Information Processing by Onset Neurons in the Cat Auditory Brainstem.

Octopus cells in the ventral cochlear nucleus (VCN) have been difficult to study because of the very features that distinguish them from other VCN neurons. We performed in vivo recordings in cats on well-isolated units, some of which were intracellularly labeled and histologically reconstructed. We found that responses to low-frequency tones with frequencies < 1 kHz reveal higher levels of neural synchrony and entrainment to the stimulus than the auditory nerve. In responses to higher frequency tones, the neural discharges occur mostly near the stimulus onset. These neurons also respond in a unique way to 100 % amplitude-modulated (AM) tones with discharges exhibiting a bandpass tuning. Responses to frequency-modulated sounds (FM) are unusual: Octopus cells react more vigorously during the ascending than the descending parts of the FM stimulus. We examined responses of neurons in the ventral nucleus of the lateral lemniscus (VNLL) whose discharges to tones and AM sounds are similar to octopus cells. Repeated stimulation with short tone pips of VCN and VNLL onset neurons evokes trains of action potentials with gradual shifts toward later times in their first spike latency. This behavior parallels short-term post-synaptic depression observed by other authors in in vitro VCN recordings of octopus cells. VCN and VNLL onset units in cats respond to frozen noise stimuli with gaps as narrow as 1 ms with a robust discharge near the stimulus onset following the gap. This finding suggests that VCN and VNLL onset cells play a role in gap detection, which is of great importance to speech perception.

Fast Waves at the Base of the Cochlea.

Georg von Békésy observed that the onset times of responses to brief-duration stimuli vary as a function of distance from the stapes, with basal regions starting to move earlier than apical ones. He noticed that the speed of signal propagation along the cochlea is slow when compared with the speed of sound in water. Fast traveling waves have been recorded in the cochlea, but their existence is interpreted as the result of an experiment artifact. Accounts of the timing of vibration onsets at the base of the cochlea generally agree with Békésy's results. Some authors, however, have argued that the measured delays are too short for consistency with Békésy's theory. To investigate the speed of the traveling wave at the base of the cochlea, we analyzed basilar membrane (BM) responses to clicks recorded at several locations in the base of the chinchilla cochlea. The initial component of the BM response matches remarkably well the initial component of the stapes response, after a 4-µs delay of the latter. A similar conclusion is reached by analyzing onset times of time-domain gain functions, which correspond to BM click responses normalized by middle-ear input. Our results suggest that BM responses to clicks arise from a combination of fast and slow traveling waves.

Response properties of cochlear nucleus neurons in monkeys.

Much of what is known about how the cochlear nuclei participate in mammalian hearing comes from studies of non-primate mammalian species. To determine to what extent the cochlear nuclei of primates resemble those of other mammalian orders, we have recorded responses to sound in three primate species: marmosets, cynomolgus macaques, and squirrel monkeys. These recordings show that the same types of temporal firing patterns are found in primates that have been described in other mammals. Responses to tones of neurons in the ventral cochlear nucleus have similar tuning, latencies, post-stimulus time and interspike interval histograms as those recorded in non-primate cochlear nucleus neurons. In the dorsal cochlear nucleus, too, responses were similar. From these results it is evident that insights gained from non-primate studies can be applied to the peripheral auditory system of primates.

Basilar membrane mechanics in the 6-9 kHz region of sensitive chinchilla cochleae.

The vibration of the basilar membrane in the 6-9 kHz region in the chinchilla cochlea has been studied using a displacement sensitive interferometer. Displacements of 0.7-1.4 nm at 0 dB sound pressure level have been obtained. At the characteristic frequency (CF), rate-of-growth (ROG) functions computed as the slope of input-output (IO) functions can be as low as 0.1 dB/dB. IO functions for frequencies > CF have ROGs near 0 dB/dB and can have notches characterized by both negative slopes and expansive ROGs, i.e., > 1 dB/dB. For frequencies < 0.6*CF, ROGs > 1.2 dB/dB were found. Cochlear gain is shown to be greater than 60 dB in sensitive preparations with a single cochlea having nearly 80 dB gain. The compressive nature of the cochlea remains at all levels though it is masked at frequencies > CF when the amplitude of a compression wave exceeds that of the traveling wave. The compression wave produces the plateau region of the mechanical response at high intensities and has a nearly constant phase versus frequency function implying a high velocity. The summation of the traveling and compression waves explains the occurrence of the notches in both the IO and iso-intensity functions. Vibration of the osseous spiral limbus may alter the drive to inner hair cells.

Mutual suppression in the 6 kHz region of sensitive chinchilla cochleae.

Basilar membrane (BM) vibration was measured using a displacement measuring interferometer for single-tone and two-tone suppression (2TS) paradigms in the 6-9 kHz region of sensitive chinchilla cochleae that had gains near or better than 60 dB. Based on prior studies of basilar membrane vibration, three significant differences remain between BM and auditory nerve (AN) 2TS responses: (1) suppression thresholds in the tail of tuning curves were much higher in BM than the auditory nerve (AN); (2) rates of suppression were significantly higher in AN than BM; and (3) the amplitude of vibration with low-frequency suppressors was always greater than the single-tone displacement rendering it impossible to explain 2TS rate suppression in the AN. The first two differences are eliminated by the results of the present study while the third remains. Suppression amplitudes greater than 40 dB and rates of suppression larger than 2.5 dB/dB were found for low-frequency suppressors. A correlation between both the gain and nonlinearity of the cochlea and 2TS properties indicates that when sensitive cochleae are studied. The third difference between BM and AN behavior could be strictly a function of the high-pass filter characteristic of the inner hair cells.

Distortion product otoacoustic emissions and basilar membrane vibration in the 6-9 kHz region of sensitive chinchilla cochleae.

Distortion product otoacoustic emissions (DPOAEs) and basilar membrane (BM) vibration were measured simultaneously in the 6-9 kHz region of chinchilla cochleae. BM-Input-Output functions in a two-tone paradigm behaved similarly to DPOAEs for the 2f1-f2 component, nonmonotonic growth with the intensity of the lower frequency primary and a notch in the functions around 60 dB SPL. Ripples in frequency functions occur in both BM and OAE curves as a function of the distortion frequency. Optimum f2/f1 ratios for DPOAE generation are near 1.2. The slope of phase curves indicates that for low f2f1(<1.1) the emission source is the place location while for f2f1>1.1 the relative constancy of the phase function suggests that the place is the nonlinear region of f2, i.e., the wave location. Magnitudes of the DPOAEs increase rapidly above 60 dB SPL suggesting a different source or mechanism at high levels. This is supported by the observation that the high level DPOAE and BM-DP responses remain for a considerable period postmortem.

Contributions of Aage Møller in the study of the cochlear nucleus.

At a time when little was known about processing in the auditory system, Aage Møller undertook an extensive investigation of the response properties of cochlear nucleus (CN) neurons. With an excellent background in physiological acoustics and a command of computational techniques he systematically explored neural tuning, rate-level functions, and receptive fields of CN neurons using microelectrode recordings. He chose to employ more natural stimuli than just pure tones and employed a variety of stimuli consisting of tones, clicks, noise, amplitude- and frequency-modulated signals to document both intensity and temporal response characteristics. The response to noise stimuli was quantified using linear systems analysis which was very innovative at that time. By choosing to perform the studies in the white rat rather than cat, he provided important comparative data on this first center of the central auditory system. Over a span of ten years he provided a significant body of observations of CN units properties that has rarely been equaled.

Effects of contrast between onsets of speech and other complex spectra.

Previous studies using speech and nonspeech analogs have shown that auditory mechanisms which serve to enhance spectral contrast contribute to perception of coarticulated speech for which spectral properties assimilate over time. In order to better understand the nature of contrastive auditory processes, a series of CV syllables varying acoustically in F2-onset frequency and perceptually from /ba/ to /da/ was identified following a variety of spectra including three-peak renditions of [e] and [o], one-peak simulations of only F2, and spectral complements of these spectra for which peaks are replaced with troughs. Results for three-versus one-peak (or trough) precursor spectra were practically indistinguishable, suggesting that effects were spectrally local and not dependent upon perception of precursors as speech. Effects of complementary (trough) spectra had complementary effects on perception of following stops; however, effects for spectral complements were particularly dependent upon the interval between precursor and CV onsets. Results from these studies cannot be explained by simple masking or adaptation of suppression. Instead, they provide evidence for the existence of processes that selectively enhance contrast between onset spectra of neighboring sounds, and these processes are relevant for perception of connected speech.

Responses to cochlear normalized speech stimuli in the auditory nerve of cat.

Previous studies of auditory-nerve fiber (ANF) representation of vowels in cats and rodents (chinchillas and guinea pigs) have shown that, at amplitudes typical for conversational speech (60-70 dB), neuronal firing rate as a function of characteristic frequency alone provides a poor representation of spectral prominences (e.g., formants) of speech sounds. However, ANF rate representations may not be as inadequate as they appear. Here, it is investigated whether some of this apparent inadequacy owes to the mismatch between animal and human cochlear characteristics. For all animal models tested in earlier studies, the basilar membrane is shorter and encompasses a broader range of frequencies than that of humans. In this study, a customized speech synthesizer was used to create a rendition of the vowel [E] with formant spacing and bandwidths that fit the cat cochlea in proportion to the human cochlea. In these vowels, the spectral envelope is matched to cochlear distance rather than to frequency. Recordings of responses to this cochlear normalized [E] in auditory-nerve fibers of cats demonstrate that rate-based encoding of vowel sounds is capable of distinguishing spectral prominences even at 70-80-dB SPL. When cochlear dimensions are taken into account, rate encoding in ANF appears more informative than was previously believed.