Aerial Hearing Research Articles

Aerial audiograms of several California sea lions (Zalophus californianus) and Steller sea lions (Eumetopias jubatus) measured using single and multiple simultaneous auditory steady-state response methods

Measurements of the electrophysiological auditory steady-state response (ASSR) have proven to be efficient for evaluating hearing sensitivity in odontocete cetaceans. In an effort to expand these methods to pinnipeds, ASSRs elicited by single and multiple simultaneous tones were used to measure aerial hearing thresholds in several California sea lions (Zalophus californianus) and Steller sea lions (Eumetopias jubatus). There were no significant differences between thresholds measured using the single and multiple ASSR methods, despite the more rapid nature of data collection using the multiple ASSR method. There was a high degree of variability in ASSR thresholds among subjects; thresholds covered a range of ∼40 dB at each tested frequency. As expected, ASSR thresholds were elevated relative to previously reported psychophysical thresholds for California and Steller sea lions. The features of high-frequency hearing limit and relative sensitivity of most ASSR audiograms were, however, similar to those of psychophysical audiograms, suggesting that ASSR methods can be used to improve understanding of hearing demographics in sea lions, especially with respect to high-frequency hearing. Thresholds for one Steller sea lion were substantially elevated relative to all other subjects, demonstrating that ASSR methods can be used to detect hearing loss in sea lions.

Hearing in the African lungfish ( Protopterus annectens ): pre-adaptation to pressure hearing in tetrapods?

Lungfishes are the closest living relatives of the tetrapods, and the ear of recent lungfishes resembles the tetrapod ear more than the ear of ray-finned fishes and is therefore of interest for understanding the evolution of hearing in the early tetrapods. The water-to-land transition resulted in major changes in the tetrapod ear associated with the detection of air-borne sound pressure, as evidenced by the late and independent origins of tympanic ears in all of the major tetrapod groups. To investigate lungfish pressure and vibration detection, we measured the sensitivity and frequency responses of five West African lungfish (Protopterus annectens) using brainstem potentials evoked by calibrated sound and vibration stimuli in air and water. We find that the lungfish ear has good low-frequency vibration sensitivity, like recent amphibians, but poor sensitivity to air-borne sound. The skull shows measurable vibrations above 100 Hz when stimulated by air-borne sound, but the ear is apparently insensitive at these frequencies, suggesting that the lungfish ear is neither adapted nor pre-adapted for aerial hearing. Thus, if the lungfish ear is a model of the ear of early tetrapods, their auditory sensitivity was limited to very low frequencies on land, mostly mediated by substrate-borne vibrations.

Psychophysical and electrophysiological aerial audiograms of a Steller sea lion (Eumetopias jubatus)

A within-subject comparison of auditory steady-state response (ASSR) and psychophysical measurements of aerial hearing sensitivity was conducted with an individual of the largest otariid species, the Steller sea lion. Psychophysical methods were used to obtain an unmasked aerial audiogram at 13 frequencies, spanning a range of 0.125-34 kHz. The subject had a hearing range (frequencies audible at 60 dB(rms) re 20 microPa) of about 0.250-30 kHz, and a region of best hearing sensitivity from 5-14.1 kHz. The psychophysical aerial audiogram of this Steller sea lion was remarkably similar to aerial audiograms previously obtained for California sea lions and northern fur seals, suggesting that the otariid pinnipeds form a functional hearing group. ASSR thresholds, measured at frequencies of 1, 2, 5, 10, 20, and 32 kHz, were elevated relative to corresponding psychophysical thresholds, ranging from +1 dB at 20 kHz, to +31 dB at 1 kHz. The ASSR audiogram accurately predicted the subject's high-frequency cutoff, and provided a reasonable estimate of hearing sensitivity at frequencies above 2 kHz. In testing situations where psychophysical methods are not possible, ASSR methods may provide an objective and efficient estimate of behavioral hearing sensitivity in otariid pinnipeds.

Aerial audiograms of Steller and California sea lions measured using auditory steady-state response methods.

Detection of aerial vocal signals by conspecifics is important in the reproductive behavior of the otariid pinnipeds. However, aerial hearing sensitivity measurements have only been obtained for a few otariid individuals that were trained to participate in behavioral experiments. In order to expand upon this small data set, auditory steady-state response (ASSR) methods were used to examine the aerial hearing sensitivity of Steller and California sea lions. Although ASSR thresholds were elevated relative to behavioral thresholds reported for otariids, the ASSR audiograms of the majority of individuals were similar to each other and to behavioral audiograms in terms of relative sensitivity. A marked reduction in sensitivity with increasing frequency regularly occurred between 16 and 32 kHz, indicating a consistent high-frequency cutoff. The reliability of the ASSR audiograms for both species suggests that behavioral aerial audiograms that exist for a few Steller and California sea lion individuals can be appropriately extrapolated to larger populations. The similarity of the ASSR audiograms among the Steller and California sea lions supports the notion that the otariid pinnipeds form a functional hearing group, with similar aerial hearing in terms of sensitivity and frequency range of hearing. [Work supported by ONR and NOAA Ocean Acoustics Program.]

A comparison of behavioral and electrophysiological measures of aerial hearing sensitivity in a Steller sea lion (Eumetopias jubatus).

A number of studies with odontocete cetaceans have demonstrated that hearing sensitivity measurements using electrophysiological auditory steady‐state responses (ASSRs) can provide an efficient means of estimating a subject’s behavioral audiogram. Expansion of ASSR methods to another marine mammal group, the otariid pinnipeds (sea lions and fur seals), holds the potential to increase the number of otariid individuals and species for which hearing sensitivity data are available. A within‐subject comparison of ASSR and behavioral measures of aerial hearing sensitivity was conducted with an individual of the largest otariid species, the Steller sea lion. Psychophysical methods were used to obtain an unmasked aerial audiogram at 13 frequencies spanning a range of 0.125 to 34 kHz. Corresponding ASSR thresholds measured at frequencies of 1, 2, 5, 10, 20, and 32 kHz had differences (relative to behavioral thresholds) ranging from 1 dB at 20 kHz to 30 dB at 1 kHz. Overall, the ASSR audiogram was a fairly accurate predictor of the behavioral audiogram at frequencies of 2 kHz and above. Our results suggest that ASSR methods can be appropriately applied to otariid pinnipeds in estimating aerial sensitivity at frequencies of approximately 2 kHz and above.

Sensitivity of a tucuxi (Sotalia fluviatilis guianensis) to airborne sound

Auditory systems of cetaceans are considered highly specialized for underwater sound processing, whereas the extent of their hearing capacity in air is still a point of issue. In this study, the sensitivity to airborne sound in a male tucuxi (Sotalia fluviatilis guianensis) was tested by means of a go/no go response paradigm. Auditory thresholds were obtained from 2 to 31.5 kHz. Compared to the hearing thresholds of other dolphins as well as of amphibian mammals, the sensitivity to airborne sound of the test subject is low from 2 to 8 kHz, with the highest threshold at 4 kHz. Thresholds at 16 and 31.5 kHz reveal a sharp increase in hearing sensitivity. Thus, although not obtained in this study, the upper aerial hearing limit is in the ultrasonic range. A comparison of the present data with the underwater audiogram of the same test subject referred to sound intensity indicates that the sensitivity of Sotalia to underwater sound is generally better than to airborne sound.

Aerial hearing sensitivity in some pinnipeds is comparable to that of humans

Aerial hearing sensitivity was measured in pinnipeds in a sound attenuating, hemi-anechoic chamber. Thresholds at 12 frequencies between 0.1 and 32.5 kHz were obtained behaviorally for three individuals (a California sea lion, a harbor seal, and a northern elephant seal) and compared to thresholds obtained using headphones in less controlled testing environments. The thresholds measured in the chamber revealed the expected relative changes in sensitivity with frequency; however, the absolute sensitivities were much better than had been previously measured. Harbor seal thresholds were on average 25 dB lower with best sensitivity of −2 dB (re: 20 μPa) at 3.2 kHz. Elephant seal thresholds averaged 23 dB lower with best sensitivity of 27 dB (re: 20 μPa) at 0.4 kHz. Thresholds for the California sea lion were also much lower than expected, with best sensitivity of 1 dB (re: 20 μPa) at 12 kHz. The thresholds measured for the sea lion and harbor seal rival those of human subjects at some frequencies, and suggest that previously reported aerial hearing thresholds in pinnipeds wwere significantly noise limited. Further, the results indicate that these pinnipeds have greater sensitivity in air than in water when comparisons are made in terms of sound pressure.

Age-related hearing loss in sea lions and their scientists

Interest in the hearing capabilities of California sea lions (Zalophus californianus) was first stimulated by the echolocation hypothesis and more recently by rising concern about coastal noise pollution. During a series of audiometric tests, we measured the absolute hearing sensitivity of two sea lions and two of their human investigators. Aerial hearing curves for each subject were obtained with a go/no-go procedure and standard psychophysics. Additionally, underwater hearing curves were obtained for the sea lions using the same procedures. Underwater, the older sea lion (22–25 years of age) showed hearing losses relative to the younger sea lion (13–16 years) that ranged from 10 dB at lower frequencies to 50 dB near the upper frequency limit. The older sea lions’ hearing losses in air were consistent with those measured underwater. The older human (69 years) tested also showed losses relative to the younger human (22 years). These differences ranged from 15 dB at lower frequencies up to 35 dB at the highest frequency tested. The results obtained in this study document age-related hearing losses in sea lions and humans. The findings are consistent with data on presbycusis in other mammalian species, showing that maximum hearing loss occurs at the highest frequencies.

Pinniped hearing and anthropogenic noise

Our behavioral studies of pinniped auditory processing, including amphibious hearing, auditory masking, and temporary threshold shift (TTS), have provided comparative data on hearing and the potential effects of anthropogenic noise for three pinniped species. Differences for one harbor seal between aerial thresholds measured using headphones in a noisy environment and those measured without headphones in a hemi-anechoic chamber are quite large. While additional data are required, the preliminary data suggest that it will be necessary to re-evaluate pinniped aerial hearing capabilities and their susceptibility to aerial anthropogenic noise impacts. Assessments of simultaneous (masking) and residual (TTS) effects of controlled noise exposure have also provided insight into the potential effects of anthopogenic noise on free-ranging pinnipeds. Our underwater masking studies indicated relatively low critical ratios for low-frequency tonal sounds, while underwater TTS studies demonstrated that auditory fatigue occurs in pinnipeds, even following exposure to moderate levels of noise. The TTS studies have also provided some means of estimating the onset of TTS and supplied data on the relative importance of fatiguing noise exposure level and duration. Results suggest that equal-energy relationships and the octave effect previously shown in humans and some terrestrial mammals may not apply for some pinnipeds.

Aerial and underwater hearing sensitivity of a northern elephant seal (Mirounga angustirostris)

Aerial (100 Hz to 28 kHz) and underwater (75 Hz to 59.8 kHz) sound detection thresholds were determined for a female northern elephant seal (Mirounga angustirostris) using behavioral psychophysical techniques. The resulting underwater audiogram shows a typical phocid pattern, with an upper frequency limit of about 59 kHz and relatively flat sensitivity from about 200 Hz to 30 kHz. In air, the elephant seal is 10–30 dB less sensitive than other phocid species tested. Underwater sound pressure thresholds averaged about 15 dB lower than aerial pressure thresholds. The degree of adaptation to underwater hearing in pinnipeds seems to follow phylogenetic trends; however, a high degree of aquatic specialization occurs in the northern elephant seal. Because the elephant seal is apparently nonvocal underwater, the most likely explanation for this high degree of aquatic hearing specialization lies in its ability to dive regularly to depths of 500–700 m. Although the elephant seal has poor aerial hearing relative to other pinnipeds, it has compensated for this deficiency by emitting very loud aerial vocalizations associated with seismic and visual signals to facilitate effective aerial communication. [Work supported by ONR.]

Electromyography of the opercularis muscle of Rana catesbeiana: an amphibian tonic muscle.

The opercularis muscle of Rana catesbeiana originates on the suprascapular cartilage of the shoulder girdle and inserts on the otic opercular element. It is part of the levator scapulae musculature and lies dorsomedial to the levator scapulae superior and inferior muscles. Bipolar electrode recordings from all three muscles show electrical activity linked to cyclical firing of the posterior intermandibularis muscle, an important ventilatory muscle. The opercularis muscle shows low amplitude, erratic signals when animals are submerged. Upon emergence of the snout region, the opercularis muscle shows rhythmic low amplitude activity at twice the rate of buccal pumping. Lung ventilation is synchronized with this rhythm and at ventilation the opercularis muscle shows higher amplitude activity. Upon submergence, opercularis activity again shows low level activity with no rhythmic pattern. Opercularis muscle activity has a major low frequency component (about 30 Hz) that probably corresponds to activity of tonic muscle fibers. Higher frequency signals (about 200-250 Hz) comparable to those of the levator scapulae muscles are also present and probably represent activity of phasic muscle fibers. Activity of the opercularis muscle is correlated with conditions in which aerial respiration is possible, and this pattern of activity supports an opercularis role in aerial hearing and/or detection of substrate vibrations. As far as we know, this is the first report of electromyographic analysis of a vertebrate tonic muscle.

The structure of the amphibian auditory periphery: A unique experiment in terrestrial hearing

The amphibian auditory periphery is traditionally viewed from one of two perspectives: (1) that it is degenerate and by implication derived from the amniote condition or (2) that it represents, at least in most frogs, a simple intermediate condition between the ears of rhipidistian fishes and reptiles. These two perspectives, or various hybrids, guide modern workers in the design of their investigations and the interpretation of the data resulting from these studies. The development and diversity of the amphibian auditory periphery is reviewed and compared to that of amniotes. The otic region in key fossil tetrapods is reviewed. Our current concepts of otic homology are reviewed and some alternative homologies are suggested. This review indicates that the most parsimonius perspective on the amphibian auditory periphery is that it represents a unique experiment in aerial hearing unrelated to that found in modern amniotes. The implications of this perspective for modern morphological and experimental work are discussed. [Work supported by NSF.]

IMPROVEMENT OF HEARING IN CASES OF OTOSCLEROSIS: A NEW, ONE STAGE SURGICAL TECHNIC

The early efforts of Jenkins 1 and Barany 1a and the recent efforts of Holmgren 2 and Sourdille 3 to ameliorate deafness in cases of otosclerosis by surgical means have led to the conclusion that when improvement in hearing has been obtained by the making of a new fenestra in the bony capsule of the labyrinth the early closure of this labyrinthine fistula by bony regeneration must be prevented surgically in order to maintain this improvement in hearing permanently. Sourdille, 4 who performs what he terms a tympanolabyrinthopexy in three principal stages at intervals of four or five months, stated: In a great number of cases, unfortunately, the success is ephemeral: four, six, or ten weeks later, one sees the aerial hearing diminish, the Rinne becomes negative and the Weber indifferent. At the same time, the air pressure in the meatus can attain 40 and even 60 cm. of water without determining nystagmus, nor a