Mechanical bases of frequency tuning and neural excitation at the base of the cochlea: comparison of basilar-membrane vibrations and auditory-nerve-fiber responses in chinchilla.

We review the mechanical origin of auditory-nerve excitation, focusing on comparisons of the magnitudes and phases of basilar-membrane (BM) vibrations and auditory-nerve fiber responses to tones at a basal site of the chinchilla cochlea with characteristic frequency approximately 9 kHz located 3.5 mm from the oval window. At this location, characteristic frequency thresholds of fibers with high spontaneous activity correspond to magnitudes of BM displacement or velocity in the order of 1 nm or 50 microm/s. Over a wide range of stimulus frequencies, neural thresholds are not determined solely by BM displacement but rather by a function of both displacement and velocity. Near-threshold, auditory-nerve responses to low-frequency tones are synchronous with peak BM velocity toward scala tympani but at 80-90 dB sound pressure level (in decibels relative to 20 microPascals) and at 100-110 dB sound pressure level responses undergo two large phase shifts approaching 180 degrees. These drastic phase changes have no counterparts in BM vibrations. Thus, although at threshold levels the encoding of BM vibrations into spike trains appears to involve only relatively minor signal transformations, the polarity of auditory-nerve responses does not conform with traditional views of how BM vibrations are transmitted to the inner hair cells. The response polarity at threshold levels, as well as the intensity-dependent phase changes, apparently reflect micromechanical interactions between the organ of Corti, the tectorial membrane and the subtectorial fluid, and/or electrical and synaptic processes at the inner hair cells.

Frequency tuning of basilar membrane and auditory nerve fibers in the same cochleae.

Responses to tones of a basilar membrane site and of auditory nerve fibers innervating neighboring inner hair cells were recorded in the same cochleae in chinchillas. At near-threshold stimulus levels, the frequency tuning of auditory nerve fibers closely paralleled that of basilar membrane displacement modified by high-pass filtering, indicating that only relatively minor signal transformations intervene between mechanical vibration and auditory nerve excitation. This finding establishes that cochlear frequency selectivity in chinchillas (and probably in mammals in general) is fully expressed in the vibrations of the basilar membrane and renders unnecessary additional ("second") filters, such as those present in the hair cells of the cochleae of reptiles.

Low-frequency suppression of auditory nerve responses to characteristic frequency tones.

The effects of low-frequency (50, 100, 200 and 400 Hz) 'suppressor' tones on responses to moderate-level characteristic frequency (CF) tones were measured in chinchilla auditory nerve fibers. Two-tone interactions were evident at suppressor intensities of 70-100 dB SPL. In this range, the average response rate decreased as a function of increasing suppressor level and the instantaneous response rate was modulated periodically. At suppression threshold, the phase of suppression typically coincided with basilar membrane displacement toward scala tympani, regardless of CF. At higher suppressor levels, two suppression maxima coexisted, synchronous with peak basilar membrane displacement toward scala tympani and scala vestibuli. Modulation and rate-suppression thresholds did not vary as a function of spontaneous activity and were only minimally correlated with fiber sensitivity. Except for fibers with CF < 1 kHz, modulation and rate-suppression thresholds were lower than rate and phase-locking thresholds for the suppressor tones presented alone. In the case of high-CF fibers with low spontaneous activity, excitation thresholds could exceed suppression thresholds by more than 30 dB. The strength of modulation decreased systematically with increasing suppressor frequency. For a given suppressor frequency, modulation was strongest in high-CF fibers and weakest in low-CF fibers. The present findings strongly support the notion that low-frequency suppression in auditory nerve fibers largely reflects an underlying basilar membrane phenomenon closely related to compressive non-linearity.

Unusual discharge patterns of single fibers in the pigeon's auditory nerve.

Extracellular recording from single auditory nerve fibers in the pigeon, Columba livia, revealed some unusual discharge patterns of spontaneous and evoked activity. Time interval histograms (TIHs) of spontaneous activity showed a random interval distribution in 73% of the auditory fibers (Fig. 1a). The remaining 27% revealed periodicity in the TIHs (Fig. 1b-e), determined by the characteristic frequency (CF) of a given fiber. Normally, those fibers had a CF less than 2.2 kHz. In both cases spontaneous activity was irregular. The time pattern of quasiperiodic spontaneous firing in different auditory fibers is described by three main types of autocorrelation histograms (ACHs; decaying, nondecaying, and modulated), reflecting the spontaneous oscillations of the hair cell membrane potential (Fig. 1b-d). Single-tone suppression in auditory fibers with quasi-periodic spontaneous activity was found (Figs. 2, 10) and it could be observed if the eighth nerve was cut. There was no suppressive effect in fibres with random spontaneous firing. The frequency selectivity properties of auditory fibers were studied by means of an automatic method. Both 'simple' (Fig. 4) and 'complex' (Figs. 7, 8) response maps were found. Apart from the usual excitatory area, complex response maps were characterized by suppressive areas lying either above (Fig. 7), below (Fig. 8e), or on both sides of the CF (Fig. 8a-c). Generally, complex response maps were observed for fibers showing quasiperiodic spontaneous activity (Figs. 7, 8). Input-output functions at frequencies evoking single-tone suppression were nonmonotonic, while they were always monotonic at frequencies near the CF (Fig. 12). No difference in sharpness was observed between normal frequency threshold curves (FTCs) and excitatory areas of 'complex' response maps (Fig. 9). 'On-off' responses evoked by suppressive stimuli were found (Figs. 2, 3). They had a periodic pattern determined by the CF and did not depend on the stimulus frequency (Fig. 3). Low-CF fibers were observed which changed their time discharge structure to tone levels about 45 dB lower than their thresholds at the CF (Fig. 6). The observed features of the discharge patterns of the pigeon's auditory fibers reflect the distinctive nature of the fundamental mechanisms of auditory analysis in birds that are connected with electrical tuning of the hair cells and probably with the micromechanics of the bird's cochlea.

[Correlation of the electrical and mechanical resonance frequencies of the cochlear hair cells of the auditory nerve fibers in the pigeon]. / Sootnoshenie chastot élektricheskogo i mekhanicheskogo rezonansov voloskovykh kletok ulitki golubia v voloknakh slukhovogo nerva.

Base period (BP) of the quasi-periodical spontaneous activity and characteristic frequency (CF) were determined in 67 auditory fibres of pigeon: BP.CF = 1.02 +/- 0.08 (c.f. 10, 11). This evidences for the coincidence between the frequencies of electrical and mechanical resonances of hair cell. Active electric resonance in the cell membrane is evoked by the positive feedback between mechanoelectric and electromechanical transduction in the cochlear hair cell.

[Complex frequency-selective properties of the fibers of the acoustic nerve in the pigeon]. / Slozhnye chastotno-izbiratel'nye svoistva volokon slukhovogo nerva golubia.

Frequency-selectivity properties of 198 single auditory fibres in the pigeon were investigated by means of an automatic method. Spontaneous activity in 56 of them innervating hair cells with oscillatory membrane potential changes could be inhibited by single-frequency stimuli (one-tone inhibition). Inhibition areas lay above (45%), below (7%) or on both sides (48%) of their characteristic frequencies (CFs). Input-output functions at inhibitory frequencies were nonmonotonic, while they were always monotonic at best frequencies near CF. One-tone inhibition was not observed in the remaining 142 fibres. Analysis of mechanoelectric processes in hair cells during one-tone inhibition indicates their possible analogy with the well known two-tone effects.

[A system of automated measurement of frequency-amplitude characteristics of auditory neurons]. / Sistema avtomaticheskogo izmereniia chastotno-amplitudnykh svoistv nervnykh élementov slukhovoi sistemy.

The digital system for automatic measurement of frequency-amplitude and frequency-threshold characteristics of auditory neurons is described. A multi-channel analyser is utilized as a storage device.

[Spontaneous activity in the single auditory nerve fiber in the pigeon]. / Spontannaia aktivnost' v odinochnykh voloknakh slukhovogo nerva golubia.

Microelectrode study of spontaneous activity of the pigeon's single auditory nerve fibers and their interval histograms shows in some of them rhythmic oscillations of excitability with characteristic frequency. The existence of these oscillations is supported by the analysis of interval histograms and autocorrelation functions of spontaneous discharges. Stimulation of these fibers with white noise caused no changes of the periodicity of interval histograms and had no effect on their periods. These characteristics of single fibers could be attributed to rhythmic oscillations of the MP of hair cells arising as a result of the mechanical narrow-band filtration of ambient noises at the basilar membrane.