Mario A. Ruggero

Responses to sound of the basilar membrane of the mammalian cochlea

Recent evidence shows that the frequency-specific non-linear properties of auditory nerve and inner hair cell responses to sound, including their sharp frequency tuning, are fully established in the vibration of the basilar membrane. In turn, the sensitivity, frequency selectivity and non-linear properties of basilar membrane responses probably result from an influence of the outer hair cells.

Application of a commercially-manufactured Doppler-shift laser velocimeter to the measurement of basilar-membrane vibration

A commercially-available laser Doppler-shift velocimeter has been coupled to a compound microscope equipped with ultra-long-working-distance objectives for the purpose of measuring basilar membrane vibrations in the chinchilla. The animal preparation is nearly identical to that used in our laboratory for similar measurements using the Mössbauer technique. The vibrometer head is mounted on the third tube of the microscopes trinocular head and its laser beam is focused on high-refractive-index glass microbeads (10-30 microns) previously dropped, through the perilymph of scala tympani, on the basilar membrane. For equal sampling times, overall sensitivity of the laser velocimetry system is at least one order of magnitude greater than usually attained using the Mössbauer technique. However, the most important advantage of laser-velocimetry vis-à-vis the Mössbauer technique is its linearity, which permits undistorted recording of signals over a wide velocity range. Thus, for example, we have measured basilar-membrane responses to clicks whose waveforms have dynamic ranges exceeding 60 dB.

Middle‐ear response in the chinchilla and its relationship to mechanics at the base of the cochlea

The responses of the malleus and the stapes to sinusoidal acoustic stimulation have been measured in the middle ears of anesthetized chinchillas using the Mössbauer technique. With intact bullas (i.e., closed except for venting via capillary tubing), the vibrations of the tip of the malleus reach a maximal peak velocity of about 2 mm/s in responses to 100-dB SPL tones in the frequency range 500-6000 Hz; vibration velocity diminishes toward lower frequencies with a slope of about 6 dB/oct. Opening the bulla widely increases the responses to low-frequency stimuli by as much as 16 dB. At low frequencies, malleus response sensitivity with either open or intact bullas far exceeds all previous measurements in cats and matches or exceeds such measurements in guinea pigs. Whether measured in open or intact bullas, phase-versus-frequency curves closely approximate those predicted from the magnitude-versus-frequency curves by minimum phase theory. The stapes responses are similar to those of the malleus, except that stapes response magnitude is lower, on the average, by 7.5 dB at frequencies below 2 kHz and 10.7 dB at 2 kHz and above. Comparison of the responses of the middle ear with those of the basilar membrane at a site 3.5 mm from the stapes indicates that, at frequencies below 150 Hz, the basilar membrane displacement is proportional to stapes acceleration. At frequencies between 150 and 2000 Hz, basilar membrane displacement is proportional to stapes velocity.

Chinchilla auditory‐nerve responses to low‐frequency tones

Single unit activity was recorded in the auditory nerves of chinchillas. Period histograms were constructed for responses to tones with frequencies 30-1000 Hz. For low-frequency tones at near-threshold levels, peak period histogram phases for low- and medium-best-frequency (BF) neurons (less than or equal to kHz) ranged from synchronous with condensation at the eardrum to 90 degrees leading it. At near-threshold (but high absolute) levels, high-BF (greater than or equal to 8 kHz) neurons responded in phase with rarefaction. At even higher levels, period histograms for responses of high-BF neurons tended to become bimodal, with one of the modes lagging rarefaction by 90 degrees. Using cochlear microphonics as an indicator of basilar membrane (BM) displacement, at threshold levels, response phase of low- and medium-BF neurons fall within a range between displacement and velocity of the BM toward scala vestibuli. High-BF neurons respond, at threshold (but high) intensities, in phase with BM displacement toward scala tympani. The rates of growth of frequency sensitivity in responses of low-BF (+ 18 dB/oct) and high-BF (+ 12 dB/oct) neurons are consistent with preferred response phases corresponding to BM SV velocity and ST displacement, respectively. At supra-threshold levels high-BF neurons may fire preferentially to both scala tympani displacement and scala vestibuli velocity. These results support the notion that, for high-intensity, low-frequency stimuli, OHC hyperpolarization can induce excitation of the dendrites innervating IHCs.

Spontaneous and impulsively evoked otoacoustic emission: indicators of cochlear pathology? ☆

The first authors right ear produces a spontaneous otoacoustic emission (SOAE) at 7529 Hz and 16 dB SPL. An external continuous tone is able to suppress the SOAE. The 3 dB iso-suppression curve is broadly tuned and displaced, relative to the SOAE, toward higher frequencies. An audiogram notch exists at frequencies just below that of the SOAE. We explain the occurrence of both spontaneous and impulsively evoked OAEs in terms of disruption of active feedback mechanisms of the OHCs upon basilar membrane vibration. According to this hypothesis, each segment of the organ of Corti feeds back positively upon its segment of basilar membrane and negatively upon adjacent segments. If a patch of OHC loss exists, adjacent segments of the basilar membrane are released from the negative feedback and respond to an impulsive stimulus with exaggerated oscillations at their resonance frequencies, thus producing OAEs. At particularly sharp transitions between normal and abnormal regions of the organ of Corti SOAEs may be generated.

Effects of excitatory and non-excitatory suppressor tones on two-tone rate suppression in auditory nerve fibers

Recordings were obtained from individual auditory nerve fibers in anesthetized chinchillas. Rate versus level functions were obtained for best frequency (BF) tones alone and for simultaneously-gated tone pairs comprising a BF tone and a second tone at a fixed intensity that produced evidence of two-tone rate suppression. Care was taken in selecting a range of suppressor tone levels that included excitatory (i.e., the suppressor tone evoked a rate change by itself) and non-excitatory (i.e., no suppressor tone-evoked rate increase) suppressor tone levels. Addition of a suppressor tone produced a shift of the dynamic range portion of the BF rate versus level function to higher test intensities. A parallel shift of the dynamic range portion of the rate versus level function was associated with a non-excitatory suppressor tone. The shift produced by an excitatory suppressor tone was characterized by a decrease in slope. Results indicated that the magnitude of shift increased monotonically as suppressor tone intensity was raised and that there was a gradual transition from a non-excitatory response to an excitatory response. The rate of shift (i.e., dB of shift per dB change in suppressor tone intensity) did not differ for non-excitatory versus excitatory responses, but was substantially greater for below-BF suppressor tones (1.38 dB/dB) than for above-BF suppressor tones (0.54 dB/dB). The rate of shift did not, however, appear to be related systematically to suppressor tone frequency separation from BF. Above- and below-BF suppression was noted for fibers over the range of best frequencies tested (110 Hz to 16.4 kHz).

Systematic errors in indirect estimates of basilar membrane travel times

There exist in the literature three attempts to derive basilar membrane travel times from the phase versus frequency characteristics of responses to tones in the auditory nerve [Anderson et al., J. Acoust. Soc. Am. 4., 1131-1139 (1971)], cochlear nucleus [Gibson et al., in Psychophysics and Physiology of Hearing, edited by Evans and Wilson (Academic, New York, 1977), pp. 57-68], and basilar membrane [Robles et al., J. Acoust. Soc. Am. 59, 926-939 (1976)]. It is argued in this paper that these derivations probably have overestimated the actual mechanical travel times. Travel time was originally defined by von Békésy as the latency between the onset of a click stimulus and the onset of basilar membrane vibration. For a linear bandpass system, the frequency-domain equivalent of this latency is the high-frequency asymptotoic slope of the phase lag versus frequency characteristic, which is not generally a linear function. In the neural studies (auditory nerve and cochlear nucleus) it was assumed that the phase versus frequency characteristic was a straight line. Slopes derived under a linear assumption are probably closer to the weighted average group delay (i.e., the center of gravity of the click response) than they are to travel time. In the Mössbauer study of basilar membrane mechanics the latency of the response to clicks was compared with the low-frequency slope of the phase characteristic. The comparison should have been made with the high-frequency slope.

Spontaneous otoacoustic emissions in a dog.

Intense (up to 59 dB SPL) spontaneous otoacoustic emissions are produced by both ears of a young dog. The right ear produces a single, very narrow-band (less than 4 Hz) emission at about 9100 Hz. Brainstem evoked-response audiometry suggests that this emission is generated near the transition between normal and abnormal regions of the cochlea.

Mossbauer Measurements of the Mechanical Response to Single-Tone and Two-Tone Stimuli at the Base of the Chinchilla Cochlea

Basilar membrane (BM) motion was measured at a site 3.5 mm from the basal end of the chinchilla cochlea using the Mossbauer technique. In preparations with little surgical damage, mechanical responses were as sharply tuned as auditory nerve fibers with the same characteristic frequency (CF, about 8.4 kHz). High-frequency plateaus were observed in both isovelocity tuning curves and phase-frequency curves. Input-output functions at frequencies around CF were strongly nonlinear. Another type of nonlinearlty, two-tone suppression, was also demonstrated in several cochleas, with suppression effects as large as 28 dB.

Basilar Membrane Responses to Clicks

Basilar membrane responses to clicks were studied in chinchilla cochleae using laser velocimetry. Responses of a basilar membrane site located 3.5 mm from the oval window [characteristic frequency (CF): 8–10 kHz] consisted of relatively undamped transient oscillations with periodicity close to 1/CF. Intense rarefaction clicks caused initial basilar membrane motion toward scala vestibuli after a latency of about 90 microseconds (measured from the onset of inward stapes displacement). The initial response oscillations grew linearly with stimulus intensity but later response cycles grew nonlinearly, at rates less than 1 dB/dB. Thus, with increases in stimulus level, the response envelopes became progressively more asymmetrical, with maxima shifting to earlier times. The magnitude and phase frequency spectra of click responses resembled the corresponding spectra for responses to tones. As click level increased, sharpness of tuning deteriorated and the maximal spectral response component shifted to lower frequencies. The phases of spectral components below characteristic frequency lagged responses evoked by less-intense clicks, while those immediately above characteristic frequency led lower-level responses.