Auditory brainstem responses to airborne sounds in the aquatic frog Xenopus laevis: correlation with middle ear characteristics

In this study we recorded auditory brainstem responses to airborne sounds to determine the hearing sensitivity of Xenopus laevis frogs and correlated their hearing profiles with middle ear characteristics. In newly metamorphosed frogs (body mass 0.5–0.76 gm, snout-vent length 17–20 mm) best hearing sensitivities were measured in the 2.4–2.8 kHz range, whereas optimal hearing sensitivity of older adults (body mass 18–90 gm; snout-vent length 57–100 mm) ranged from 1.0 to 1.2 kHz. Middle ear volumes reconstructed from serial sections showed approximate volume of 0.002 cc and 0.04–0.07 cc in newly metamorphosed and older frogs, respectively. This inverse frequency–volume relationship is consistent with the properties of an acoustic resonator indicating that differences in best hearing sensitivity are at least in part correlated to variation in middle ear volumes for airborne sounds. These results are consistent with peak frequency vibrational velocity profiles of Xenopus tympanic disk that have been shown to be dependent on underlying middle ear volumes and corroborate the occurrence of peak amplitudes of otoacoustic emissions in the 1.0–1.2 kHz region in adult Xenopus frogs.     

Hearing sensitivity and amplitude coding in bats are differentially shaped by echolocation calls and social calls

Differences in auditory perception between species are influenced by phylogenetic origin and the perceptual challenges imposed by the natural environment, such as detecting prey- or predator-generated sounds and communication signals. Bats are well suited for comparative studies on auditory perception since they predominantly rely on echolocation to perceive the world, while their social calls and most environmental sounds have low frequencies. We tested if hearing sensitivity and stimulus level coding in bats differ between high and low-frequency ranges by measuring auditory brainstem responses (ABRs) of 86 bats belonging to 11 species. In most species, auditory sensitivity was equally good at both high- and low-frequency ranges, while amplitude was more finely coded for higher frequency ranges. Additionally, we conducted a phylogenetic comparative analysis by combining our ABR data with published data on 27 species. Species-specific peaks in hearing sensitivity correlated with peak frequencies of echolocation calls and pup isolation calls, suggesting that changes in hearing sensitivity evolved in response to frequency changes of echolocation and social calls. Overall, our study provides the most comprehensive comparative assessment of bat hearing capacities to date and highlights the evolutionary pressures acting on their sensory perception.     

The influence of carotid arterial sounds on hearing sensitivity in mammals

Pulsations of the internal carotid and stapedial arteries produce unwanted sounds (noise) in the middle ear cavity which influence hearing in some mammals. 'Noise' pressure levels calculated from pulse rates, volume pulsations of the arteries, and Fourier analysis of arterial waveforms, correlate well with low frequency thresholds of hearing in the Long-eared hedgehog, Tree shrew and Kangaroo rat. In mammals adapted to hear low frequency sounds, such as the Kangaroo rat and fossorial insectivores, the arteries are enclosed in noise attenuating bony tubes. However, most small mammals possess extended high frequency hearing with little sensitivity at the low frequencies of the arterial sounds. In lower tetrapods such as anurans and most lizards, the broad connection between the middle ear cavity and the pharynx creates a leakage pathway which greatly reduces the noise from the stapedial artery. It is probably for these reasons that the large intratympanic arteries did not disturb hearing in early mammals or submammalian forms.     

What did Morganucodon hear?

The structure of the middle and inner ear of Morganucodon , one of the oldest known mammals, is reviewed and compared to the structure of the ears of extant mammals, reptiles and birds with known auditory capabilities. Specifically, allometric relationships between ear dimensions (basilar-membrane length, tympanic-membrane area and stapes-footplate area) and specific features of the audiogram are defined in extant ears. These relationships are then used to make several predictions of auditory function in Morganucodon. The results point out that the ear structures of Morganucodon–Art similar in dimensions to ear structures in both extant small mammals–with predominantly high-frequency (10 kHz) auditory capabilities, and reptiles and birds- with better low and middle-frequency hearing (< 5 kHz). Although the allometric analysis cannot by itself determine whether Morganucodon heard more like present-day small mammals, or birds and reptiles, the apparent stiffness of the Morganucodon middle ear is both more consistent with the high-frequency mammalian middle ear and would act to decrease the sensitivity of a bird-reptile middle ear to low-frequency sound. Several likely hearing scenarios for Morganucodon are defined, including a scenario in which these animals had ears like those of modern small mammals that are selectively sensitive to high-frequency sounds, and a second scenario in which the Morganucodon ear was moderately sensitive to sounds of a narrow middle-frequency range (5–7 kHz) and relatively insensitive to sounds of higher or lower frequency. The evidence needed to substantiate either scenario includes some objective measure of the stiffness of the Morganucodon ossicular system, while a key datum needed to distinguish between the two hypotheses includes confirmation of the presence or absence of a cochlear lamina in the Morganucodon inner ear.     

Infrasonic hearing in birds: a review of audiometry and hypothesized structure–function relationships

The perception of airborne infrasound (sounds below 20 Hz, inaudible to humans except at very high levels) has been documented in a handful of mammals and birds. While animals that produce vocalizations with infrasonic components (e.g. elephants) present conspicuous examples of potential use of infrasound in the context of communication, the extent to which airborne infrasound perception exists among terrestrial animals is unclear. Given that most infrasound in the environment arises from geophysical sources, many of which could be ecologically relevant, communication might not be the only use of infrasound by animals. Therefore, infrasound perception could be more common than currently realized. At least three bird species, each of which do not communicate using infrasound, are capable of detecting infrasound, but the associated auditory mechanisms are not well understood. Here we combine an evaluation of hearing measurements with anatomical observations to propose and evaluate hypotheses supporting avian infrasound detection. Environmental infrasound is mixed with non‐acoustic pressure fluctuations that also occur at infrasonic frequencies. The ear can detect such non‐acoustic pressure perturbations and therefore, distinguishing responses to infrasound from responses to non‐acoustic perturbations presents a great challenge. Our review shows that infrasound could stimulate the ear through the middle ear (tympanic) route and by extratympanic routes bypassing the middle ear. While vibration velocities of the middle ear decline towards infrasonic frequencies, whole‐body vibrations – which are normally much lower amplitude than that those of the middle ear in the ‘audible’ range (i.e. >20 Hz) – do not exhibit a similar decline and therefore may reach vibration magnitudes comparable to the middle ear at infrasonic frequencies. Low stiffness in the middle and inner ear is expected to aid infrasound transmission. In the middle ear, this could be achieved by large air cavities in the skull connected to the middle ear and low stiffness of middle ear structures; in the inner ear, the stiffness of round windows and cochlear partitions are key factors. Within the inner ear, the sizes of the helicotrema and cochlear aqueduct are expected to play important roles in shunting low‐frequency vibrations away from low‐frequency hair‐cell sensors in the cochlea. The basilar papilla, the auditory organ in birds, responds to infrasound in some species, and in pigeons, infrasonic‐sensitive neurons were traced back to the apical, abneural end of the basilar papilla. Vestibular organs and the paratympanic organ, a hair cell organ outside of the inner ear, are additional untested candidates for infrasound detection in birds. In summary, this review brings together evidence to create a hypothetical framework for infrasonic hearing mechanisms in birds and other animals.     

Scaling of the marsupial middle ear and its functional significance

The marsupial middle ear performs an anatomical impedance matching for acoustic energy travelling in air to reach the cochlea. The size of the middle ear sets constraints for the frequencies transmitted. For generalized placental mammals, it has been shown that the limit for high-frequency hearing can be predicted on the basis of middle ear ossicle mass, provided that the ears fulfil requirements of isometry. We studied the interspecific size variation of the middle ear in 23 marsupial species, with the following measurable parameters: skull mass, condylobasal length, ossicular masses for malleus, incus and stapes, tympanic membrane area, oval window area, and lever arm lengths for malleus and incus. Our results show that the middle ear size grows with negative allometry in relation to body size and that the internal proportions of the marsupial middle ear are largely isometric. This resembles the situation in placental mammals and allows us to use their isometric middle ear model to predict the high-frequency hearing limit for marsupials. We found that the isometry model predicts the high-frequency hearing limit for different marsupials well, indicating that marsupials can be used as auditory models for general therian mammalian hearing. At very high frequencies, other factors, such as the inner ear, seem to constrain mammalian hearing.     

Specialization for underwater hearing by the tympanic middle ear of the turtle, Trachemys scripta elegans

Turtles, like other amphibious animals, face a trade-off between terrestrial and aquatic hearing. We used laser vibrometry and auditory brainstem responses to measure their sensitivity to vibration stimuli and to airborne versus underwater sound. Turtles are most sensitive to sound underwater, and their sensitivity depends on the large middle ear, which has a compliant tympanic disc attached to the columella. Behind the disc, the middle ear is a large air-filled cavity with a volume of approximately 0.5 ml and a resonance frequency of approximately 500 Hz underwater. Laser vibrometry measurements underwater showed peak vibrations at 500-600 Hz with a maximum of 300 μm s(-1) Pa(-1), approximately 100 times more than the surrounding water. In air, the auditory brainstem response audiogram showed a best sensitivity to sound of 300-500 Hz. Audiograms before and after removing the skin covering reveal that the cartilaginous tympanic disc shows unchanged sensitivity, indicating that the tympanic disc, and not the overlying skin, is the key sound receiver. If air and water thresholds are compared in terms of sound intensity, thresholds in water are approximately 20-30 dB lower than in air. Therefore, this tympanic ear is specialized for underwater hearing, most probably because sound-induced pulsations of the air in the middle ear cavity drive the tympanic disc.     

Comparative anatomy of the bony labyrinth of extant and extinct porpoises (Cetacea: Phocoenidae)

The inner ear anatomy of cetaceans, now more readily accessible by means of nondestructive high‐resolution X‐ray computed tomographic (CT) scanning, provides a window into their acoustic abilities and ecological preferences. Inner ear labyrinths also may be a source for additional morphological characters for phylogenetic analyses. In this study, we explore digital endocasts of the inner ear labyrinths of representative species of extinct and extant porpoises (Mammalia: Cetacea: Phocoenidae), a clade of some of the smallest odontocete cetaceans, which produce some of the highest‐frequency clicks for biosonar and communication. Metrics used to infer hearing ranges based on cochlear morphology indicate that all taxa considered could hear high‐frequency sounds, thus the group had already acquired high‐frequency hearing capabilities by the Miocene (9–11 Mya) at the latest. Vestibular morphology indicates that extant species with pelagic preferences have similarly low semicircular canal deviations from 90°, values indicating more sensitivity to head rotations. Species with near‐shore preferences have higher canal deviation values, indicating less sensitivity to head rotations. Extending these analyses to the extinct species, we demonstrate a good match between those predicted to have coastal (such as Semirostrum cerutti) preferences and high canal deviation values. We establish new body length relationships based on correlations with inner ear labyrinth volume, which can be further explored among other aquatic mammals to infer body size of specimens consisting of fragmentary material.     

Organs of hearing and equilibrium during ontogenesis of mammals

The peripheral part of acoustic analyzer was studied during pre- and postnatal development of mammals. The main trends of structural evolution of the outer, middle, and inner ear were followed in representatives of different ecological groups during postnatal development. The use of ecologomorphological approach made it possible to establish that specific structural features of the hearing organ in different mammals are determined by adaptation to specific acoustic properties of the environment. It was shown that morphofunctional adaptations directed at optimization of acoustic sensitivity in different environmental conditions were leading in the hearing organ evolution. Comparative-embryological studies of the peripheral part of acoustic system made it possible to determine the stages of formation of individual structures and establish general patterns of prenatal development of the organs of hearing and equilibrium in different mammals.     

Organs of hearing and equilibrium during ontogenesis of mammals

The peripheral part of acoustic analyzer was studied during pre-and postnatal development of mammals. The main trends of structural evolution of the outer, middle, and inner ear were followed in representatives of different ecological groups during postnatal development. The use of ecologomorphological approach made it possible to establish that specific structural features of the hearing organ in different mammals are determined by adaptation to specific acoustic properties of the environment. It was shown that morphofunctional adaptations directed at optimization of acoustic sensitivity in different environmental conditions were leading in the hearing organ evolution. Comparative-embryological studies of the peripheral part of acoustic system made it possible to determine the stages of formation of individual structures and establish general patterns of prenatal development of the organs of hearing and equilibrium in different mammals.     

Correlations between auditory structures and hearing sensitivity in non‐human primates

Primates show distinctions in hearing sensitivity and auditory morphology that generally follow phylogenetic patterns. However, few previous studies have attempted to investigate how differences in primate hearing are directly related to differences in ear morphology. This research helps fill this void by exploring the form‐to‐function relationships of the auditory system in a phylogenetically broad sample of non‐human primates. Numerous structures from the outer, middle, and inner ears were measured in taxa with known hearing capabilities. The structures investigated include the overall size and shape of the pinna, the areas of the tympanic membrane and stapedial footplate, the masses and lever arm lengths of the ossicles, the volumes of the middle ear cavities, and the length of the cochlea. The results demonstrate that a variety of auditory structures show significant correlations with certain aspects of hearing (particularly low‐frequency sensitivity). Although the majority of these relationships agree with expectations from auditory theory, some traditional (and possibly outdated) ideas were not supported. For example, the common misconception that higher middle ear transformer ratios (e.g., impedance transformer ratio) result in increased hearing sensitivity was not supported. Although simple correlations between form and function do not necessarily imply causality, the relationships defined in this study not only increase our understanding of auditory patterns in extant taxa but also lay the foundation to begin investigating the hearing in fossil primates. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

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.     

Effects of noise on inner ear

The effects of noise on health depend both on individual factors and characteristics of sound exposure. In case of acoustic trauma, reversible or irreversible lesions of inner ear components are possible. Most often there is immediately an acute tinnitus and hearing loss. Audiometric tests demonstrate hearing loss on the high frequency, generally focused on 4 kHz. Immediate treatment is recommended even there is no currently indicator of the ability to restore hearing. New perspectives on treatment are directed to local treatment and/or using new procedure as antioxidative treatment. Occupational and leisure are the two conditions in which chronic exposure to noise is found. Detection and prevention of noise-induced hearing loss is easier in case of industrial workers than in case of noise exposition for musicians and other sounds and stage technicians or concert managers, and of course non-professional with exposure to amplified music.     

Acoustic communication and the evolution of hearing in fishes

Fishes have evolved a diversity of sound-generating organs and acoustic signals of various temporal and spectral content. Additionally, representatives of many teleost families such as otophysines, anabantoids, mormyrids and holocentrids possess accessory structures that enhance hearing abilities by acoustically coupling air-filled cavities to the inner ear. Contrary to the accessory hearing structures such as Weberian ossicles in otophysines and suprabranchial chambers in anabantoids, sonic organs do not occur in all members of these taxa. Comparison of audiograms among nine representatives of seven otophysan families from four orders revealed major differences in auditory sensitivity, especially at higher frequencies (> 1 kHz) where thresholds differed by up to 50 dB. These differences showed no apparent correspondence to the ability to produce sounds (vocal versus non-vocal species) or to the spectral content of species-specific sounds. In anabantoids, the lowest auditory thresholds were found in the blue gourami Trichogaster trichopterus, a species not thought to be vocal. Dominant frequencies of sounds corresponded with optimal hearing bandwidth in two out of three vocalizing species. Based on these results, it is concluded that the selective pressures involved in the evolution of accessory hearing structures and in the design of vocal signals were other than those serving to optimize acoustic communication.     

Frequency discrimination by the bottle-nosed dolphin and the Northern fur seal depending on sound parameters and sound conduction pathways

Underwater differential frequency hearing thresholds in the Black Sea bottle-nosed dolphin (Tursiops truncatus p.) and the northern fur seal (Callorhinus ursinus) were measured depending on signal frequency and sound conduction pathways. The measurements were performed by the method of instrumental conditioned reflexes with food reinforcement under conditions of full and partial (with heads out of water at sound conduction through body tissues) submergence of animals into water. It was shown that in a frequency range of 5-100 kHz, underwater differential frequency hearing thresholds of the bottle-nosed dolphin changed from 0.46-0.60% to 0.21-0.34% and depended little on sound conduction pathways. The minimum underwater differential frequency hearing thresholds of the northern fur seal corresponded to the frequencies of maximum hearing sensitivity, changed from 1.7% to 1-2.3% in a frequency range of 1-20 kHz, sharply increased at the edges of the frequency hearing perception range, and depended little (in a range of 5-40 kHz) on sound conduction pathways. Thus, underwater sounds propagating through the body tissues of dolphin and fur seal reach the inner ear.     

Anatomy and physics of the exceptional sensitivity of dolphin hearing (Odontoceti: Cetacea)

During the past 50 years, the high acoustic sensitivity and the echolocation behavior of dolphins and other small odontocetes have been studied thoroughly. However, understanding has been scarce as to how the dolphin cochlea is stimulated by high frequency echoes, and likewise regarding the ear mechanics affecting dolphin audiograms. The characteristic impedance of mammalian soft tissues is similar to that of water, and thus no radical refractions of sound, nor reflections of sound, can be expected at the water/soft tissue interfaces. Consequently, a sound-collecting terrestrial pinna and an outer ear canal serve little purpose in underwater hearing. Additionally, compared to terrestrial mammals whose middle ear performs an impedance match from air to the cochlea, the impedance match performed by the odontocete middle ear needs to be reversed to perform an opposite match from water to the cochlea. In this paper, we discuss anatomical adaptations of dolphins: a lower jaw collecting sound, thus replacing the terrestrial outer ear pinna, and a thin and large tympanic bone plate replacing the tympanic membrane of terrestrial mammals. The paper describes the lower jaw anatomy and hypothetical middle ear mechanisms explaining both the high sensitivity and the converted acoustic impedance match.     

A Role of Medial Olivocochlear Reflex as a Protection Mechanism from Noise-Induced Hearing Loss Revealed in Short-Practicing Violinists

Previous studies have indicated that extended exposure to a high level of sound might increase the risk of hearing loss among professional symphony orchestra musicians. One of the major problems associated with musicians’ hearing loss is difficulty in estimating its risk simply on the basis of the physical amount of exposure, i.e. the exposure level and duration. The aim of this study was to examine whether the measurement of the medial olivocochlear reflex (MOCR), which is assumed to protect the cochlear from acoustic damage, could enable us to assess the risk of hearing loss among musicians. To test this, we compared the MOCR strength and the hearing deterioration caused by one-hour instrument practice. The participants in the study were music university students who are majoring in the violin, whose left ear is exposed to intense violin sounds (broadband sounds containing a significant number of high-frequency components) during their regular instrument practice. Audiogram and click-evoked otoacoustic emissions (CEOAEs) were measured before and after a one-hour violin practice. There was a larger exposure to the left ear than to the right ear, and we observed a left-ear specific temporary threshold shift (TTS) after the violin practice. Left-ear CEOAEs decreased proportionally to the TTS. The exposure level, however, could not entirely explain the inter-individual variation in the TTS and the decrease in CEOAE. On the other hand, the MOCR strength could predict the size of the TTS and CEOAE decrease. Our findings imply that, among other factors, the MOCR is a promising measure for assessing the risk of hearing loss among musicians.     

Non‐Selective and Time‐Dependent Behavioural Responses of Common Toads (Bufo bufo) to Predator Acoustic Cues

Acoustic predator recognition has rarely been studied in anurans, in spite of the fact that hearing is widespread in these animals and that it has been demonstrated to play an important role in both arthropods and other vertebrates. Using field playback experiments, we tested the hypothesis that adult common toads (Bufo bufo) are capable of recognizing natural vocalizations of a common predator, the Eurasian otter (Lutra lutra), and show antipredator responses. We found that toads exposed to both natural (two types of otter sounds) and synthetic stimuli [white noise (WN) and otter sound‐based amplitude modulated WN] increased time allocated to locomotion and escape behaviour. These responses were correlated with time elapsed from sunset to the onset of testing and were independent from the type of acoustic signal, toad features and other environmental factors monitored. We conclude that B. bufo has not developed a selective recognition of predator vocalizations, suggesting that low‐frequency or seismic sounds associated with predator movements may provide anurans with better cues about an approaching risk. We propose that the time‐dependent response to acoustic stimuli of common toads represents a case of threat‐sensitivity and demonstrates that it can occur even when the response to the threat is not predator specific.     

Functional morphology of the middle ear in Chlorotalpa golden moles (Mammalia, Chrysochloridae): predictions from three models

The ossicular apparatus of golden moles in the genus Chlorotalpa has received comparatively little attention in the literature, although the malleus is known to be intermediate in size between the "unmodified" malleus of Amblysomus and the hypertrophied mallei found in some other golden moles. In the present study, the middle ear structures of three Chlorotalpa species (C. duthieae, C. sclateri, and C. arendsi) are described. Measurements of middle ear structures were applied into three existing models of middle ear function. The predictions from the models suggest that the airborne hearing of Chlorotalpa species is limited to relatively low frequencies, but the impedance transformation by the middle ear apparatus is expected to be reasonably efficient. The sensitivity of the middle ear apparatus to inertial bone conduction is intermediate between that predicted for Amblysomus and that predicted for species with hypertrophied mallei. Hearing in fossorial mammals may be limited by factors other than the middle ear apparatus: the predictions for Chlorotalpa must therefore be treated with caution. However, a consideration of the "intermediate" middle ear morphology of Chlorotalpa species sheds some light on the origin of ossicular hypertrophy in golden moles. The limited enlargement of the malleus seen in Chlorotalpa is expected to have improved seismic sensitivity by bone conduction significantly at low frequencies, while airborne hearing might not have been adversely affected.     

Hearing in laboratory animals: strain differences and nonauditory effects of noise

Hearing in laboratory animals is a topic that traditionally has been the domain of the auditory researcher. However, hearing loss and exposure to various environmental sounds can lead to changes in multiple organ systems, making what laboratory animals hear of consequence for researchers beyond those solely interested in hearing. For example, several inbred mouse strains commonly used in biomedical research (e.g., C57BL/6, DBA/2, and BALB/c) experience a genetically determined, progressive hearing loss that can lead to secondary changes in systems ranging from brain neurochemistry to social behavior. Both researchers and laboratory animal facility personnel should be aware of both strain and species differences in hearing in order to minimize potentially confounding variables in their research and to aid in the interpretation of data. Independent of genetic differences, acoustic noise levels in laboratory animal facilities can have considerable effects on the inhabitants. A large body of literature describes the nonauditory impact of noise on the biology and behavior of various strains and species of laboratory animals. The broad systemic effects of noise exposure include changes in endocrine and cardiovascular function, sleep-wake cycle disturbances, seizure susceptibility, and an array of behavioral changes. These changes are determined partly by species and strain; partly by noise intensity level, duration, predictability, and other characteristics of the sound; and partly by animal history and exposure context. This article reviews some of the basic strain and species differences in hearing and outlines how the acoustic environment affects different mammals.