The career and research contributions of Richard R. Fay.

For over 50 years, Richard R. (Dick) Fay made major contributions to our understanding of vertebrate hearing. Much of Dick's work focused on hearing in fishes and, particularly, goldfish, as well as a few other species, in a substantial body of work on sound localization mechanisms. However, Dick's focus was always on using his studies to try and understand bigger issues of vertebrate hearing and its evolution. This article is slightly adapted from an article that Dick wrote in 2010 on the closure of the Parmly Hearing Institute at Loyola University Chicago. Except for small modifications and minor updates, the words and ideas herein are those of Dick.

Intra- and Intersexual swim bladder dimorphisms in the plainfin midshipman fish (Porichthys notatus): Implications of swim bladder proximity to the inner ear for sound pressure detection.

The plainfin midshipman fish, Porichthys notatus, is a nocturnal marine teleost that uses social acoustic signals for communication during the breeding season. Nesting type I males produce multiharmonic advertisement calls by contracting their swim bladder sonic muscles to attract females for courtship and spawning while subsequently attracting cuckholding type II males. Here, we report intra- and intersexual dimorphisms of the swim bladder in a vocal teleost fish and detail the swim bladder dimorphisms in the three sexual phenotypes (females, type I and II males) of plainfin midshipman fish. Micro-computerized tomography revealed that females and type II males have prominent, horn-like rostral swim bladder extensions that project toward the inner ear end organs (saccule, lagena, and utricle). The rostral swim bladder extensions were longer, and the distance between these swim bladder extensions and each inner-ear end organ type was significantly shorter in both females and type II males compared to that in type I males. Our results revealed that the normalized swim bladder length of females and type II males was longer than that in type I males while there was no difference in normalized swim bladder width among the three sexual phenotypes. We predict that these intrasexual and intersexual differences in swim bladder morphology among midshipman sexual phenotypes will afford greater sound pressure sensitivity and higher frequency detection in females and type II males and facilitate the detection and localization of conspecifics in shallow water environments, like those in which midshipman breed and nest.

"Large" Tank Acoustics: How Big Is Big Enough?

In this paper, we discuss the issues encountered when trying to perform hearing experiments in water-filled tanks that are several meters in lateral extent, typically large in terms of the size of the animals under study but not necessarily so with respect to the wavelengths of interest. This paper presents measurements of pressure and particle motion fields in these "large" tanks. The observed characteristics and complexities are discussed in reference to their potential impact on the planning and interpretation of hearing experiments.

It Started in Hawai'i Kai: Reminiscences of 43 Years (and Counting) of Collaboration and Friendship.

This paper discusses the 43+ year collaboration of Arthur Popper and Richard Fay. Over these years, we have co-authored over 30 papers and 55 books. The collaboration benefits from a strong friendship that includes our spouses and children. By any measure, our collaboration must be seen as being successful. The basis for this success is, we think, twofold. First, we have very complementary and overlapping research interests. This has enabled us to tackle issues, whether in research or in planning meetings or books, from different perspectives. Second, a hallmark of our successful collaboration has been our deep and close friendship and the extension of that friendship to our spouses and children. In this paper, we discuss some of the events that have shaped our collaboration, and some of the people who have impacted our lives.

Parvulescu Revisited: Small Tank Acoustics for Bioacousticians.

Researchers often perform hearing studies on fish in small tanks. The acoustic field in such a tank is considerably different from the acoustic field that occurs in the animal's natural environment. The significance of these differences is magnified by the nature of the fish's auditory system where either acoustic pressure (a scalar), acoustic particle velocity (a vector), or both may serve as the stimulus. It is essential for the underwater acoustician to understand the acoustics of small tanks to be able to carry out valid auditory research in the laboratory and to properly compare and interpret the results of others.

Auditory Evoked Potential Audiograms Compared with Behavioral Audiograms in Aquatic Animals.

Auditory evoked potentials (AEPs) have become popular for estimating hearing thresholds and audiograms. What is the utility of these measurements? How do AEP audiograms compare with behavioral audiograms? In general, AEP measurements for fishes and marine mammals often underestimate behavioral thresholds, but comparisons are especially complicated when the AEP and behavioral measures are obtained under different acoustic conditions. There is no single representative relationship between AEP and behavioral audiograms and these audiograms should not be considered equivalent. We suggest that the most valuable comparisons are those made by the same researcher using similar acoustic conditions for both measurements.

Computerized tomography of the otic capsule and otoliths in the oyster toadfish, Opsanus tau.

The neurocranium of the toadfish (Opsanus tau) exhibits a distinct translucent region in the otic capsule (OC) that may have functional significance for the auditory pathway. This study used ultrahigh resolution computerized tomography (100 µm voxels) to compare the relative density of three sites along the OC (dorsolateral, midlateral, and ventromedial) and two reference sites (dorsal: supraoccipital crest; ventral: parasphenoid bone) in the neurocranium. Higher attenuation occurs where structural density is greater; thus, we compared the X-ray attenuations measured, which provided a measure of relative density. The maximum attenuation value was recorded for each of the five sites (x and y) on consecutive sections throughout the OC and for each of the three calcareous otoliths associated with the sensory maculae (lagena, saccule, and utricle) in the OC. All three otoliths had higher attenuations than any sites in the neurocranium. Both dorsal and ventral reference sites (supraoccipital crest and parasphenoid bone, respectively) had attenuation levels consistent with calcified bone and had relatively small, irregular variations along the length of the OC in all individuals. The lowest relative attenuations (lowest densities) occurred consistently at the three sites along the OC. In addition, the lowest attenuations measured along the OC occurred at the ventromedial site around the saccular otolith for all seven fish. The decrease in bone density along the OC is consistent with the hypothesis that there is a low-density channel in the skull to facilitate transmission of acoustic stimuli to the auditory endorgans of the ear.

Use of the swim bladder and lateral line in near-field sound source localization by fish.

We investigated the roles of the swim bladder and the lateral line system in sound localization behavior by the plainfin midshipman fish (Porichthys notatus). Reproductive female midshipman underwent either surgical deflation of the swim bladder or cryoablation of the lateral line and were then tested in a monopolar sound source localization task. Fish with nominally 'deflated' swim bladders performed similar to sham-deflated controls; however, post-experiment evaluation of swim bladder deflation revealed that a majority of 'deflated' fish (88%, seven of the eight fish) that exhibited positive phonotaxis had partially inflated swim bladders. In total, 95% (21/22) of fish that localized the source had at least partially inflated swim bladders, indicating that pressure reception is likely required for sound source localization. In lateral line experiments, no difference was observed in the proportion of females exhibiting positive phonotaxis with ablated (37%) versus sham-ablated (47%) lateral line systems. These data suggest that the lateral line system is likely not required for sound source localization, although this system may be important for fine-tuning the approach to the sound source. We found that midshipman can solve the 180 deg ambiguity of source direction in the shallow water of our test tank, which is similar to their nesting environment. We also found that the potential directional cues (phase relationship between pressure and particle motion) in shallow water differs from a theoretical free-field. Therefore, the general question of how fish use acoustic pressure cues to solve the 180 deg ambiguity of source direction from the particle motion vector remains unresolved.

Does the magnocellular octaval nucleus process auditory information in the toadfish, Opsanus tau?

Previous work on auditory processing in Opsanus tau has focused on the descending octaval nucleus; however, the magnocellular octaval nucleus receives similar inputs from the otolithic endorgans. The purpose of this study was to assess whether cells in any of the three subdivisions of the magnocellular nucleus respond to auditory frequencies and encode sound source direction. Extracellular recording sites were chosen based on anatomical landmarks, and neurobiotin injections confirmed the location of auditory sites in subdivisions of the magnocellular nucleus. In general, the auditory cells in M2 and M3 responded best to frequencies at or below 100 Hz. Most auditory cells responded well to directional stimuli presented along axes in the horizontal plane. Cells in M3 (not M2) also responded to lateral line stimulation, consistent with otolithic endorgan and lateral line inputs to M3. The convergence of auditory and lateral line inputs in M3, the lack of Mauthner cells in this species, and previous evidence that the magnocellular nucleus does not contribute to ascending auditory pathways suggest to us that the large cells of M3 may play a role in rapid behavioral responses to particle motion stimuli in oyster toadfish.

Auditory evoked potential audiometry in fish.

A recent survey lists more than 100 papers utilizing the auditory evoked potential (AEP) recording technique for studying hearing in fishes. More than 95 % of these AEP-studies were published after Kenyon et al. introduced a non-invasive electrophysiological approach in 1998 allowing rapid evaluation of hearing and repeated testing of animals. First, our review compares AEP hearing thresholds to behaviorally gained thresholds. Second, baseline hearing abilities are described and compared in 111 fish species out of 51 families. Following this, studies investigating the functional significance of various accessory hearing structures (Weberian ossicles, swim bladder, otic bladders) by eliminating these morphological structures in various ways are dealt with. Furthermore, studies on the ontogenetic development of hearing are summarized. The AEP-technique was frequently used to study the effects of high sound/noise levels on hearing in particular by measuring the temporary threshold shifts after exposure to various noise types (white noise, pure tones and anthropogenic noises). In addition, the hearing thresholds were determined in the presence of noise (white, ambient, ship noise) in several studies, a phenomenon termed masking. Various ecological (e.g., temperature, cave dwelling), genetic (e.g., albinism), methodical (e.g., ototoxic drugs, threshold criteria, speaker choice) and behavioral (e.g., dominance, reproductive status) factors potentially influencing hearing were investigated. Finally, the technique was successfully utilized to study acoustic communication by comparing hearing curves with sound spectra either under quiet conditions or in the presence of noise, by analyzing the temporal resolution ability of the auditory system and the detection of temporal, spectral and amplitude characteristics of conspecific vocalizations.

Experiments in comparative hearing: Georg von Békésy and beyond.

Georg von Békésy was one of the first comparative auditory researchers. He not only studied basilar membrane (BM) movements in a range of mammals of widely different sizes, he also worked on the chicken basilar papilla and the frog middle ear. We show that, in mammals, at least, his data do not differ from those that could be collected using modern techniques but with the same, very loud sounds. There is in all cases a major difference to frequency maps collected using low-level sounds. In contrast, the same cannot be said of his chicken data, perhaps due to the different roles played by the BM in mammals and birds. In lizards, the BM is not tuned and it is perhaps good that Békésy did not begin with those species and get discouraged in his seminal comparative work.

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.

Local acoustic particle motion guides sound-source localization behavior in the plainfin midshipman fish, Porichthys notatus.

Sound-source localization behavior was studied in the plainfin midshipman fish (Porichthys notatus) by making use of the naturally occurring phonotaxis response of gravid females to playback of the male's advertisement call. The observations took place outdoors in a circular concrete tank. A dipole sound projector was placed at the center of the tank and an 80-90 Hz tone (the approximate fundamental frequency to the male's advertisement call) was broadcast to gravid females that were released from alternative sites approximately 100 cm from the source. The phonotaxic responses of females to the source were recorded, analyzed and compared with the sound field. One release site was approximately along the vibratory axis of the dipole source, and the other was approximately orthogonal to the vibratory axis. The sound field in the tank was fully characterized through measurements of the sound pressure field using hydrophones and acoustic particle motion using an accelerometer. These measurements confirmed that the sound field was a nearly ideal dipole. When released along the dipole vibratory axis, the responding female fish took essentially straight paths to the source. However, when released approximately 90 deg to the source's vibratory axis, the responding females took highly curved paths to the source that were approximately in line with the local particle motion axes. These results indicate that the acoustic cues used by fish during sound-source localization include the axes of particle motion of the local sound field.

Coding of sound direction in the auditory periphery of the lake sturgeon, Acipenser fulvescens.

The lake sturgeon, Acipenser fulvescens, belongs to one of the few extant nonteleost ray-finned fishes and diverged from the main vertebrate lineage about 250 million years ago. The aim of this study was to use this species to explore the peripheral neural coding strategies for sound direction and compare these results to modern bony fishes (teleosts). Extracellular recordings were made from afferent neurons innervating the saccule and lagena of the inner ear while the fish was stimulated using a shaker system. Afferents were highly directional and strongly phase locked to the stimulus. Directional response profiles resembled cosine functions, and directional preferences occurred at a wide range of stimulus intensities (spanning at least 60 dB re 1 nm displacement). Seventy-six percent of afferents were directionally selective for stimuli in the vertical plane near 90° (up down) and did not respond to horizontal stimulation. Sixty-two percent of afferents responsive to horizontal stimulation had their best axis in azimuths near 0° (front back). These findings suggest that in the lake sturgeon, in contrast to teleosts, the saccule and lagena may convey more limited information about the direction of a sound source, raising the possibility that this species uses a different mechanism for localizing sound. For azimuth, a mechanism could involve the utricle or perhaps the computation of arrival time differences. For elevation, behavioral strategies such as directing the head to maximize input to the area of best sensitivity may be used. Alternatively, the lake sturgeon may have a more limited ability for sound source localization compared with teleosts.

Signal-to-noise ratio for source determination and for a comodulated masker in goldfish, Carassius auratus.

The masking effects of white and amplitude comodulated noise were studied with respect to simple signal detection and sound source determination in goldfish. A stimulus generalization method was used to determine the signal-to-noise ratio required to completely determine the signal's characteristics. It was found that the S∕N required for this determination is about 4 dB greater than that required for signal detection, or was about 4 dB greater than the critical masking ratio. This means that the potential harm to fish of a given masking noise is at least 4 dB greater than previously thought, based on critical masking ratios. However, for amplitude comodulated noise between 10 and 50 Hz modulation rate, the potential harmful effects are up to 5.3 dB less than would be predicted from the critical masking ratio for unmodulated noise.

Rethinking sound detection by fishes.

In this paper we reconsider the designation of fishes as being either "hearing specialists" or "hearing generalists," and recommend dropping the terms. We argue that this classification is only vaguely and variously defined in the literature, and that these terms often have unclear and different meaning to different investigators. Furthermore, we make the argument that the ancestral, and most common, mode of hearing in fishes involves sensitivity to acoustic particle motion via direct inertial stimulation of the otolith organ(s). Moreover, any possible pressure sensitivity is the result of the presence of an air bubble (e.g., the swim bladder), and that hearing sensitivity may be enhanced by the fish having a specific connection between the inner ear to a bubble of air. There are data showing that some fish species have a sensitivity to both pressure and motion that is frequency dependent. Thus such species could not possibly be termed as either hearing "generalists" or specialists," and many more species probably could be classified in this way as well. Furthermore, we propose that the term "specialization" be reserved for cases in which a species has some kind of morphological connection or close continuity between the inner ear and an air bubble that affects behavioral sensitivity to sound pressure (i.e., an otophysic connection).

Sound source localization by the plainfin midshipman fish, Porichthys notatus.

The aim of this study was to use plainfin midshipman fish (Porichthys notatus) as a general model to explore how fishes localize an underwater sound source in the relatively simple geometry of a monopole sound field. The robust phonotaxic responses displayed by gravid females toward a monopole sound projector (J-9) broadcasting a low-frequency (90 Hz) tone similar to the fundamental frequency of the male's advertisement call were examined. The projector's sound field was mapped at 5 cm resolution azimuth using an eight-hydrophone array. Acoustic pressure was measured with the array and acoustic particle motion was calculated from pressure gradients between hydrophones. The response pathways of the fish were analyzed from video recordings and compared to the sound field. Gravid females at initial release were directed toward the sound source, and the majority (73%) swam to the playback projector with straight to slightly curved tracks in the direction of the source and in line with local particle motion vectors. In contrast, the initial direction of the control (sound-off) group did not differ from random. This paper reports on a comparison of fish localization behavior with directional cues available in the form of local particle motion vectors.