Bertrand Delgutte

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.

Two-tone rate suppression in auditory-nerve fibers: Dependence on suppressor frequency and level

The growth of two-tone rate suppression with suppressor level was studied for auditory-nerve fibers in anesthetized cats. The level of a tone at the characteristic frequency (CF) was adjusted by an adaptive procedure (PEST) so that, when presented with a suppressor tone, the CF tone would produce a criterion discharge rate. Suppression (in dB) was defined as the CF-tone level that met criterion in the presence of a suppressor minus the level that met criterion in quiet. The growth of suppression with suppressor level was well characterized by a straight line whose slope (in dB-excitor/dB-suppressor) varied with suppressor frequency by as much as a factor of 10 in the same fiber. These slope differences were systematically related to the position of the suppressor frequency relative to the fiber CF: for below-CF suppressors, slopes ranged from 1 to 3 dB/dB, while, for above-CF suppressors, they were between 0.15 and 0.7 dB/dB. Slopes decreased rapidly with increasing suppressor frequency near the CF, but, for frequencies well below the CF, the slope reached a maximum that increased gradually with CF. These results resemble psychophysical data on the growth of masking and psychophysical suppression, and pose difficulties for existing models of two-tone suppression.

Auditory nerve fiber responses to electric stimulation: Modulated and unmodulated pulse trains

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.

Speech coding in the auditory nerve: IV. Sounds with consonant‐like dynamic characteristics

Discharge patterns of auditory-nerve fibers in anesthetized cats were obtained for two stimulus levels in response to synthetic stimuli with dynamic characteristics appropriate for selected consonants. A set of stimuli was constructed by preceding a signal that was identified as /da/by another sound that was systematically manipulated so that the entire complex would sound like either /da/, /ada/, /na/, /sa/, /sa/, or others. Discharge rates of auditory-nerve fibers in response to the common /da/-like formant transitions depended on the preceding context. Average discharge rates during these transitions decreased most for fibers whose CFs were in frequency regions where the context had considerable energy. Some effect of the preceding context on fine time patterns of response to the transitions was also found, but the identity of the largest response components (which often corresponded to the formant frequencies) was in general unaffected. Thus the response patterns during the formant transitions contain cues about both the nature of the transitions and the preceding context. A second set of stimuli sounding like /s/ and /c/ was obtained by varying the duration of the rise in amplitude at the onset of a filtered noise burst. At both 45 and 60 dB SPL, there were fibers which showed a more prominent peak in discharge rate at stimulus onset for /c/ than for /s/, but the CF regions that reflected the clearest distinctions depended on stimulus level. The peaks in discharge rate that occur in response to rapid changes in amplitude or spectrum might be used by the central processor as pointers to portions of speech signals that are rich in phonetic information.

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. (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 toward 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.

Phase-locking of auditory-nerve discharges to sinusoidal electric stimulation of the cochlea

The activity of auditory-nerve fibers was recorded in anesthetized cats in response to sinusoidal electric stimuli applied through a bipolar electrode pair inserted about 5 mm into the cochlea through the round window. The synchronization index was calculated from period histograms for frequencies ranging from 0.2 to over 10 kHz. The stimulus artifact was largely eliminated through the use of differential micropipettes and an adaptive digital filter. Measured synchronization indices were many times larger than the indices that could be attributed to the residual stimulus artifact. Synchronization indices at each stimulus frequency varied considerably from fiber to fiber, even in the same animal. The dependence of synchrony on stimulus frequency was also variable, decreasing monotonically in some fibers and nonmonotonically in others. The average electric synchronization index for all fibers did not fall as steeply with frequency as does the average synchrony for acoustic stimuli. The finding of significant phase locking to electric stimuli well above 1 kHz suggests that the poor frequency discrimination of cochlear-implant recipients for single-channel stimulation above this frequency may be due to the inability of the central processor to make effective use of the available phase-locking information for monaural stimulation.

Physiological Models for Basic Auditory Percepts

Explaining auditory perceptual phenomena in terms of physiological mechanisms has a long tradition going back at least to von Helmholtz (1863), and possibly to as early as Pythagoras’ experiments on pitch and musical consonance (ca. 530 B.C.; see Cohen and Drabken 1948). In modern practice, such efforts take the form of computational models because these models help generate hypotheses that can be explicitly stated and quantitatively tested for complex systems. Relating physiology to behavior is perhaps the most direct route toward understanding how the auditory system works, because neither physiological nor perceptual data alone provide sufficient information: physiological studies cannot identify the function of the neural structures under investigation, while perceptual studies do not reveal the implementation of these functions. This endeavor is not only an intellectual challenge (Schouten’s “ever wondering mind”), it can also have practical value. Perceptual impairments such as difficulties in understanding speech may only yield to surgical and pharmacological cures if the problem is sufficiently well identified at the physiological level. Because any behavior such as speech perception involves a complex physiological system with many interacting components, it becomes essential to identify the roles of these various components in the behavior.

Desynchronization of electrically evoked auditory-nerve activity by high-frequency pulse trains of long duration

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.

Speech coding in the auditory nerve: III. Voiceless fricative consonants

Responses of auditory-nerve fibers in anesthetized cats were recorded for synthetic voiceless fricative consonants. The four stimuli (/x/, /s/, /s/, and /f/) were presented at two levels corresponding to speech in which the levels of the vowels would be approximately 60 and 75 dB SPL, respectively. Discharge patterns were characterized in terms of PST histograms and their power spectra. For both stimulus levels, frequency regions in which the stimuli had considerable energy corresponded well with characteristic-frequency (CF) regions in which average discharge rates were the highest. At the higher level, the profiles of discharge rate against CF were more distinctive for the stimulus onset than for the central portion. Power spectra of PST histograms had large response components near fiber characteristic frequencies for CFs up to 3-4 kHz, as well as low-frequency components for all fibers. The relative amplitudes of these components varied for the different stimuli. In general, the formant frequencies of the fricatives did not correspond with the largest response components, except for formants below about 3 kHz. Processing schemes based on fine time patterns of discharge that were effective for vowel stimuli generally failed to extract the formant frequencies of fricatives.

Improved temporal coding of sinusoids in electric stimulation of the auditory nerve using desynchronizing pulse trains.

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.