show that dynamic range adaptation, distinct from classic firing rate adaptation, also occurs in primary auditory neurons in anesthetized cats for tone and noise stimuli. Specifically, the range of sound levels over which firing rates of auditory-nerve (AN) fibers grows rapidly with level shifts nearly linearly with the most probable levels in a dynamic sound stimulus. This dynamic range adaptation was observed for fibers with all characteristic frequencies and spontaneous discharge rates. As in the midbrain, dynamic range adaptation improved the precision of level coding by the AN fiber population for the prevailing sound levels in the stimulus. However, dynamic range adaptation in the AN was weaker than in the midbrain, and not sufficient (0.25 dB/dB on average for broadband noise) to prevent a significant degradation of the precision of level coding by the AN population above 60 dB SPL. These findings suggest that adaptive processing of sound levels first occurs in the auditory periphery and is enhanced along the auditory pathway.
PMCID: PMC2774902  PMID: 19889991
dynamic range problem; rate-level function; adaptation; sound level statistics; intensity coding; anesthetized cat
11.  Accurate Sound Localization in Reverberant Environments is Mediated by Robust Encoding of Spatial Cues in the Auditory Midbrain 
Neuron  2009;62(1):123-134.
In reverberant environments, acoustic reflections interfere with the direct sound arriving at a listener’s ears, distorting the spatial cues for sound localization. Yet, human listeners have little difficulty localizing sounds in most settings. Because reverberant energy builds up over time, the source location is represented relatively faithfully during the early portion of a sound, but this representation becomes increasingly degraded later in the stimulus. We show that the directional sensitivity of single neurons in the auditory midbrain of anesthetized cats follows a similar time course, although onset dominance in temporal response patterns results in more robust directional sensitivity than expected, suggesting a simple mechanism for improving directional sensitivity in reverberation. In parallel behavioral experiments, we demonstrate that human lateralization judgments are consistent with predictions from a population rate model decoding the observed midbrain responses, suggesting a subcortical origin for robust sound localization in reverberant environments.
PMCID: PMC2693331  PMID: 19376072
12.  Pitch representations in the auditory nerve: Two concurrent complex tones 
Journal of neurophysiology  2008;100(3):1301-1319.
Pitch differences between concurrent sounds are important cues used in auditory scene analysis and also play a major role in music perception. To investigate the neural codes underlying these perceptual abilities, we recorded from single fibers in the cat auditory nerve in response to two concurrent harmonic complex tones with missing fundamentals and equal-amplitude harmonics. We investigated the efficacy of rate-place and interspike-interval codes to represent both pitches of the two tones, which had fundamental frequency (F0) ratios of 15/14 or 11/9. We relied on the principle of scaling invariance in cochlear mechanics to infer the spatiotemporal response patterns to a given stimulus from a series of measurements made in a single fiber as a function of F0. Templates created by a peripheral auditory model were used to estimate the F0s of double complex tones from the inferred distribution of firing rate along the tonotopic axis. This rate-place representation was accurate for F0s above about 900 Hz. Surprisingly, rate-based F0 estimates were accurate even when the two-tone mixture contained no resolved harmonics, so long as some harmonics were resolved prior to mixing. We also extended methods used previously for single complex tones to estimate the F0s of concurrent complex tones from interspike-interval distributions pooled over the tonotopic axis. The interval-based representation was accurate for F0s below about 900 Hz, where the two-tone mixture contained no resolved harmonics. Together, the rate-place and interval-based representations allow accurate pitch perception for concurrent sounds over the entire range of human voice and cat vocalizations.
PMCID: PMC2544468  PMID: 18632887
sound segregation; pitch; temporal coding; rate coding; cochlear scaling invariance
13.  Sensitivity of Inferior Colliculus Neurons to Interaural Time Differences in the Envelope Versus the Fine Structure With Bilateral Cochlear Implants 
Journal of neurophysiology  2008;99(5):2390-2407.
Bilateral cochlear implantation seeks to improve hearing by taking advantage of the binaural processing of the central auditory system. Cochlear implants typically encode sound in each spectral channel by amplitude modulating (AM) a fixed-rate pulse train, thus interaural time differences (ITD) are only delivered in the envelope. We investigated the ITD sensitivity of inferior colliculus (IC) neurons with sinusoidally AM pulse trains. ITD was introduced independently to the AM and/or carrier pulses to measure the relative efficacy of envelope and fine structure for delivering ITD information. We found that many IC cells are sensitive to ITD in both the envelope (ITDenv) and fine structure (ITDfs) for appropriate modulation frequencies and carrier rates. ITDenv sensitivity was generally similar to that seen in normal-hearing animals with AM tones. ITDenv tuning generally improved with increasing modulation frequency up to the maximum modulation frequency that elicited a sustained response in a neuron (tested ≤Hz). ITDfs sensitivity was present in about half the neurons for 1,000 pulse/s (pps) carriers and was nonexistent at 5,000 pps. The neurons that were sensitive to ITDfs at 1,000 pps were those that showed the best ITD sensitivity to low-rate pulse trains. Overall, the best ITD sensitivity was found for ITD contained in the fine structure of a moderate rate AM pulse train (1,000 pps). These results suggest that the interaural timing of current pulses should be accurately controlled in a bilateral cochlear implant processing strategy that provides salient ITD cues.
PMCID: PMC2570106  PMID: 18287556
14.  Response Properties of Neighboring Neurons in the Auditory Midbrain for Pure-Tone Stimulation: A Tetrode Study 
Journal of neurophysiology  2007;98(4):2058-2073.
The complex anatomical structure of the central nucleus of the inferior colliculus (ICC), the principal auditory nucleus in the midbrain, may provide the basis for functional organization of auditory information. To investigate this organization, we used tetrodes to record from neighboring neurons in the ICC of anesthetized cats and studied the similarity and difference among the responses of these neurons to pure-tone stimuli using widely used physiological characterizations. Consistent with the tonotopic arrangement of neurons in the ICC and reports of a threshold map, we found a high degree of correlation in the best frequencies (BFs) of neighboring neurons, which were mostly <3 kHz in our sample, and the pure-tone thresholds among neighboring neurons. However, width of frequency tuning, shapes of the frequency response areas, and temporal discharge patterns showed little or no correlation among neighboring neurons. Because the BF and threshold are measured at levels near the threshold and the characteristic frequency (CF), neighboring neurons may receive similar primary inputs tuned to their CF; however, at higher levels, additional inputs from other frequency channels may be recruited, introducing greater variability in the responses. There was also no correlation among neighboring neurons' sensitivity to interaural time differences (ITD) measured with binaural beats. However, the characteristic phases (CPs) of neighboring neurons revealed a significant correlation. Because the CP is related to the neural mechanisms generating the ITD sensitivity, this result is consistent with segregation of inputs to the ICC from the lateral and medial superior olives.
PMCID: PMC2065857  PMID: 17671101
15.  A possible neurophysiological basis of the octave enlargement effect 
Although the physical octave is defined as a simple ratio of 2:1, listeners prefer slightly greater octave ratios. Ohgushi [J. Acoust. Soc. Am. 73, 1694–1700 (1983)] suggested that a temporal model for octave matching would predict this octave enlargement effect because, in response to pure tones, auditory-nerve interspike intervals are slightly larger than the stimulus period. In an effort to test Ohgushi’s hypothesis, auditory-nerve single-unit responses to pure-tone stimuli were collected from Dial-anesthetized cats. It was found that although interspike interval distributions show clear phase-locking to the stimulus, intervals systematically deviate from integer multiples of the stimulus period. Due to refractory effects, intervals smaller than 5 msec are slightly larger than the stimulus period and deviate most for small intervals. On the other hand, first-order intervals are smaller than the stimulus period for stimulus frequencies less than 500 Hz. It is shown that this deviation is the combined effect of phase-locking and multiple spikes within one stimulus period. A model for octave matching was implemented which compares frequency estimates of two tones based on their interspike interval distributions. The model quantitatively predicts the octave enlargement effect. These results are consistent with the idea that musical pitch is derived from auditory-nerve interspike interval distributions.
PMCID: PMC2346780  PMID: 10573885
16.  Mathematical Models of Cochlear Nucleus Onset Neurons: I. Point Neuron with Many Weak Synaptic Inputs 
The cochlear nucleus (CN) presents a unique opportunity for quantitatively studying input-output transformations by neurons because it gives rise to a variety of different response types from a relatively homogeneous input source, the auditory nerve (AN). Particularly interesting among CN neurons are Onset (On) neurons, which have a prominent response to the onset of sustained sounds followed by little or no response in the steady-state. On neurons contrast sharply with their AN inputs, which respond vigorously throughout stimuli. On neurons can entrain to stimuli (firing once per cycle of a periodic stimulus) at up to 1000 Hz, unlike their AN inputs. To understand the mechanisms underlying these response patterns, we tested whether an integrate-to-threshold point-neuron model with a fixed refractory period can account for On discharge patterns for tones, systematically examining the effect of membrane time constant and the number and strength of the exclusively excitatory AN synaptic inputs. To produce both onset responses to high-frequency tone bursts and entrainment to a broad range of low-frequency tones, the model must have a short time constant (≈0.125 ms) and a large number (>100) of weak synaptic inputs, properties that are consistent with the electrical properties and anatomy of On-responding cells. With these parameters, the model acts like a coincidence detector with a threshold-like relationship between the instantaneous discharge rates of the output and the inputs. Onset responses to high-frequency tone bursts result because the threshold effect enhances the initial response of the AN inputs and suppresses their relatively lower sustained response. However, when the model entrains across a broad range of frequencies, it also produces short interspike intervals at the onset of high-frequency tone bursts, a response pattern not found in all types of On neurons. These results show a tradeoff, that may be a general property of many neurons, between following rapid stimulus fluctuations and responding without short interspike intervals at the onset of sustained stimuli.
PMCID: PMC2280068  PMID: 12435925
integrate-and-fire model; coincidence detection; cochlear nucleus
17.  Auditory nerve fiber responses to electric stimulation: Modulated and unmodulated pulse trainsa 
Many modern cochlear implants use sound processing strategies that stimulate the cochlea with modulated pulse trains. Rubinstein et al. [Hear. Res. 127, 108 (1999)] suggested that representation of the modulator in auditory nerve responses might be improved by the addition of a sustained, high-rate, desynchronizing pulse train (DPT). In addition, activity in response to the DPT may mimic the spontaneous activity (SA) in a healthy ear. The goals of this study were to compare responses of auditory nerve fibers in acutely deafened, anesthetized cats elicited by high-rate electric pulse trains delivered through an intracochlear electrode with SA, and to measure responses of these fibers to amplitude-modulated pulse trains superimposed upon a DPT. Responses to pulse trains showed variability from presentation to presentation, but differed from SA in the shape of the envelope of the interval histogram (IH) for pulse rates above 4.8 kpps (kilo pulses per second). These IHs had a prominent mode near 5 ms that was followed by a long tail. Responses to modulated biphasic pulse trains resembled responses to tones in intact ears for small (<10%) modulation depths, suggesting that acousticlike responses to sinusoidal stimuli might be obtained with a DPT. However, realistic responses were only observed over a narrow range of levels and modulation depths. Improved coding of complex stimulus waveforms may be achieved by signal processing strategies for cochlear implants that properly incorporate a DPT.
PMCID: PMC2275322  PMID: 11508961
18.  Improved neural representation of vowels in electric stimulation using desynchronizing pulse trainsa) 
Current cochlear implant processors poorly represent sound waveforms in the temporal discharge patterns of auditory-nerve fibers (ANFs). A previous study [Litvak et al., J. Acoust. Soc. Am. 114, 2079–2098 (2003)] showed that the temporal representation of sinusoidal stimuli can be improved in a majority of ANFs by encoding the stimuli as small modulations of a sustained, high-rate (5 kpps), desynchronizing pulse train (DPT). Here, these findings are extended to more complex stimuli by recording ANF responses to pulse trains modulated by bandpass filtered vowels. Responses to vowel modulators depended strongly on the discharge pattern evoked by the unmodulated DPT. ANFs that gave sustained responses to the DPT had period histograms that resembled the modulator waveform for low (<5%) modulation depths. Spectra of period histograms contained peaks near the formant frequencies. In contrast, ANFs that gave a transient (<1 min) response to the DPT poorly represented the formant frequencies. A model incorporating a linear modulation filter, a noisy threshold, and neural refractoriness predicts the shapes of period histograms for both types of fibers. These results suggest that a DPT-enhanced strategy may achieve good representation of the stimulus fine structure in the temporal discharge patterns of ANFs for frequencies up to 1000 Hz. It remains to be seen whether these temporal discharge patterns can be utilized by cochlear implant subjects.
PMCID: PMC2275169  PMID: 14587608
19.  Desynchronization of electrically evoked auditory-nerve activity by high-frequency pulse trains of long durationa) 
Rubinstein et al. [Hear. Res. 127, 108–118 (1999)] suggested that the neural representation of the waveforms of electric stimuli might be improved by introducing an ongoing, high-rate, desynchronizing pulse train (DPT). A DPT may desynchronize neural responses to electric stimulation in a manner similar to spontaneous activity in a healthy ear. To test this hypothesis, responses of auditory-nerve fibers (ANFs) to 10-min-long electric pulse trains (5 kpps) were recorded from acutely deafened, anesthetized cats. Stimuli were delivered via an intracochlear electrode, and their amplitude was chosen to elicit a response in most ANFs. Responses to pulse trains showed pronounced adaptation during the first 1–2 min, followed by either a sustained response or cessation of spike discharges for the remainder of the stimulus. The adapted discharge rates showed a broad distribution across the ANF population like spontaneous activity. However, a higher proportion of fibers (46%) responded to the DPT at rates below 5 spikes/s than for spontaneous activity, and 12% of the fibers responded at higher rates than any spontaneously active fiber. Interspike interval histograms of sustained responses for some fibers had Poisson-like (exponential) shapes, resembling spontaneous activity, while others exhibited preferred intervals and, occasionally, bursting. Simultaneous recordings from pairs of fibers revealed no evidence of correlated activity, suggesting that the DPT does desynchronize the auditory nerve activity. Overall, these results suggest that responses to an ongoing DPT resemble spontaneous activity in a normal ear for a substantial fraction of the ANFs.
PMCID: PMC2270484  PMID: 14587606
20.  Improved temporal coding of sinusoids in electric stimulation of the auditory nerve using desynchronizing pulse trainsa) 
Rubinstein et al. [Hearing Res. 127, 108–118 (1999)] suggested that the representation of electric stimulus waveforms in the temporal discharge patterns of auditory-nerve fiber (ANF) might be improved by introducing an ongoing, high-rate, desynchronizing pulse train (DPT). To test this hypothesis, activity of ANFs was studied in acutely deafened, anesthetized cats in response to 10-min-long, 5-kpps electric pulse trains that were sinusoidally modulated for 400 ms every second. Two classes of responses to sinusoidal modulations of the DPT were observed. Fibers that only responded transiently to the unmodulated DPT showed hyper synchronization and narrow dynamic ranges to sinusoidal modulators, much as responses to electric sinusoids presented without a DPT. In contrast, fibers that exhibited sustained responses to the DPT were sensitive to modulation depths as low as 0.25% for a modulation frequency of 417 Hz. Over a 20-dB range of modulation depths, responses of these fibers resembled responses to tones in a healthy ear in both discharge rate and synchronization index. This range is much wider than the dynamic range typically found with electrical stimulation without a DPT, and comparable to the dynamic range for acoustic stimulation. These results suggest that a stimulation strategy that uses small signals superimposed upon a large DPT to encode sounds may evoke temporal discharge patterns in some ANFs that resemble responses to sound in a healthy ear.
PMCID: PMC2270483  PMID: 14587607
21.  Mathematical Models of Cochlear Nucleus Onset Neurons: II. Model with Dynamic Spike-Blocking State 
Onset (On) neurons in the cochlear nucleus (CN), characterized by their prominent response to the onset followed by little or no response to the steady-state of sustained stimuli, have a remarkable ability to entrain (firing 1 spike per cycle of a periodic stimulus) to low-frequency tones up to 1000 Hz. In this article, we present a point-neuron model with independent, excitatory auditory-nerve (AN) inputs that accounts for the ability of On neurons to both produce onset responses for high-frequency tone bursts and entrain to a wide range of low-frequency tones. With a fixed-duration spike-blocking state after a spike (an absolute refractory period), the model produces entrainment to a broad range of low-frequency tones and an On response with short interspike intervals (chopping) for high-frequency tone bursts. To produce On response patterns with no chopping, we introduce a novel, more complex, active membrane model in which the spike-blocking state is maintained until the instantaneous membrane voltage falls below a transition voltage. During the sustained depolarization for a high-frequency tone burst, the new model does not chop because it enters a spike-blocking state after the first spike and fails to leave this state until the membrane voltage returns toward rest at the end of the stimulus. The model entrains to low-frequency tones because the membrane voltage falls below the transition voltage on every cycle when the AN inputs are phase-locked. With the complex membrane model, On response patterns having moderate steady-state activity for high-frequency tone bursts (On-L) are distinguished from those having no steady-state activity (On-I) by requiring fewer AN inputs. Voltage-gated ion channels found in On-responding neurons of the CN may underlie the hypothesized dynamic spike-blocking state. These results provide a mechanistic rationale for distinguishing between the different physiological classes of CN On neurons.
PMCID: PMC2270482  PMID: 12435926
refractory period; state-dependent spike discharge; voltage-gated ion channels; cochlear nucleus
22.  Chimaeric sounds reveal dichotomies in auditory perception 
Nature  2002;416(6876):87-90.
By Fourier's theorem1, signals can be decomposed into a sum of sinusoids of different frequencies. This is especially relevant for hearing, because the inner ear performs a form of mechanical Fourier transform by mapping frequencies along the length of the cochlear partition. An alternative signal decomposition, originated by Hilbert2, is to factor a signal into the product of a slowly varying envelope and a rapidly varying fine time structure. Neurons in the auditory brainstem3–6 sensitive to these features have been found in mammalian physiological studies. To investigate the relative perceptual importance of envelope and fine structure, we synthesized stimuli that we call ‘auditory chimaeras’, which have the envelope of one sound and the fine structure of another. Here we show that the envelope is most important for speech reception, and the fine structure is most important for pitch perception and sound localization. When the two features are in conflict, the sound of speech is heard at a location determined by the fine structure, but the words are identified according to the envelope. This finding reveals a possible acoustic basis for the hypothesized ‘what’ and ‘where’ pathways in the auditory cortex7–10.
PMCID: PMC2268248  PMID: 11882898
23.  Using Evoked Potentials to Match Interaural Electrode Pairs with Bilateral Cochlear Implants 
Bilateral cochlear implantation seeks to restore the advantages of binaural hearing to the profoundly deaf by providing binaural cues normally important for accurate sound localization and speech reception in noise. Psychophysical observations suggest that a key issue for the implementation of a successful binaural prosthesis is the ability to match the cochlear positions of stimulation channels in each ear. We used a cat model of bilateral cochlear implants with eight-electrode arrays implanted in each cochlea to develop and test a noninvasive method based on evoked potentials for matching interaural electrodes. The arrays allowed the cochlear location of stimulation to be independently varied in each ear. The binaural interaction component (BIC) of the electrically evoked auditory brainstem response (EABR) was used as an assay of binaural processing. BIC amplitude peaked for interaural electrode pairs at the same relative cochlear position and dropped with increasing cochlear separation in either direction. To test the hypothesis that BIC amplitude peaks when electrodes from the two sides activate maximally overlapping neural populations, we measured multiunit neural activity along the tonotopic gradient of the inferior colliculus (IC) with 16-channel recording probes and determined the spatial pattern of IC activation for each stimulating electrode. We found that the interaural electrode pairings that produced the best aligned IC activation patterns were also those that yielded maximum BIC amplitude. These results suggest that EABR measurements may provide a method for assigning frequency–channel mappings in bilateral implant recipients, such as pediatric patients, for which psychophysical measures of pitch ranking or binaural fusion are unavailable.
PMCID: PMC1907379  PMID: 17225976
binaural hearing; electric stimulation; neural prosthesis; cochlear implant; inferior colliculus
24.  Pitch of Complex Tones: Rate-Place and Interspike Interval Representations in the Auditory Nerve 
Journal of neurophysiology  2005;94(1):347-362.
Harmonic complex tones elicit a pitch sensation at their fundamental frequency (F0), even when their spectrum contains no energy at F0, a phenomenon known as “pitch of the missing fundamental.” The strength of this pitch percept depends upon the degree to which individual harmonics are spaced sufficiently apart to be “resolved” by the mechanical frequency analysis in the cochlea. We investigated the resolvability of harmonics of missing-fundamental complex tones in the auditory nerve (AN) of anesthetized cats at low and moderate stimulus levels and compared the effectiveness of two representations of pitch over a much wider range of F0s (110–3,520 Hz) than in previous studies. We found that individual harmonics are increasingly well resolved in rate responses of AN fibers as the characteristic frequency (CF) increases. We obtained rate-based estimates of pitch dependent upon harmonic resolvability by matching harmonic templates to profiles of average discharge rate against CF. These estimates were most accurate for F0s above 400–500 Hz, where harmonics were sufficiently resolved. We also derived pitch estimates from all-order interspike-interval distributions, pooled over our entire sample of fibers. Such interval-based pitch estimates, which are dependent on phase-locking to the harmonics, were accurate for F0s below 1,300 Hz, consistent with the upper limit of the pitch of the missing fundamental in humans. The two pitch representations are complementary with respect to the F0 range over which they are effective; however, neither is entirely satisfactory in accounting for human psychophysical data.
PMCID: PMC2094528  PMID: 15788522
25.  A Physiologically Based Model of Interaural Time Difference Discrimination 
Interaural time difference (ITD) is a cue to the location of sounds containing low frequencies and is represented in the inferior colliculus (IC) by cells that respond maximally at a particular best delay (BD). Previous studies have demonstrated that single ITD-sensitive cells contain sufficient information in their discharge patterns to account for ITD acuity on the midline (ITD = 0). If ITD discrimination were based on the activity of the most sensitive cell available (“lower envelope hypothesis”), then ITD acuity should be relatively constant as a function of ITD. In response to broadband noise, however, the ITD acuity of human listeners degrades as ITD increases. To account for these results, we hypothesize that pooling of information across neurons is an essential component of ITD discrimination. This report describes a neural pooling model of ITD discrimination based on the response properties of ITD-sensitive cells in the IC of anesthetized cats.
Rate versus ITD curves were fit with a cross-correlation model of ITD sensitivity, and the parameters were used to constrain a population model of ITD discrimination. The model accurately predicts ITD acuity as a function of ITD for broadband noise stimuli when responses are pooled across best frequency (BF). Furthermore, ITD tuning based solely on a system of internal delays is not sufficient to predict ITD acuity in response to 500 Hz tones, suggesting that acuity is likely refined by additional mechanisms. The physiological data confirms evidence from the guinea pig that BD varies systematically with BF, generalizing the observation across species.
PMCID: PMC2041891  PMID: 15306644
auditory; binaural; hearing; inferior colliculus; localization; psychophysics

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