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Binaural computations involving the convergence of excitatory and inhibitory inputs have been proposed to explain directional sharpening and frequency tuning documented in the brainstem of a teleost fish, the oyster toadfish (Opsanus tau). To assess the presence of inhibitory neurons in the ascending auditory circuit, we used a monoclonal antibody to GABA to evaluate immunoreactivity at three levels of the circuit: the first order descending octaval nucleus (DON), the secondary octaval population (dorsal division), and the midbrain torus semicircularis. We observed a subset of immunoreactive (IR) cells and puncta distributed throughout the neuropil at all three locations. To assess whether contralateral inhibition is present, fluorescent dextran crystals were inserted into dorsal DON to fill contralateral, commissural inputs retrogradely prior to GABA immunohistochemistry. GABA-IR somata and puncta co-occurred with retrogradely filled, GABA-negative auditory projection cells. GABA-IR projection cells were more common in the dorsolateral DON than in the dorsomedial DON, but GABA-IR puncta were common in both dorsolateral and dorsomedial divisions. Our findings demonstrate that GABA is present in the ascending auditory circuit in the brainstem of the toadfish, indicating that GABA-mediated inhibition participates in shaping auditory response characteristics in a teleost fish as in other vertebrates.

The perception of two simultaneous tones was investigated in goldfish using classical respiratory conditioning and a stimulus generalization paradigm. Pairs of tones were used to make up a mixture of 150 Hz and a higher harmonic or a mistuned harmonic. Fish were conditioned to the two-tone mixture and then tested for generalization to several pure tones. The simultaneous tones tended to be segregated in perception, with the generalization gradient for single tones having two peaks corresponding to the frequencies of the tone pairs. There were no consistent differences in the generalization gradients following conditioning to harmonic or inharmonic tone pairs. In addition, experiments were carried out in which the two tones of the pair were heard on alternate trials, always as single tones, followed by generalization tests to single tones. There was more generalization in this experiment, reflecting the fact that conditioning and generalization test stimuli were both single tones. However, the shapes of the generalization gradients were similar to those in which fish were conditioned to two simultaneous tones, indicating that the simultaneity of the tones did not make them harder to segregate. As the frequency separation between the two components narrowed, segregation tended to fail.

SUMMARYComparisons of left and right auditory input are required for sound source localization in most terrestrial vertebrates. Previous physiological and neuroanatomical studies have indicated that binaural convergence is present in the ascending auditory system of the toadfish. In this study, we introduce a new technique, otolith tipping, to reversibly alter directional auditory input to the central nervous system of a fish. The normal directional response pattern (DRP) was recorded extracellularly for auditory cells in the first-order descending octaval nucleus (DON) or the midbrain torus semicircularis (TS) using particle motion stimuli in the horizontal and mid-sagittal planes. The same stimuli were used during tipping of the saccular otolith to evaluate changes in the DRPs. Post-tipping DRPs were generated and compared with the pre-tipping DRPs to ensure that the data had been collected consistently from the same unit. In the DON, ipsilateral or contralateral tipping most often eliminated spike activity, but changes in spike rate(±) and DRP shape were also documented. In the TS, tipping most often caused a change in spike rate (±) and altered the shape or best axis of the DRP. The data indicate that there are complex interactions of excitatory and inhibitory inputs in the DON and TS resulting from the convergence of binaural inputs. As in anurans, but unlike other terrestrial vertebrates,binaural processing associated with encoding the direction of a sound source begins in the first-order auditory nucleus of this teleost.

Classical conditioning and stimulus generalization methods have revealed much about the sense of hearing in non-human animals, and are now used here to investigate how goldfish perceive a variety of complex sounds, including multi-harmonic complexes and rippled noise (RN). In several experiments, animals were conditioned to respond to one type of complex sound, and were then tested for generalization to other sounds differing along one or more acoustic dimensions from the conditioning sounds. Overall, generalization occurred only to the extent that the conditioning and test sounds were essentially similar in spectral range and, in most cases, waveform periodicity. For example, goldfish showed inverted V-shaped generalization gradients to harmonic complexes varying in fundamental frequency after conditioning to complexes having a fundamental frequency of 100 Hz. In several cases, similar gradients were observed whether the fundamental frequency component was present or absent in conditioning and testing complexes, indicating that goldfish, like other vertebrate listeners, do not “miss the fundamental” when it is missing. This generalization pattern tended to disappear when harmonic complexes were used that had random phase relations among the components, or slight mistuning of all components. In a few cases, patterns of generalization were determined by as yet unidentified acoustic features. Goldfish did not generalize to RN or harmonic complexes after conditioning to tones, and vice versa, in spite of the three signal types having fundamental frequency components and periodicity in common. Moreover, goldfish did not generalize robustly to infinitely iterated rippled noise after conditioning to harmonic complexes with a prominent periodic envelope, and vice versa, in spite of the two signal types having similar spectra and pitches as judged by human listeners. These and other results suggest that the pitch of harmonic complexes is prominent in goldfish generalization behavior and that this pitch-like dimension arises primarily from the signal’s periodicity. The perceptions of single tones, RNs, and harmonic complexes having the same fundamental frequency are fundamentally different. It is concluded that the different perceptions of these signals arise in part from differences in periodic envelope prominence and spectral envelope, and possibly in the stochastic versus deterministic natures of their respective waveforms.

SUMMARY Zebrafish (Danio rerio) were placed in small wells that could be driven vertically with a series of calibrated sinusoids. Video images of the fish were obtained and analyzed to determine the levels and frequencies at which the fish responded to the stimulus tones. It was found that fish 4 days post fertilization (dpf) did not respond to the stimulus tones, whereas fish 5 dpf to adult did respond. It was further found that the stimulus thresholds and frequency bandwidth to which the fish responded did not change from 5 dpf to adult; indicating that the otolithic organ adaptations for high-frequency hearing are already present in larval fish. Deflating the swimbladders in adult fish eliminated their response, which is consistent with sensing sound pressure. Deflating the swimbladder in larval fish did not affect their thresholds, which is consistent with sensing the particle motion of the fluid directly. Because adult fish with Weberian ossicles have a greater input to the inner ear for a given sound pressure level (SPL), the finding that the adult and larval fish respond at the same SPL with intact swimbladders suggests that the acoustic startle response threshold is adjusted as the fish develop in order to maintain appropriate reactions to relevant stimuli.

Bimodal cells in the torus semicircularis of the toadfish respond to both directional acoustic stimuli and hydrodynamic stimuli. Our previous physiological work indicated that bimodal cells may be distributed throughout the torus semicircularis. In this study, neurobiotin was used to compare the distribution of auditory-only and bimodal sites and to assess the inputs to those sites. A brief neurobiotin injection with short survival time was used to document the recording location. In other fish, a longer injection and survival time was used at an auditory-only or a bimodal site to fill the axons of the medullary inputs. Auditory-only sites were located in the most dorsal and medial sites in nucleus centralis. Bimodal sites were identified within both nucleus centralis and nucleus ventrolateralis. The greatest number of retrogradely filled cell bodies was found in the descending octaval nucleus following injection at auditory-only recording sites in nucleus centralis. In contrast, retrogradely filled cell bodies were found in both the descending octaval nucleus and the lateral line nucleus medialis following injection at bimodal sites in nucleus centralis or nucleus ventrolateralis. Retrogradely filled cell bodies were located in the dorsal and ventral divisions of the secondary octaval population from injections at either bimodal or auditory-only sites. The secondary octaval population has been implicated in auditory processing based on previous studies of both auditory specialist and auditory generalist fishes; however, this study is the first to reveal the potential role of the secondary octaval population in directional hearing in a fish. Relatively large numbers of retrogradely filled cells around the lateral lemniscus at consistent locations in the medulla indicate that a perilemniscal cell group also might be a component of the directional hearing circuit.

Single-unit recordings were made from areas in the midbrain (torus semicircularis) of the oyster toadfish. We evaluated frequency tuning and directional responses using whole-body oscillation to simulate auditory stimulation by particle motion along axes in the horizontal and mid-sagittal planes. We also tested for bimodality in responses to auditory and hydrodynamic stimuli. One recording location in each animal was marked by a neurobiotin injection to confirm the recording site. Recordings were made in nucleus centralis, nucleus ventrolateralis, and the deep cell layer. Most units were frequency-selective with best frequencies between 50 and 141 Hz. Suppression of activity was apparent in 10% of the cells. Bimodality was common, including inhibition and suppression of background activity by auditory or hydrodynamic stimulation. The majority of the cells were directionally selective with directional response patterns that were sharpened compared with those of primary saccular afferents. The best directional axes were arrayed widely in spherical space, covering most azimuths and elevations. This representation is adequate for the computation of the motional axis of an auditory stimulus for sound source localization.

While particle motion is thought to directly stimulate the inner ear of most fish species, it is difficult to measure and might not be predictable from pressure measurements in a small tank. It is therefore important to replicate experiments conducted relative to pressure measurements using stimuli of known particle motion, to ensure that unmeasured components of the stimulus field do not produce misleading frequency response profiles. The frequency sensitivity of the inner ear of the plainfin midshipman fish, Porichthys notatus, in response to isopressure stimuli has been described. This study now examines the frequency and directional response properties of midshipman saccular afferents in response to whole-body displacements simulating acoustic particle motion. Best frequencies were distributed bimodally, with peaks at 50 Hz and 100 Hz. Most units had cosinusoidally shaped directional response profiles in the horizontal and vertical planes, though some units showed slight deviations from this pattern. A few units (probably saccular efferents) had omnidirectional directional response profiles and did not phase lock to the stimulus waveform. These results are consistent with responses of the midshipman saccular nerve to isopressure stimuli, and strengthen the hypothesis that the frequency sensitivity of the midshipman ear matches the frequency content of behaviorally relevant vocalizations.

This article provides an overview to articles on fish bioacoustics – the study of hearing, sound production, communication, and the lateral line of fishes. Since bioacoustics includes the ear, this section also includes articles on the anatomy of the ear as well as the other important role of the ear beyond hearing, the vestibular sense.

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.

Chapters cannot be read stand-alone. Please see complete SpringerBrief at: http://link.springer.com/book/10.1007/978-3-319-06659-2.

Chapters cannot be read stand-alone. Please see complete SpringerBrief at: http://link.springer.com/book/10.1007/978-3-319-06659-2.

Chapters cannot be read stand-alone. Please see complete SpringerBrief at: http://link.springer.com/book/10.1007/978-3-319-06659-2.

This chapter chronicles the evolution of experiments from 1966 through 2011 that led to determining what fish listen to. By 2009, it became clear that goldfish are listening to the soundscape, like most other animals. This conclusion is based on three conceptions: (1) the fish brain is similar in morphotype to all vertebrate brains; (2) the goldfish, at least, has the processing power to analyze complex soundscapes; and (3) the processing of fish vocalizations couldn’t be a determining factor in the evolution of fish hearing. Goldfish possess the sense of hearing required to process the various sources likely making up a fish’s soundscape. They seem to be able to process the acoustic spectrum. They can process reverberations and reflections and various temporal patterns, and some species can locate the sources of sound using binaural hearing. Suggested here, then, is the notion of environmental soundscapes as the most probably important sources of information to organisms. Environmental information exists to be exploited for appropriate behavior with respect to audible sound sources and events, and fish have the capacity to exploit it for general orientation. This is what fish and other species listen to.

Chapters cannot be read stand-alone. Please see complete SpringerBrief at: http://link.springer.com/book/10.1007/978-3-319-06659-2.

Chapters cannot be read stand-alone. Please see complete SpringerBrief at: http://link.springer.com/book/10.1007/978-3-319-06659-2.

Chapters cannot be read stand-alone. Please see complete SpringerBrief at: http://link.springer.com/book/10.1007/978-3-319-06659-2.

A Brief History of SHAR.- Structures, Mechanisms and Energetics in Temporal Processing.- The Human Auditory Cortex: In Search of the Flying Dutchman.- From Cajal to the Connectome: Building a Neuroanatomical Framework for Understanding the Auditory System.- Recording from Hair Cells.- Three Decades of Tinnitus Related Research.- The Sense of Hearing in Fishes.- A Quarter-Century's Perspective on a Psychoacoustical Approach to Loudness.- Nonsyndromic Deafness: It Ain't Necessarily So.- Evolving Mechanosensory Hair Cells to Hearing Organs by Altering Genes and Their Expression.- The Implications of Discharge Regularity-My Forty-Year Peek into the Vestibular System.- Aging, Hearing Loss and Speech Recognition: Stop Shouting, I Can't Understand You.- Cochlear Mechanics, Otoacoustic Emissions and Medial Olivocochlear Efferents: 20 Years of Advances and Controversies Along with Areas Ripe for New Work.- Examining Fish in the Sea: A European Perspective on Fish Hearing Experiments.- The Behavioral Study of Mammalian Hearing.- Hearing in Insects: The Why, When and How.- The Cognitive Auditory System.- Fundamentals of Hearing in Amniote Vertebrate.- Directional Hearing in Insects and Other Small Animals: The Physics of Pressure-Difference Receiving Ears.- Cortical Representation of Sound Locations: Distributed Representation by Magnitude and Timing of Neural Spike Patterns.- Mechanisms Underlying the Pitch of Pure and Complex Tones.- Unavoidably Delayed: A Personal Perspective of Twenty Years of Research on a Sound Localization Cue.- Size Matters in Hearing: How the Auditory System Normalizes the Sounds of Speech and Music for Source Size.- A Changing View of the Auditory System Obtained from the Ears of Bats.- From Cave Fish to Pile Driving: A Tail of Fish Bioacoustics.- Current Topics in the Study of Sound Conduction to the Inner Ear.- From Degenerative Debris to Neuronal Tracing: An Anterograde View of Auditory Circuits.- Adventures in Bionic Hearing.- My Dull Deaf Ears: Four Millennia of Acquired Hearing Loss.- What's the Use of Genetics?.- Advances in the Understanding of Binaural Information Processing: Consideration of the Stimulus as Processed.- Temporal Processing: Observations on the Psychophysics and Modeling of Temporal Integration and Temporal Resolution.- Psychoacoustics and Auditory Perception.- APPENDIX: Table of Contents from SHAR volumes 1-49.

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%, 7 of the 8 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° 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° ambiguity of source direction from the particle motion vector remains unresolved.

The Gems of the Past: A Brief History of Lateral Line Research in the Context of the Hearing Sciences.- Morphological Diversity, Development, and Evolution of the Mechanosensory Lateral Line System.- The Hydrodynamic of Flow Stimuli.- The Biophysics of the Fish Lateral Line.- Sensory Ecology and Neuroethology of the Lateral Line.- Information Encoding and Processing by the Peripheral Lateral Line System.- The Central Nervous Organization of the Lateral Line System.- Central Processing of Lateral Line Information.- Functional Overlap and Nonoverlap Between Lateral Line and Auditory Systems.- The Hearing Loss, Protection, and Regeneration in the Larval Zebrafish Lateral Line.

This paper considers aspects of the evolution of the vertebrate auditory system from an 'ichthyocentric' perspective. It is argued that all vertebrate auditory systems are required to do certain basic tasks including acoustic feature discrimination, sound source localization, frequency analysis, and auditory scene analysis, among others. These sorts of capabilities arose very early in the evolution of the vertebrates and have been modified by selection in different species. In some cases the same structures have been involved in detection and analysis throughout the vertebrates, while in other cases the mechanism by which the same type of analysis takes place may have changed.

This paper reviews and discusses several investigations of the peripheral neural code for the directional axis of acoustical particle motion in the saccule of two fishes: goldfish ( Carassius auratus ) and toadfish ( Opsanus tau ). Most saccular afferents are directional in the manner of hair cells, having a cosine–shaped directional response pattern. The saccular sensory epithelia are orientated almost vertically in a parasagittal plane. In the horizontal plane, these epithelia are orientated obliquely with respect to the midline. Hair–cell stereocilia project perpendicularly. Thus, directional response patterns of saccular afferents tend to be orientated in azimuth parallel to the orientation of the epithelia in the head. The oblique angle of the toadfish saccule is greater than that of the goldfish, and the range of best directions in the horizontal plane for each species reflects those differing orientations. The azimuth of acoustical particle motion could be computed by comparing the relative activation of the two saccules, as is the case for the ears of most terrestrial vertebrates. The spatial patterns of saccular hair–cell orientation of most fishes thus appear to have little function in azimuthal source location, but for toadfish are probably most important for determining the elevation of monopole sources.

Neurobiotin was injected iontophoretically into saccular afferents of toadfish (Opsanus tau) after intracellular recording to examine dendritic arbors and central projections with respect to the physiological and directional response properties of the cells. Dendritic arbors of 36 afferents were examined in detail. Maximum diameter of the arbor and the number of terminal points were positively correlated with each other, but neither was predictive of spontaneous activity or sensitivity. Best azimuths were centered around 30 degrees -40 degrees, which corresponds to the angle of the saccule with respect to the fish's midline. In general, best elevations for afferents corresponded to hair cell orientations in the region innervated; unexpectedly low elevations obtained from afferents innervating the middle saccule may reflect curvature of the sensory epithelium against the otolith. Three efferent cells were filled partially. The location and large size of the efferent projections indicate that activity along the saccule could be modulated by a single efferent. All afferents projected to the dorsal zone of the descending octaval nucleus (dDON); many afferents bifurcated to terminate in the anterior octaval nucleus, and a few of those also had terminal fields in the medial zone of DON. All afferent projections into the dDON consisted of multiple axon collaterals projecting to numerous sites along the rostral-caudal extent of the nucleus. Variation in terminal field sites also was noted in the medial to lateral axis of the dDON; however, there were no consistent correlations between terminal field locations, physiology, and best directions of the saccular afferents.