Otto Gleich

Activity patterns of cochlear ganglion neurones in the starling

Summary1.Spontaneous activity and responses to simple tonal stimuli were studied in cochlear ganglion neurones of the starling.2.Both regular and irregular spontaneous activity were recorded (Figs. 1 to 5). Non-auditory cells have their origin in the macula lagenae. Mean spontaneous rate for auditory cells (all irregularly spiking) was 45 spikes s−1.3.In half the units having characteristic frequencies (CFs) <1.5 kHz, time-interval histograms (TIHs) of spontaneous activity showed regularly-spaced peaks or ‘preferred’ intervals. The spacing of the peak intervals was, on average, 15% greater than the CF-period interval of the respective units (Fig. 11).4.In TIH of lower-frequency cells without preferred intervals, the modal interval was also on average about 15% longer than the CF-period interval (Fig. 11). Apparently, the resting oscillation frequency of these cells lies below their CF.5.Tuning curves (TCs) of neurones to short tone bursts show no systematic asymmetry as in mammals. Below CF 1 kHz, the low-frequency flanks of the TCs are, on average, steeper than the high-frequency flanks. Above CF 1 kHz, the reverse is true (Fig. 15).6.The cochlear ganglion and nerve are tonotopically organized. Low-frequency fibres arise apically in the papilla basilaris and are found near non-auditory (lagenar) fibres (Figs. 2 and 19).7.Discharge rates to short tones were monotonically related to sound presure level (Fig. 20). Saturation rates often exceeded 300 spikes s−1.8.‘On-off’ responses and primary suppression of spontaneous activity were observed (Figs. 22 and 23).9.A direct comparison of spontaneous activity and tuning-curve symmetry (Fig. 15b) revealed that, apart from quantative differences, fundamental qualitative differences exist between starling and guinea-pig primary afferents.

An auditory fovea in the barn owl cochlea

The distribution of frequencies along the basilar papilla of the barn owl (Tyto alba) was studied by labelling small groups of primary auditory neurones of defined frequency response and tracing them to their peripheral innervation sites. The exact location of marked neurones was determined in cochlear wholemounts with the aid of a special surface preparation technique. The average basilar papilla length (in fixed, embedded specimens) was 10.74 mm.The resulting frequency map shows the basic vertebrate pattern with the lowest frequencies represented apically and increasingly higher frequencies mapped at progressively more basal locations. However, the length of basilar papilla devoted to different frequency ranges, i.e. the space per octave, varies dramatically in the barn owl. The lower frequencies (up to 2 kHz) show values between about 0.35 and 1 mm/octave, which are roughly equivalent to values reported for other birds. Above that, the space increases enormously, the highest octave (5–10 kHz) covering about 6 mm, or more than half of the length of the basilar papilla.Such an overrepresentation of a narrow, behaviourally very important frequency band is also seen in some bats, where it has been termed an acoustic or auditory fovea.

Auditory primary afferents in the starling: Correlation of function and morphology

Despite the independent evolution of birds and mammals, a number of structural similarities of their hearing organs have developed in parallel. By tracing the peripheral origin of functionally-characterized primary neurons, the present study demonstrates functional similarities between the respective hair cell populations of the hearing organs of birds and mammals. The space devoted to one octave on the starlings basilar papilla is not constant over the whole length; rather it increases from the apical low- to the basal high-frequency end. The finding that (with the exception of a specialized area near the apical end) only tall hair cells situated on the neural limbus receive active afferent innervation is a functional parallel to the mammalian inner hair cells. The thresholds of afferents increase with distance of the related hair cells from the neural side of the papilla and cover a range of more than 50 dB within the area of tall hair cells.

Auditory temporal resolution in birds: Discrimination of harmonic complexes

The ability of three species of birds to discriminate among selected harmonic complexes with fundamental frequencies varying from 50 to 1000 Hz was examined in behavioral experiments. The stimuli were synthetic harmonic complexes with waveform shapes altered by component phase selection, holding spectral and intensive information constant. Birds were able to discriminate between waveforms with randomly selected component phases and those with all components in cosine phase, as well as between positive and negative Schroeder-phase waveforms with harmonic periods as short as 1-2 ms. By contrast, human listeners are unable to make these discriminations at periods less than about 3-4 ms. Electrophysiological measures, including cochlear microphonic and compound action potential measurements to the same stimuli used in behavioral tests, showed differences between birds and gerbils paralleling, but not completely accounting for, the psychophysical differences observed between birds and humans. It appears from these data that birds can hear the fine temporal structure in complex waveforms over very short periods. These data show birds are capable of more precise temporal resolution for complex sounds than is observed in humans and perhaps other mammals. Physiological data further show that at least part of the mechanisms underlying this high temporal resolving power resides at the peripheral level of the avian auditory system.

Auditory brainstem responses in adult budgerigars (Melopsittacus undulatus)

The auditory brainstem response (ABR) was recorded in adult budgerigars (Melopsittacus undulatus) in response to clicks and tones. The typical budgerigar ABR waveform showed two prominent peaks occurring within 4 ms of the stimulus onset. As sound-pressure levels increased, ABR peak latency decreased, and peak amplitude increased for all waves while interwave interval remained relatively constant. While ABR thresholds were about 30 dB higher than behavioral thresholds, the shape of the budgerigar audiogram derived from the ABR closely paralleled that of the behavioral audiogram. Based on the ABR, budgerigars hear best between 1000 and 5700 Hz with best sensitivity at 2860 Hz-the frequency corresponding to the peak frequency in budgerigar vocalizations. The latency of ABR peaks increased and amplitude decreased with increasing repetition rate. This rate-dependent latency increase is greater for wave 2 as indicated by the latency increase in the interwave interval. Generally, changes in the ABR to stimulation intensity, frequency, and repetition rate are comparable to what has been found in other vertebrates.

Functional differentiation of sensory cells in the avian auditory periphery

SummaryMammals and birds have independently developed different populations of sensory cells grouped across the width of their auditory papillae. Although in mammals there is clear evidence for disparate functions for the two hair-cell populations, the different anatomical pattern in birds has made comparisons difficult. In two species of birds, we have used single-fibre staining techniques to trace physiologically-characterized primary auditory nerve fibres to their peripheral synapses. As in mammals, acoustically-active afferent fibres of these birds innervate exclusively the neurally-lying group of hair cells in a 1∶1 relationship, suggesting important parallels in the functional organization of the auditory papillae in these two vertebrate classes. In addition, we found a strong trend of the threshold to acoustic stimuli at the characteristic frequency across the width of the avian papilla.

The hearing organ of birds and crocodilia

Among the vertebrates, birds are one of the most vocal groups. Many birds (especially the passerines, or song birds) rely strongly on their sense of hearing for communication in territorial, social, and sexual behavior and for alarm signals. Their relatives, the Crocodilia (crocodiles, alligators, and gavials) are also vocal—a rare trait in reptiles. They are known to use several kinds of vocalization as communication signals in different behavioral contexts both as adults and as young, even within the egg (e.g., Garrick et al. 1978). In addition, some birds use their hearing for passive sound localization of prey (e.g., owls, Konishi 1973) or for active echolocation in their cave habitats (e.g., oil birds and cave swiftlets, Konishi and Knudsen 1979). Thus the sense of hearing is critically important in the life of many birds and Crocodilia, and selection pressures have produced an excellent sensitivity to sound (in birds as good as in mammals) in the frequency range covered (few birds hear higher frequencies than about 10-12 kHz).

The phase response of primary auditory afferents in a songbird (Sturnus vulgaris L.).

The effects of stimulus frequency and intensity on phase-locking characteristics of cochlear ganglion cells were studied in the starling. All cells showed phase-locking to tone stimuli within their response area. Phase-locking at CF is found on average 9 dB below discharge rate threshold. Phase-locking is best at 0.4 kHz and deteriorates with increasing frequency almost independently of CF. No phase-locking was evident for test frequencies above 3-4 kHz. Phase-locking in cells with CFs above 1.0 kHz is better below CF than at CF. For constant sound pressure, an increase in stimulus frequency always produced an increase in phase lag of the neural response. The phase vs. frequency data obtained at constant sound pressure can be reasonably approximated by straight line functions. The slopes of these functions indicate the latency of the neural response, and are correlated with the CFs of the respective cells; the latency tends to be longer in low-CF cells and shorter in high-CF cells. The latency decreases by 0.04 ms per 1 dB sound pressure increase. The response phase at CF is nearly stimulus level-independent. Increasing stimulus intensity causes increasing phase lag below CF and decreasing phase lag above CF. These results are compared to findings in other vertebrates and demonstrate the similarities of phase-locking characteristics despite the substantial anatomical differences among the vertebrate groups.

Activity patterns of primary auditory-nerve fibres in chickens: Development of fundamental properties

We have examined the activity patterns of single auditory-nerve fibers in the chicken and tested for possible changes during post-hatching development. For this purpose, we recorded from fibres in the cochlear ganglion of chickens of two age groups (about P2 and P21) and investigated their spontaneous and sound-evoked activity patterns under nembutal-chloralhydrate anaesthesia. The spontaneous activity of primary auditory neurones was irregular, the average rates were between 20.5 (P2) and 23 (P21) spikes/s. Many low-frequency fibres from both age groups showed preferred intervals in their spontaneous activity. Tuning characteristics, including the range of characteristic frequencies, the presence of primary and two-tone suppression, the slopes of tuning-curve flanks and Q10dB values were similar to those previously reported for the starling and were statistically indistinguishable between the two age groups. However, there was a difference in fibre thresholds at the highest frequencies. Systematic differences were also present between the two age groups with regard to some characteristics of the rate-intensity functions. These data indicate that whereas the tuning properties of primary auditory fibres of the chicken cochlea are mature as early as post-hatching day 2, the intensity functions are not.

The organization of tip links and stereocilia on hair cells of bird and lizard basilar papillae

Auditory papillae from three species of bird (pigeon, starling, and chick), and two species of European lizard (Podarcis muralis and Podarcis sicula) were examined by scanning electron microscopy. Hair bundles from all papillae showed tip links oriented along the direction of gradation in heights of the stereocilia (i.e. parallel to the hair-cell axis of bilateral symmetry, and so parallel to the excitatory-inhibitory axis for mechanotransduction). This orientation was seen irrespective of the overall orientation of the hair bundle within the papilla. The stereocilia formed columns, joined by the tip links, which ran parallel to the hair-cell axis of bilateral symmetry. The stereocilia within the same column tended to stay together, while those in different columns tended to separate during preparation. In many columns all the stereocilia tended to be a little taller, or a little shorter, than the equivalent stereocilia in adjacent columns, suggesting that all the stereocilia within one column had been affected by a common height determinant during development. In addition, links running laterally between stereocilia were seen, in a band near the base of the stereocilia. The results are consistent with the hypothesis that tip links are a universal feature of mechano-transducing acousticolateral hair cells, and that they are involved in sensory transduction. The results also support suggestions that the tip links may play a role in determining the heights of the stereocilia during development.