Encoding of phase spectra by the peripheral auditory system of the bullfrog

In this study we have examined the sensitivity of auditory nerve fibers in the bullfrog (Rana catesbeiana) to changes in the phase spectrum of an equal-amplitude multi-harmonic stimulus which spanned the bullfrog's range of hearing. To assess peripheral auditory phase sensitivity, changes in the response properties of VIIIth nerve fibers were measured when the relative phase angle of a single harmonic component nearest a unit's best excitatory frequency was systematically varied. The results revealed that shifts in the phase spectrum are encoded in at least J different ways by the peripheral auditory system of the bullfrog: 1) by changes in the degree of spike synchronization of fibers from both inner ear organs (the amphibian papilla and the basilar papilla) to the fundamental waveform period; 2) by changes in the shapes of period histograms of fibers from both organs; and 3) by changes in the spike rates of amphibian papilla fibers. The presence of phase sensitivity in the peripheral auditory system of the bullfrog indicates that information regarding the fine-temporal waveshape and the underlying phase spectrum of an acoustic signal is contained within the spike trains of VIIIth nerve fibers. Similar sensitivities to changes in the phase spectra and temporal waveshapes of acoustic signals may also be present in the peripheral auditory system of other vertebrates. Such studies could provide valuable insight into the role that phase spectra and temporal waveshape may play in bioacoustic communication.Abbreviations BEF best excitatory frequency - BEC best excitatory component - CS_{f 1} synchronization to the fundamental period Portions of this study have been summarized in abstract form (Bodnar and Capranica 1991)     

Mechanics of the exceptional anuran ear

The anuran ear is frequently used for studying fundamental properties of vertebrate auditory systems. This is due to its unique anatomical features, most prominently the lack of a basilar membrane and the presence of two dedicated acoustic end organs, the basilar papilla and the amphibian papilla. Our current anatomical and functional knowledge implies that three distinct regions can be identified within these two organs. The basilar papilla functions as a single auditory filter. The low-frequency portion of the amphibian papilla is an electrically tuned, tonotopically organized auditory end organ. The high-frequency portion of the amphibian papilla is mechanically tuned and tonotopically organized, and it emits spontaneous otoacoustic emissions. This high-frequency portion of the amphibian papilla shows a remarkable, functional resemblance to the mammalian cochlea.     

The tonotopic organization of the bullfrog amphibian papilla,an auditory organ lacking a basilar membrane

Summary Intracellular dye-injection studies have revealed tonotopic organization of the bullfrog (Rana catesbeiana) amphibian papilla, an auditory organ lacking a basilar membrane or its equivalent. The best excitatory frequency (BEF) for auditory stimuli was identified in each of twenty-nine VIIIth-nerve afferent axons that subsequently were traced to their peripheral terminations at the sensory surface. Among those axons, the five with BEFs greater than 550 Hz all terminated in the caudalmost region of the papilla, the ten with the BEFs greater than 300 Hz and less than or equal to 550 Hz all terminated in the central region of the papilla, and the fourteen with BEFs equal to or less than 300 Hz all terminated in the rostralmost region of the papilla (Fig. 4). The tectorium is very much larger and presumably more massive under the low-frequency region of the papilla than it is under the high-frequency region (Fig. 1). Higher-frequency axons tended to innervate few (one to four) receptor cells, and low-frequency axons tended to innervate many (six or more). Higher-frequency axons often terminated in large claw-like structures that engulfed the basal portions of individual hair cells and in this way were morphologically similar to type I terminals in the inner ears of higher vertebrates.Abbreviations BEF best excitatory frequency - HRP horseradish peroxidase     

Peripheral auditory processing in the bobtail lizard Tiliqua rugosa

Summary We have labelled single physiologically-characterized primary auditory neurones in the bobtail lizard and traced them to their innervation sites within the basilar papilla. The distribution of stained fibre terminals shows that low frequencies (up to a characteristic frequency, CF, of about 0.8 kHz) are processed in the smaller apical segment of the papilla and medium to high frequencies in the much longer basal segment. It is possible that the frequency ranges of these segments partly overlap in individual animals.The tonotopic organization of the basal segment is well described by an exponential relationship; the CF increases towards the basal end. Systematic, peripheral recordings from the auditory nerve very close to the papilla confirm this tonotopicity for the basal segment.The apical segment of the papilla shows an unusual tonotopic organization in that the CF appears to increase across the epithelium, from abneural to neural. A tonotopicity in this direction has not previously been demonstrated in vertebrates.All stained neurones branched within the basilar papilla to innervate, typically, between 4 and 14 hair cells. The branching patterns of fibres innervating in the apical and basal papillar segment, respectively, show characteristic differences. Apical fibres tend to innervate hair cells with the same morphological polarity and often branch extensively along the segment. Basal fibres, in contrast, typically innervate about equal numbers of hair cells of opposing polarity and are more restricted in their longitudinal branching.Abbreviation CF characteristic frequency     

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.Abbreviations CF characteristic frequency - HRP horseradish peroxidase - NA Nucleus angularis - NM Nucleus magnocellularis     

The middle ear in the ontogenesis of mammals

The middle ear in mammals is characterized by structural variations and a broad spectrum of adaptive transformations related to peculiarities of species ecology, but it preserves the general basic principle of structure in most mammals. In species remote from a phylogenetic point of view but close in ecologic specialization, features of parallelism are observed concerning the development of separate elements of auditory ossicles as well as the way of their interconnection and attachment to the tympanum. Along the way to the adaptation to the water lifestyle in semi-aquatic and aquatic species, new additional structures, not intrinsic to initial terrestrial forms, have been formed. The use of ecological and morphological approaches to research the peripheral division of the auditory system of mammals with different ecological specialization in the ontogenesis permitted us to reveal that peculiarities of its structure in different groups of mammals are preconditioned by the animals’ adaptation to specific acoustic properties of their environment. Morphological and functional adaptations of the peripheral auditory system aimed at optimizing auditory sensitivity in the environments differing in physical properties are of great importance in evolution. Adaptive specific features in the structure of the middle ear in aquatic species appear at early stages of development in spite of intrauterine growth without the direct influence of environmental conditions.     

Hearing conspecific vocal signals alters peripheral auditory sensitivity

We investigated whether hearing advertisement calls over several nights, as happens in natural frog choruses, modified the responses of the peripheral auditory system in the green treefrog, Hyla cinerea. Using auditory evoked potentials (AEP), we found that exposure to 10 nights of a simulated male chorus lowered auditory thresholds in males and females, while exposure to random tones had no effect in males, but did result in lower thresholds in females. The threshold change was larger at the lower frequencies stimulating the amphibian papilla than at higher frequencies stimulating the basilar papilla. Suprathreshold responses to tonal stimuli were assessed for two peaks in the AEP recordings. For the peak P1 (assessed for 0.8–1.25 kHz), peak amplitude increased following chorus exposure. For peak P2 (assessed for 2–4 kHz), peak amplitude decreased at frequencies between 2.5 and 4.0 kHz, but remained unaltered at 2.0 kHz. Our results show for the first time, to our knowledge, that hearing dynamic social stimuli, like frog choruses, can alter the responses of the auditory periphery in a way that could enhance the detection of and response to conspecific acoustic communication signals.     

Distribution of calcium-binding proteins,parvalbumin and calbindin,in the midbrain auditory center (MLd) of a pigeon

Immunohistochemical distribution of calcium-binding proteins, parvalbumin (PV) and calbindin (CB), has been studied in the mesencephalic auditory center (MLd) of pigeon (Columba livia). In the central region of the MLd (core, ICC), an overlap in distribution of the PVand CB-immunopositive (ip) neurons and neuropil has been observed, with different patterns in the central and peripheral parts. In the peripheral region of the MLd (belt, ICS, and ICX), both neurons and neuropil contained only CB. A selective CB chemospecificity of the belt, ICS, and ICX is an evolutionary conserved feature characteristic of all avian species. Interspecies differences in the distribution of PV and CB immunoreactivity in the ICC are a result of adaptive functional specialization, which provides specific processing of different aspects of the auditory information.     

Seismic and auditory tuning curves from bullfrog saccular and amphibian papular axons

We present seismic and auditory frequency tuning curves of individual bullfrog, Rana catesbeiana, saccular and amphibian papilla axons that responded to both seismic and auditory stimuli. In this study we found: 1) most saccular axons respond well to auditory stimuli with moderate signal strength (50-70 dB SPL) as well as to seismic stimuli; 2) most amphibian papilla axons respond well to seismic stimuli as well as to auditory stimuli, and their seismic sensitivities are comparable to those of saccular axons (responding to sinusoidal stimuli with peak accelerations in the range 0.001 to 0.1 cm/S2); 3) the responses to both seismic and auditory stimuli from both saccule and amphibian papilla are tuned, i.e. the strength of the response varies with the frequency of the stimulus; and this tuning is clearly not the result of second order resonance; 4) in individual axons the tuning properties for seismic stimuli often are not the same as those for auditory stimuli, a fact that may provide clues about how the stimulus signal energy is transferred to the hair cells in each case.     

Peripheral frequency mis-match in the primitive ensiferan Cyphoderris monstrosa (Orthoptera: Haglidae)

Peripheral auditory frequency tuning in the ensiferan insect Cyphoderris monstrosa (Orthoptera: Haglidae) was examined by comparing tympanal vibrations and primary auditory receptor responses. In this species there is a mis-match between the frequency of maximal auditory sensitivity and the frequency content of the species' acoustic signals. The mis-match is not a function of the mechanical properties of the tympanum, but is evident at the level of primary receptors. There are two classes of primary receptors: low-tuned and broadly tuned. Differences in the absolute sensitivity of the two receptor types at the male song frequency would allow the auditory system to discriminate intraspecific signals from sounds containing lower frequencies. Comparisons of tympanal and receptor tuning indicated that the sensitivity of the broadly tuned receptors did not differ from that of the tympanum, while low-tuned receptors had significantly narrower frequency tuning. The results suggest that the limited specialization for the encoding of intraspecific signals in the auditory system of C. monstrosa is a primitive rather than a degenerate condition. The limited specialization of C. monstrosa may reflect the evolutionary origin of communication-related hearing from a generalized precursor through the addition of peripheral adaptations (tympana, additional receptors) to enhance frequency sensitivity and discrimination. Accepted: 13 March 1999     

Modulation of activity in starling cochlear ganglion units by middle-ear muscle contractions,perilymph movements and lagena stimuli

In the present study three groups of cochlear ganglion neurons were detected which differed in respect to their tone-evoked and spontaneous activity: auditory units which showed an irregular spontaneous discharge, non-auditory neurones with regular activity and such with an irregular spontaneous discharge pattern. Electrically-elicited contractions of the middle-ear muscle influenced the tone-evoked and/or the spontaneous activity of the auditory and the non-auditory neurones with irregular spontaneous discharge but not, however, the regularly firing units. Similar results were obtained with imposed perilymph movements in the cochlea (evoked via the vestibular system. Fractions of all three groups of cochlear ganglion neurones were responsive to direct deformations of the membraneous lagena. Several (auditory and non-auditory) units with irregular discharge were excited during a basilar membrane displacement towards scala vestibuli whereas a basilar membrane motion towards scala tympani resulted in a decrease of the discharge rate. A few units showed a different reaction. The results provide evidence that the neurones with periodic spontaneous discharge innervate the lagena and that this sense organ has no auditory significance in birds. The peripheral origin of the 'non-auditory' neurones with irregular spontaneous activity remains undecided and might be the macula lagenae or the apical portion of the basilar papilla.     

Signal Redundancy and Receiver Permissiveness in Acoustic Mate Recognition by the Tungara Frog, Physalaemus pustulosus

The tungara frog has an advertisement call with two structurallyand functionally distinct components: the whine is both necessaryand sufficient for species recognition, and addition of chucksfurther enhances call attractiveness. Only the fundamental frequencyof the whine contributes to phonotaxis; the upper harmonicsplay no role. Furthermore, only a small portion of the whine,within the first 0–100 msec, is necessary to elicit phonotaxis;there is some redundancy since either the 0–50 msec orthe 50–100 msec portion elicits a response. Most of theremainder of the whine's fundamental further enhances call attractiveness.Only the amphibian papilla in the peripheral auditory systemis involved in decoding the whine. In stark contrast, severalchuck variants, which stimulate either the amphibian papillaor the basilar papilla, and white noise are as effective inenhancing call attractiveness as is the normal chuck, showingthat either peripheral end organ can be involved in the perceptionof a more attractive call. Thus there is greater receiver specificityfor decoding stimuli in interspecific mate choice, and greaterreceiver permissiveness for decoding stimuli in intraspecificmate choice; it appears that intraspecific mate choice can takeadvantage of a greater array of neural pathways for call decodingthan can interspecific mate choice.     

The anatomy, physiology, functional significance and evolution of specialized hearing organs of gerbilline rodents

Middle and inner ear anatomy correlates with neurophysiological responses to a wide range of sound frequencies for species of the Gerbillinae representing generalized, intermediate, and specialized anatomical conditions. Neurophysiological data were recorded from 81 specimens of 13 species representing six genera. Anatomical parameters involved in the process of hearing were correlated with the neurophysiological data to assess the effects of different degrees of anatomical specialization on hearing. The 13 species tested in this manner have graphic curves of auditory sensitivity of remarkably similar disposition over the frequencies tested and to those published for Kangaroo Rats. Ears with anatomical specializations show greater auditory sensitivity. The natural history of the Gerbillinae, particularly the kinds of predators, degree of predation, and habitat is reviewed and utilized to interpret the significance of the degree of auditory specialization in the forms studied and to evaluate the prevailing hypothesis that these specializations enhance the ability of these rodents to survive in open desert situations by detecting and evading predators. The middle ear anatomy of five additional genera and species was also studied. Thus, data on the entire spectrum of gerbilline middle ear morphology provide an evolutionary sequence. Certain anatomical parameters of the organ of Corti show a degree of specialization parallel to that of features of the middle ear. The morphological changes and possible functional roles of these features are considered. A very high correlation exists for degree of specialization and aridity of habitat, thus specialization increases with increasing aridity. This increased specialization may result from more effective predation in open xeric environments. Auditory acuity for a wide range of low frequency sounds augmented by auditory specialization is hence more advantageous here. There does not appear to be selection for hearing at particular frequencies in this range. The peaks of greatest auditory sensitivity appear to correspond to the resonant frequencies of the different components of the middle ear transformer and cavity.     

Aroclor 1254 impairs the hearing ability of Xenopus laevis

In this study we assessed the effects of chronic, dietary exposure of Aroclor 1254 (A1254) on the hearing of Xenopus frogs. We used the auditory brainstem response (ABR) to assay changes in hearing physiology; ABR thresholds, as well as latency-intensity and amplitude-intensity profiles of the initial positive (P1) and negative (N1) peaks were measured. Two groups of animals that received 50 ppm and 100 ppm of A1254 in their diet from 5 days post-fertilization through metamorphosis were compared to a control group that received untreated chow. The results showed significant threshold elevations in the 3–4 kHz range and significantly delayed peak latencies and reduced amplitudes at these frequencies in A1254 treated animals as compared to control animals. These findings indicate that A1254 selectively damages the high-frequency sensorineural hearing system associated with the basilar papilla of frogs. This preferential damage may be related to inherent differences in the vulnerability of the basilar versus amphibian papilla in the frog. The overall results of this study are also consistent with the reported A1254-induced auditory deficits in mammals indicating that the basilar papilla of the Xenopus frog may serve as an effective model for studying the effects of A1254 on the auditory system.     

Female reproductive state influences the auditory midbrain response

Female behavioral responses to sensory stimuli can be highly variable across the reproductive cycle. Female green treefrogs (Hyla cinerea) use the male vocal signal to locate and choose a mate. Gravid females approach a vocalizing male to mate but do not approach if they have recently mated. Such differences in behavioral response may be due in part to shifts in the neural representation of auditory information in the brain. In this study, we investigated the influence of female reproductive state on neural responses in the auditory midbrain to both communication signals (advertisement calls) and non-communication sounds (band limited noise bursts). Recently mated females exhibited significantly reduced response strengths compared to females not recently mated. Reduced response strengths in post-mated females were in response to both noise bursts and male advertisement calls but were limited to the lower frequency range corresponding to the amphibian papilla of the peripheral auditory system. Our results therefore show that the ability of social signals to stimulate the auditory system differs in females depending on their reproductive state, and that the differential effect on low versus high spectral sensitivities may influence the way the two spectral peaks of male advertisement calls are represented.     

Three populations of primary auditory fibers in the bullfrog (Rana catesbeiana): Their peripheral origins and frequency sensitivities

Summary Single unit recordings from the VIIIth nerve of the bullfrog (Rana catesbeiana) in response to tones reveal three populations of auditory fibers: low-frequency inhibitable fibers, mid-frequency non-inhibitable fibers and high-frequency non-inhibitable fibers. By selectively sectioning and recording from individual nerve branchlets within the inner ear, it is shown that the amphibian papilla gives rise to low and mid-frequency sensitive units and the basilar papilla gives rise to high-frequency sensitive units.This study was supported by an NIH Research Grant NS-09244 from the U.S. Public Health Service.     

Peripheral auditory tuning for fine frequency analysis by the CF-FM bat,Rhinolophus ferrumequinum

Summary For echolocation,Rhinolophus ferrumequinum emits orientation sounds, each of which consists of a long constant-frequency (CF) component and short frequency-modulated (FM) components. The CF component is about 83 kHz and is used for Doppler-shift compensation. In this bat, single auditory nerve fibers and cochlear nuclear neurons tuned at about 83 kHz show low threshold and very sharp filter characteristics. The slopes of their tuning curves ranged between 1,000 and 3,500 dB/octave and their Q-10 dB values were between 20 and 400, 140 on the average (Figs. 3–5). The peripheral auditory system is apparently specialized for the reception and fine frequency analysis of the CF component in orientation sounds and Doppler-shift compensated echoes. This specialization is not due to suppression or inhibition comparable to lateral inhibition, but due to the mechanical specialization of the cochlea. Peripheral auditory neurons with the best frequency between 77 and 87 kHz showed not only on-responses, but also off-responses to tonal stimuli (Figs. 1, 2, and 6). The off-responses with a latency comparable to that of N₁-off were not due to a rebound from either suppression or inhibition, but probably due to a mechanical transient occurring in the cochlea at the cessation of a tone burst.We thank Alexander von Humboldt Stiftung, Deutsche Forschungsgemeinschaft (Grant No. Ne146/6-8), Stiftung Volkswagenwerk (Grant No. 111858), and American National Science Foundation (Grant No. 40018 and BMS 75-17077) for their support for our cooperative work.     

FGFR3 expression during development and regeneration of the chick inner ear sensory epithelia.

Several studies suggest fibroblast growth factor receptor 3 (FGFR3) plays a role in the development of the auditory epithelium in mammals. We undertook a study of FGFR3 in the developing and mature chicken inner ear and during regeneration of this epithelium to determine whether FGFR3 shows a similar pattern of expression in birds. FGFR3 mRNA is highly expressed in most support cells in the mature chick basilar papilla but not in vestibular organs of the chick. The gene is expressed early in the development of the basilar papilla. Gentamicin treatment sufficient to destroy hair cells in the basilar papilla causes a rapid, transient downregulation of FGFR3 mRNA in the region of damage. In the initial stages of hair cell regeneration, the support cells that reenter the mitotic cycle in the basilar papilla do not express detectable levels of FGFR3 mRNA. However, once the hair cells have regenerated in this region, the levels of FGFR3 mRNA and protein expression rapidly return to approximate those in the undamaged epithelium. These results indicate that FGFR3 expression changes after drug-induced hair cell damage to the basilar papilla in an opposite way to that found in the mammalian cochlea and may be involved in regulating the proliferation of support cells.