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In many animals, vocal-acoustic communication is fundamental for facilitating social behaviors. For the vocal plainfin midshipman fish, the detection and localization of social acoustic signals are critical to the species’ reproductive success. Here, we show that the utricle, an inner ear end organ often thought to primarily serve a vestibular function, serves an auditory function that is seasonally plastic and modulated by the animal’s reproductive state effectively enhancing auditory sensitivity to courting male advertisement calls.

In seasonally breeding vertebrates, hormones coordinate changes in nervous system structure and function to facilitate reproductive readiness and success. Steroid hormones often exert their effects indirectly via regulation of neuromodulators, which in turn can coordinate the modulation of sensory input with appropriate motor output. Female plainfin midshipman fish (Porichthys notatus) undergo increased peripheral auditory sensitivity in time for the summer breeding season, improving their ability to detect mates, which is regulated by steroid hormones. Reproductive females also show differences in catecholaminergic innervation of auditory circuitry compared with winter, non-reproductive females as measured by tyrosine hydroxylase (TH), the rate-limiting enzyme in catecholaminergic synthesis. Importantly, catecholaminergic input to the inner ear from a dopaminergic-specific forebrain nucleus is decreased in the summer and dopamine inhibits the sensitivity of the inner ear, suggesting that gonadal steroids may alter auditory sensitivity by regulating dopamine innervation. In this study, we gonadectomized non-reproductive females, implanted them with estradiol (E2) or testosterone (T), and measured TH immunoreactive (TH-ir) fibers in auditory nuclei where catecholaminergic innervation was previously shown to be seasonally plastic. We found that treatment with T, but not E2, reduced TH-ir innervation in the auditory hindbrain. T-treatment also reduced TH-ir fibers in the forebrain dopaminergic cell group that projects to the inner ear, and likely to the auditory hindbrain. Higher T plasma in the treatment group was correlated with reduced-ir TH terminals in the inner ear. These T-treatment induced changes in TH-ir fibers mimic the seasonal downregulation of dopamine in the midshipman inner ear and provide evidence that steroid hormone regulation of peripheral auditory sensitivity is mediated, in part, by dopamine.

Zebrafish, like all fish species, use sound to learn about their environment. Thus, human-generated (anthropogenic) sound added to the environment has the potential to disrupt the detection of biologically relevant sounds, alter behavior, impact fitness, and produce stress and other effects that can alter the well-being of animals. This review considers the bioacoustics of zebrafish in the laboratory with two goals. First, we discuss zebrafish hearing and the problems and issues that must be considered in any studies to get a clear understanding of hearing capabilities. Second, we focus on the potential effects of sounds in the tank environment and its impact on zebrafish physiology and health. To do this, we discuss underwater acoustics and the very specialized acoustics of fish tanks, in which zebrafish live and are studied. We consider what is known about zebrafish hearing and what is known about the potential impacts of tank acoustics on zebrafish and their well-being. We conclude with suggestions regarding the major gaps in what is known about zebrafish hearing as well as questions that must be explored to better understand how well zebrafish tolerate and deal with the acoustic world they live in within laboratories.

The auditory system of the plainfin midshipman fish ( Porichthys notatus) is an important sensory system used to detect and encode biologically relevant acoustic stimuli important for survival and reproduction including social acoustic signals used for intraspecific communication. Previous work showed that hair cell (HC) density in the midshipman saccule increased seasonally with reproductive state and was concurrent with enhanced auditory saccular sensitivity in both females and type I males. Although reproductive state-dependent changes in HC density have been well characterized in the adult midshipman saccule, less is known about how the saccule changes during ontogeny. Here, we examined the ontogenetic development of the saccule in four relative sizes of midshipman (larvae, small juveniles, large juveniles, and nonreproductive adults) to determine whether the density, total number, and orientation patterns of saccular HCs change during ontogeny. In addition, we also examined whether the total number of HCs in the saccule differ from that of the utricle and lagena in nonreproductive adults. We found that HC density varied across developmental stage. The ontogenetic reduction in HC density was concurrent with an ontogenetic increase in macula area. The orientation pattern of saccular HCs was similar to the standard pattern previously described in other teleost fishes, and this pattern of HC orientation was retained during ontogeny. Lastly, the estimated number of saccular HCs increased with developmental stage from the smallest larvae (2,336 HCs) to the largest nonreproductive adult (145,717 HCs), and in nonreproductive adults estimated HC numbers were highest in the saccule (mean ± SD = 28,479 ± 4,809 HCs), intermediate in the utricle (mean ± SD = 11,008 ± 1,619 HCs) and lowest in the lagena (mean ± SD = 4,560 ± 769 HCs).

Investigators working with fish bioacoustics used to refer to fishes that have a narrow hearing bandwidth and poor sensitivity as “hearing generalists” (or “non-specialists”), while fishes that could detect a wider hearing bandwidth and had greater sensitivity were referred to as specialists. However, as more was learned about fish hearing mechanism and capacities, these terms became hard to apply, since it was clear there were gradations in hearing capabilities. Popper and Fay, in a paper in Hearing Research in 2011, proposed that these terms be dropped because of the gradation. While this was widely accepted by investigators, it is now apparent that the lack of relatively concise terminology for fish hearing capabilities makes it hard to discuss fish hearing. Thus, in this paper we resurrect the terms specialist and non-specialist but use them with modifiers to express the specific structure of function that is considered a specialization. Moreover, this resurrection recognizes that hearing specializations in fishes may not only be related to increased bandwidth and/or sensitivity, but to other, perhaps more important, aspects of hearing such as sound source localization, discrimination between sounds, and detection of sounds in the presence of masking signals.

Vocal courtship is vital to the reproductive success of many vertebrates and is therefore a highly-motivated behavioral state. Catecholamines have been shown to play an essential role in the expression and maintenance of motivated vocal behavior, such as the coordination of vocal-motor output in songbirds. However, it is not well-understood if this relationship applies to anamniote vocal species. Using the plainfin midshipman fish model, we tested whether specific catecholaminergic (i.e., dopaminergic and noradrenergic) nuclei and nodes of the social behavior network (SBN) are differentially activated in vocally courting (humming) versus non-humming males. Herein, we demonstrate that tyrosine hydroxylase immunoreactive (TH-ir) neuron number in the noradrenergic locus coeruleus (LC) and induction of cFos (an immediate early gene product and proxy for neural activation) in the preoptic area differentiated humming from non-humming males. Furthermore, we found relationships between activation of the LC and SBN nuclei with the total amount of time that males spent humming, further reinforcing a role for these specific brain regions in the production of motivated reproductive-related vocalizations. Finally, we found that patterns of functional connectivity between catecholaminergic nuclei and nodes of the SBN differed between humming and non-humming males, supporting the notion that adaptive behaviors (such as the expression of advertisement hums) emerge from the interactions between various catecholaminergic nuclei and the SBN.

Vocal species use acoustic signals to facilitate diverse behaviors such as mate attraction and territorial defense. However, little is known regarding the neural substrates that interpret such divergent conspecific signals. Using the plainfin midshipman fish model, we tested whether specific catecholaminergic (i.e., dopaminergic and noradrenergic) nuclei and nodes of the social behavior network (SBN) are differentially responsive following exposure to playbacks of divergent social signals in sneaker males. We chose sneaker (type II) males since they attempt to steal fertilizations from territorial type I males who use an advertisement call (hum) to attract females yet are also subjected to vocal agonistic behavior (grunts) by type I males. We demonstrate that induction of cFos (an immediate early gene product and proxy for neural activation) in two forebrain dopaminergic nuclei is greater in sneaker males exposed to hums but not grunts compared to ambient noise, suggesting hums preferentially activate these nuclei, further asserting dopamine as an important regulator of social-acoustic behaviors. Moreover, acoustic exposure to social signals with divergent salience engendered contrasting shifts in functional connectivity between dopaminergic nuclei and nodes of the SBN, supporting the idea that interactions between these two circuits may underlie adaptive decision-making related to intraspecific male competition.

The auditory system of the plainfin midshipman fish (Porichthys notatus) is an important sensory system used to detect and encode biologically relevant acoustic stimuli important for survival and reproduction including social acoustic signals used for intraspecific communication. Previous work showed that hair cell (HC) density in the midshipman saccule increased seasonally with reproductive state and was concurrent with enhanced auditory saccular sensitivity in both females and type I males. Although reproductive state-dependent changes in HC density have been well characterized in the adult midshipman saccule, less is known about how the saccule changes during ontogeny. Here, we examined the ontogenetic development of the saccule in four relative sizes of midshipman (larvae, small juveniles, large juveniles, and nonreproductive adults) to determine whether the density, total number, and orientation patterns of saccular HCs change during ontogeny. In addition, we also examined whether the total number of HCs in the saccule differ from that of the utricle and lagena in nonreproductive adults. We found that HC density varied across developmental stage. The ontogenetic reduction in HC density was concurrent with an ontogenetic increase in macula area. The orientation pattern of saccular HCs was similar to the standard pattern previously described in other teleost fishes, and this pattern of HC orientation was retained during ontogeny. Lastly, the estimated number of saccular HCs increased with developmental stage from the smallest larvae (2,336 HCs) to the largest nonreproductive adult (145,717 HCs), and in nonreproductive adults estimated HC numbers were highest in the saccule (mean ± SD = 28,479 ± 4,809 HCs), intermediate in the utricle (mean ± SD = 11,008 ± 1,619 HCs) and lowest in the lagena (mean ± SD = 4,560 ± 769 HCs).

The plainfin midshipman

The plainfin midshipman fish (Porichthys notatus) is an established model for investigating acoustic communication because the reproductive success of this species is dependent on the production and reception of social acoustic signals. Previous work showed that female midshipman have swim bladders with rostral horn-like extensions that project close to the saccule and lagena, while nesting (type I) males lack such rostral swim bladder extensions. The relative close proximity of the swim bladder to the lagena should increase auditory sensitivity to sound pressure and higher frequencies. Here, we test the hypothesis that the swim bladder of female midshipman enhances lagenar sensitivity to sound pressure and higher frequencies. Evoked potentials were recorded from auditory hair cell receptors in the lagena in reproductive females with intact (control condition) and removed (treated condition) swim bladders while pure tone stimuli (85–1005 Hz) were presented by an underwater speaker. Females with intact swim bladders had auditory thresholds 3–6 dB lower than females without swim bladders over a range of frequencies from 85 to 405 Hz. At frequencies from 545 to 1005 Hz, only females with intact swim bladders had measurable auditory thresholds (150–153 dB re. 1 µPa). The higher percentage of evoked lagenar potentials recorded in control females at frequencies >505 Hz indicates that the swim bladder extends the bandwidth of detectable frequencies. These findings reveal that the swim bladders in female midshipman can enhance lagenar sensitivity to sound pressure and higher frequencies, which may be important for the detection of behaviorally relevant social signals.

The plainfin midshipman, Porichthys notatus, is a soniferous marine teleost fish that generates acoustic signals for intraspecific social communication. Nocturnally active males and females rely on their auditory sense to detect and locate vocally active conspecifics during social behaviors. Previous work showed that the midshipman inner ear saccule and lagena are highly adapted to detect and encode socially relevant acoustic stimuli, but the auditory sensitivity and function of the midshipman utricle remain largely unknown. Here, we characterize the auditory evoked potentials from hair cells in the utricle of non-reproductive type I males and test the hypothesis that the midshipman utricle is sensitive to behaviorally-relevant acoustic stimuli. Hair cell potentials were recorded from the rostral, medial and caudal regions of the utricle in response to pure tone stimuli presented by an underwater speaker. We show that the utricle is highly sensitive to particle motion stimuli produced by an underwater speaker positioned in the horizontal plane. Utricular potentials were recorded across a broad range of frequencies with lowest particle acceleration (dB re: 1 ms−2) thresholds occurring at 105 Hz (lowest frequency tested; mean threshold=-32 dB re: 1 ms−2) and highest thresholds at 605 to 1005 Hz (mean threshold range=−5 to −4 dB re: 1 ms−2). The high gain and broadband frequency sensitivity of the utricle suggests that it likely serves a primary auditory function and is well suited to detect conspecific vocalizations including broadband agonistic signals and the multiharmonic advertisement calls produce by reproductive type I males.

In nature, it can be challenging to figure out whether success at attracting mates and reproducing is due to something intrinsic about an individual or something about the quality of the resources they possess. In a series of lab and field studies using the plainfin midshipman fish, we show that both factors are complex and that resource quality can impose a limit on reproductive success regardless of the quality of the resource owner.

While the peripheral auditory system of fish has been well studied, less is known about how the fish’s brain and central auditory system process complex social acoustic signals. The plainfin midshipman fish, Porichthys notatus, has become a good species for investigating the neural basis of acoustic communication because the production and reception of acoustic signals is paramount for this species’ reproductive success. Nesting males produce long-duration advertisement calls that females detect and localize among the noise in the intertidal zone to successfully find mates and spawn. How female midshipman are able to discriminate male advertisement calls from environmental noise and other acoustic stimuli is unknown. Using the immediate early gene product cFos as a marker for neural activity, we quantified neural activation of the ascending auditory pathway in female midshipman exposed to conspecific advertisement calls, heterospecific white seabass calls, or ambient environment noise. We hypothesized that auditory hindbrain nuclei would be activated by general acoustic stimuli (ambient noise and other biotic acoustic stimuli) whereas auditory neurons in the midbrain and forebrain would be selectively activated by conspecific advertisement calls. We show that neural activation in two regions of the auditory hindbrain, i.e., the rostral intermediate division of the descending octaval nucleus and the ventral division of the secondary octaval nucleus, did not differ via cFos immunoreactive (cFos-ir) activity when exposed to different acoustic stimuli. In contrast, female midshipman exposed to conspecific advertisement calls showed greater cFos-ir in the nucleus centralis of the midbrain torus semicircularis compared to fish exposed only to ambient noise. No difference in cFos-ir was observed in the torus semicircularis of animals exposed to conspecific versus heterospecific calls. However, cFos-ir was greater in two forebrain structures that receive auditory input, i.e., the central posterior nucleus of the thalamus and the anterior tuberal hypothalamus, when exposed to conspecific calls versus either ambient noise or heterospecific calls. Our results suggest that higher-order neurons in the female midshipman midbrain torus semicircularis, thalamic central posterior nucleus, and hypothalamic anterior tuberal nucleus may be necessary for the discrimination of complex social acoustic signals. Furthermore, neurons in the central posterior and anterior tuberal nuclei are differentially activated by exposure to conspecific versus other acoustic stimuli.

Age-related hearing loss (ARHL), also known as presbycusis, is a widespread and debilitating condition impacting many older adults. Conventionally, researchers utilize mammalian model systems or human cadaveric tissue to study ARHL pathology. Recently, the zebrafish has become an effective and tractable model system for a wide variety of genetic and environmental auditory insults, but little is known about the incidence or extent of ARHL in zebrafish and other non-mammalian models. Here, we evaluated whether zebrafish exhibit age-related loss in auditory sensitivity. The auditory sensitivity of adult wild-type zebrafish (AB/WIK strain) from three adult age subgroups (13-month, 20-month, and 37-month) was characterized using the auditory evoked potential (AEP) recording technique. AEPs were elicited using pure tone stimuli (115–4500 Hz) presented via an underwater loudspeaker and recorded using shielded subdermal metal electrodes. Based on measures of sound pressure and particle acceleration, the mean AEP thresholds of 37-month-old fish [mean sound pressure level (SPL) = 122.2 dB ± 2.2 dB SE re: 1 μPa; mean particle acceleration level (PAL) = -27.5 ± 2.3 dB SE re: 1 ms−2] were approximately 9 dB higher than that of 20-month-old fish [(mean SPL = 113.1 ± 2.7 dB SE re: 1 μPa; mean PAL = -37.2 ± 2.8 dB re: 1 ms−2; p = 0.007)] and 6 dB higher than that of 13-month-old fish [(mean SPL = 116.3 ± 2.5 dB SE re: 1 μPa; mean PAL = -34.1 ± 2.6 dB SE re: 1 ms−2; p = 0.052)]. Lowest AEP thresholds for all three age groups were generally between 800 Hz and 1850 Hz, with no evidence for frequency-specific age-related loss. Our results suggest that zebrafish undergo age-related loss in auditory sensitivity, but the form and magnitude of loss is markedly different than in mammals, including humans. Future work is needed to further describe the incidence and extent of ARHL across vertebrate groups and to determine which, if any, ARHL mechanisms may be conserved across vertebrates to support meaningful comparative/translational studies.

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.

Adult female and nesting (type I) male midshipman fish (Porichthys notatus) exhibit an adaptive form of auditory plasticity for the enhanced detection of social acoustic signals. Whether this adaptive plasticity also occurs in “sneaker” type II males is unknown. Here, we characterize auditory-evoked potentials recorded from hair cells in the saccule of reproductive and non-reproductive “sneaker” type II male midshipman to determine whether this sexual phenotype exhibits seasonal, reproductive state-dependent changes in auditory sensitivity and frequency response to behaviorally relevant auditory stimuli. Saccular potentials were recorded from the middle and caudal region of the saccule while sound was presented via an underwater speaker. Our results indicate saccular hair cells from reproductive type II males had thresholds based on measures of sound pressure and acceleration (re. 1 µPa and 1 ms−2, respectively) that were ~8–21 dB lower than non-reproductive type II males across a broad range of frequencies, which include the dominant higher frequencies in type I male vocalizations. This increase in type II auditory sensitivity may potentially facilitate eavesdropping by sneaker males and their assessment of vocal type I males for the selection of cuckoldry sites during the breeding season.

The plainfin midshipman (Porichthys notatus) is an acoustically communicative teleost fish. Here, we evaluated auditory evoked potentials (AEPs) in reproductive female midshipman exposed to tones at or near dominant frequencies of the male midshipman advertisement call. An initial series of experiments characterized AEPs at behaviorally relevant suprathreshold sound levels (130–140 dB SPL re. 1 µPa). AEPs decreased in magnitude with increasing stimulus frequency and featured a stereotyped component at twice the stimulus frequency. Recording electrode position was varied systematically and found to affect AEP magnitude and phase characteristics. Later experiments employed stimuli of a single frequency to evaluate contributions of the saccule to the AEP, with particular attention to the effects of sound source azimuth on AEP amplitude. Unilateral excision of saccular otoliths (sagittae) decreased AEP amplitude; unexpectedly, decreases differed for right versus left otolith excision. A final set of experiments manipulated the sound pressure-responsive swim bladder. Swim bladder excision further reduced the magnitude of AEP responses, effectively eliminating responses at the standard test intensity (130 dB SPL) in some animals. Higher-intensity stimulation yielded response minima at forward azimuths ipsilateral to the excised sagitta, but average cross-azimuth modulation generally remained slight. Collectively, the data underscore that electrode position is an essential variable to control in fish AEP studies and suggest that in female midshipman: (1) the saccule contributes to the AEP, but its directionality as indexed by the AEP is limited, (2) a left–right auditory asymmetry may exist and (3) the swim bladder provides gain in auditory sensitivity that may be important for advertisement call detection and phonotaxis.

The plainfin midshipman fish, Porichthys notatus, is a seasonally breeding, nocturnal marine teleost fish that produces acoustic signals for intraspecific social communication. Females rely on audition to detect and locate “singing” males that produce multiharmonic advertisement calls in the shallow-water, intertidal breeding environments. Previous work showed that females possess sexually-dimorphic, horn-like rostral swim bladder extensions that extend toward the primary auditory end organs, the saccule and lagena. Here, we test the hypothesis that the rostral swim bladder extensions in females increase auditory sensitivity to sound pressure and higher frequencies, which potentially could enhance mate detection and localization in shallow water habitats. We recorded the auditory evoked potentials that originated from hair cell receptors in the saccule of control females with intact swim bladders and compared them with that from treated females (swim bladders removed) and type I males (intact swim bladders lacking rostral extensions). Saccular potentials were recorded from hair cell populations in vivo while behaviorally relevant pure tone stimuli (75-1005 Hz) were presented by an underwater speaker. Results indicate that control females were approximately 5-11 dB (re: 1 µPa) more sensitive to sound pressure than treated females and type I males at the frequencies tested. A higher percentage of the evoked saccular potentials were recorded from control females at frequencies >305 Hz than from treated females and type I males. This enhanced sensitivity in females to sound pressure and higher frequencies may facilitate the acquisition of auditory information needed for conspecific localization and mate choice decisions during the breeding season.

The primary goal of this volume is to provide an updated perspective on the topics of electrogenesis and electroreception in fishes. Throughout, there is an emphasis on how comparative perspectives can inform general issues regarding the neural mechanisms of behavior, from detailed comparisons among related species having divergent phenotypes to broad comparisons across distantly related clades having similar phenotypes. The underlying theme throughout is that evolution provides a natural experiment that can be exploited to relate variation in behavior to variation in its neural substrates. This allows for the development and testing of hypotheses regarding the neural control of behavior and for distinguishing generally applicable principles from clade-specific differences. The chapters cover a range of topics including the evolution and development of electric organs and electroreceptors, electrosensory transduction, evolutionary drivers and biophysical bases of electric signal diversity, influences of hormones and motor systems on electrosensory processing, envelope and temporal coding, use of control theory to characterize active sensing, and the role of active electrolocation and spatial learning in behavior. In this introductory chapter, a brief history of research on electrogenesis and electroreception in fishes is presented, with a summary of some of the most important neuroethological studies in electric fish that have contributed greatly to our understanding of brain function and the neural basis of behavior. The field of electroreception research continues to provide fertile ground for using comparative frameworks to understand the neurobiology of animal communication, social behavior, orientation and navigation, and the evolution of information processing.

Summary Dopamine is integral to attentional and motivational processes, but studies are largely restricted to the central nervous system. In mammals [ 1 , 2 ] and fishes [ 3 , 4 ], central dopaminergic neurons project to the inner ear and could modulate acoustic signals at the earliest stages of processing. Studies in rodents show dopamine inhibits cochlear afferent neurons and protects against noise-induced acoustic injury [ 5 , 6 , 7 , 8 , 9 , 10 ]. However, other functions for inner ear dopamine have not been investigated, and the effect of dopamine on peripheral auditory processing in non-mammalians remains unknown [ 11 , 12 ]. Insights could be gained by studies conducted in the context of intraspecific acoustic communication. We present evidence from a vocal fish linking reproductive-state-dependent changes in auditory sensitivity with seasonal changes in the dopaminergic efferent system in the saccule, their primary organ of hearing. Plainfin midshipman (Porichthys notatus) migrate from deep-water winter habitats to the intertidal zone in the summer to breed. Nesting males produce nocturnal vocalizations to attract females [ 13 ]. Both sexes undergo seasonal enhancement of hearing sensitivity at the level of the hair cell [ 14 , 15 , 16 ], increasing the likelihood of detecting conspecific signals [ 17 , 18 ]. Importantly, reproductive females concurrently have reduced dopaminergic input to the saccule [ 19 ]. Here, we show that dopamine decreases saccule auditory sensitivity via a D2-like receptor. Saccule D2a receptor expression is reduced in the summer and correlates with sensitivity within and across seasons. We propose that reproductive-state-dependent changes to the dopaminergic efferent system provide a release of inhibition in the saccule, enhancing peripheral encoding of social-acoustic signals.

The plainfin midshipman fish (Porichthys notatus) is a species of marine teleost that produces acoustic signals that are important for mediating social behavior. The auditory sensitivity of the saccule is well established in this species, but the sensitivity and function of the midshipman’s putative auditory lagena are unknown. Here, we characterize the auditory-evoked potentials from hair cells in the lagena of reproductive type I males to determine the frequency response and auditory sensitivity of the lagena to behaviorally relevant acoustic stimuli. Lagenar potentials were recorded from the caudal and medial region of the lagena, while acoustic stimuli were presented by an underwater speaker. Our results indicate that the midshipman lagena has a similar low-frequency sensitivity to that of the midshipman saccule based on sound pressure and acceleration (re: 1 µPa and 1 ms(−2), respectively), but the thresholds of the lagena were higher across all frequencies tested. The relatively high auditory thresholds of the lagena may be important for encoding high levels of behaviorally relevant acoustic stimuli when close to a sound source.

The plainfin midshipman fish (Porichthys notatus) is a nocturnal, seasonally breeding, intertidal-nesting teleost fish that produces social acoustic signals for intraspecific communication. Type I or “nesting” males produce agonistic and reproductive-related acoustic signals including a multiharmonic advertisement call during the summer breeding season. Previous work showed that type I male auditory sensitivity of the saccule, the primary midshipman auditory end organ, changes seasonally with reproductive state such that reproductive males become more sensitive and better suited than nonreproductive males to detect the dominant frequencies contained within type I vocalizations. Here, we examine whether reproductive type I males also exhibit reproductive-state dependent changes in hair cell (HC) density in the three putative auditory end organs (saccule, lagena, and utricle). We show that saccular HC density was greater in reproductive type I males compared to nonreproductive type I males, and that the increase in HC density occurs throughout the saccular epithelium in both the central and marginal epithelia regions. We also show as saccular HC density increases there is a concurrent decrease in saccular support cell (SC) density in reproductive type I males with no overall change in total cell density (i.e., HC + SC). In contrast, we did not observe any seasonal changes in HC density in the utricle or lagena between nonreproductive and reproductive type I males. In addition, we compare the saccular HC densities in reproductive type I males with that of reproductive females and show that females have greater saccular HC densities, which suggest a sexually dimorphic difference in HC receptor density between the two sexual phenotypes, at least during the summer breeding season.

While the peripheral auditory system of fishes has been well studied, less is known about how the fish’s brain and central auditory system process complex social acoustic signals. The plainfin midshipman fish, Porichthys notatus, has become a good species for investigating the neural basis of acoustic communication because the production and reception of acoustic signals is paramount for this species’ reproductive success. Nesting males produce long duration advertisement calls that females detect and localize amongst the noise in the intertidal zone to successfully find mates and spawn. How female midshipman are able to discriminate male advertisement calls from environmental noise and other acoustic stimuli is unknown. Using the immediate early gene product cFos as a marker for neural activity, we quantified neural activation of the ascending auditory pathway in female midshipman exposed to conspecific advertisement calls, heterospecific white seabass calls or ambient environment noise. We hypothesized that auditory hindbrain nuclei would be activated by general acoustic stimuli (ambient noise and other biotic acoustic stimuli) whereas auditory neurons in the midbrain and forebrain would be selectively activated by conspecific advertisement calls. We show that neural activation in two regions of the auditory hindbrain, the rostral intermediate division of the descending octaval nucleus and the ventral division of the secondary octaval nucleus, did not differ via cFos immunoreactive (cFos-ir) activity when exposed to different acoustic stimuli. In contrast, female midshipman exposed to conspecific advertisement calls showed greater cFos-ir in the nucleus centralis of the midbrain torus semicircularis compared to fish exposed only to ambient noise. No difference in cFos-ir was observed in the torus semicircularis of animals exposed to conspecific versus heterospecific calls. However, cFos-ir was greater in two forebrain structures that receive auditory input, the central posterior nucleus of the thalamus and the anterior tuberal hypothalamus, when exposed to conspecific calls versus exposure to either ambient noise or heterospecific calls. Our results suggest that higher order neurons in the female midshipman midbrain torus semicircularis, thalamic central posterior nucleus and hypothalamic anterior tuberal nucleus may be necessary for the discrimination of complex, specie-specific social acoustic signals. Furthermore, neurons in the central posterior and anterior tuberal nuclei are differentially activated by exposure to conspecific vs. other acoustic stimuli.

Little is known regarding the coordination of audition with decision-making and subsequent motor responses that initiate social behavior including mate localization during courtship. Using the midshipman fish model, we tested the hypothesis that the time spent by females attending and responding to the advertisement call is correlated with the activation of a specific subset of catecholaminergic (CA) and social decision-making network (SDM) nuclei underlying auditory- driven sexual motivation. In addition, we quantified the relationship of neural activation between CA and SDM nuclei in all responders with the goal of providing a map of functional connectivity of the circuitry underlying a motivated state responsive to acoustic cues during mate localization. In order to make a baseline qualitative comparison of this functional brain map to unmotivated females, we made a similar correlative comparison of brain activation in females who were unresponsive to the advertisement call playback. Our results support an important role for dopaminergic neurons in the periventricular posterior tuberculum and ventral thalamus, putative A11 and A13 tetrapod homologues, respectively, as well as the posterior parvocellular preoptic area and dorsomedial telencephalon, (laterobasal amygdala homologue) in auditory attention and appetitive sexual behavior in fishes. These findings may also offer insights into the function of these highly conserved nuclei in the context of auditory-driven reproductive social behavior across vertebrates.

Seasonal changes in reproductive-related vocal behavior are widespread among fishes. This review highlights recent studies of the vocal plainfin midshipman fish, Porichthys notatus, a neuroethological model system used for the past two decades to explore neural and endocrine mechanisms of vocal-acoustic social behaviors shared with tetrapods. Integrative approaches combining behavior, neurophysiology, neuropharmacology, neuroanatomy, and gene expression methodologies have taken advantage of simple, stereotyped and easily quantifiable behaviors controlled by discrete neural networks in this model system to enable discoveries such as the first demonstration of adaptive seasonal plasticity in the auditory periphery of a vertebrate as well as rapid steroid and neuropeptide effects on vocal physiology and behavior. This simple model system has now revealed cellular and molecular mechanisms underlying seasonal and steroid-driven auditory and vocal plasticity in the vertebrate brain.

Overexposure to loud noise is known to lead to deficits in auditory sensitivity and perception. We studied the effects of noise exposure on sensorimotor behaviors of larval (5–7 days post-fertilization) zebrafish (Danio rerio), particularly the auditory-evoked startle response and hearing sensitivity to acoustic startle stimuli. We observed a temporary 10–15 dB decrease in startle response threshold after 18 h of flat-spectrum noise exposure at 20 dB re·1 ms(−2). Larval zebrafish also exhibited decreased habituation to startle-inducing stimuli following noise exposure. The noise-induced sensitization was not due to changes in absolute hearing thresholds, but was specific to the auditory-evoked escape responses. The observed noise-induced sensitization was disrupted by AMPA receptor blockade using DNQX, but not NMDA receptor blockade. Together, these experiments suggest a complex effect of noise exposure on the neural circuits mediating auditory-evoked behaviors in larval zebrafish.

Although the neuroanatomical distribution of catecholaminergic (CA) neurons has been well documented across all vertebrate classes, few studies have examined CA connectivity to physiologically and anatomically identified neural circuitry that controls behavior. The goal of this study was to characterize CA distribution in the brain and inner ear of the plainfin midshipman fish (Porichthys notatus) with particular emphasis on their relationship with anatomically labeled circuitry that both produces and encodes social acoustic signals in this species. Neurobiotin labeling of the main auditory end organ, the saccule, combined with tyrosine hydroxylase immunofluorescence (TH-ir) revealed a strong CA innervation of both the peripheral and central auditory system. Diencephalic TH-ir neurons in the periventricular posterior tuberculum, known to be dopaminergic, send ascending projections to the ventral telencephalon and prominent descending projections to vocal-acoustic integration sites, notably the hindbrain octavolateralis efferent nucleus, as well as onto the base of hair cells in the saccule via nerve VIII. Neurobiotin backfills of the vocal nerve in combination with TH-ir revealed CA terminals on all components of the vocal pattern generator, which appears to largely originate from local TH-ir neurons but may include input from diencephalic projections as well. This study provides strong neuroanatomical evidence that catecholamines are important modulators of both auditory and vocal circuitry and acoustic-driven social behavior in midshipman fish. This demonstration of TH-ir terminals in the main end organ of hearing in a nonmammalian vertebrate suggests a conserved and important anatomical and functional role for dopamine in normal audition.

In humans, excessive noise exposure from occupational or recreational sources causes permanent hearing loss. Similarly, exposure to underwater anthropogenic noise can cause hearing loss in aquatic organisms, including fish. While fish can recover from noise-induced hearing loss, underwater noise exposure can cause behavioral changes that reduce organismal fitness. In all vertebrates, acoustic trauma can cause damage to sensory hair cells. To better study the effects of noise on hair cells, we have developed a noise exposure system that uses broadband sound to damage hair cells of the inner ear and lateral line of larval zebrafish. Acoustic over-exposure kills hair cells in an intensity- and time-dependent manner, with maximum hair cell damage observed 72 hours after noise exposure. This time course is consistent with mammalian studies, where hair cell death occurs days to weeks after noise exposure. Other features of acoustic trauma are also conserved between zebrafish and mammals, including activation of apoptotic signaling cascades and changes in hair cell-afferent synapses. These studies demonstrate that larval zebrafish are a tractable new model for studies of noise-induced hair cell death. However, our acoustic trauma system could also be used in other species, allowing for new studies of underwater noise in larval fishes.

SUMMARYZebrafish (Danio rerio) have become a valuable model for investigating the molecular genetics and development of the inner ear in vertebrates. In this study, we employed a prepulse inhibition (PPI) paradigm to assess hearing in larval wild-type (AB) zebrafish during early development at 5–6 days post-fertilization (d.p.f.). We measured the PPI of the acoustic startle response in zebrafish using a 1-dimensional shaker that simulated the particle motion component of sound along the fish's dorsoventral axis. The thresholds to startle-inducing stimuli were determined in 5–6 d.p.f. zebrafish, and their hearing sensitivity was then characterized using the thresholds of prepulse tone stimuli (90–1200 Hz) that inhibited the acoustic startle response to a reliable startle stimulus (820 Hz at 20 dB re. 1 m s−2). Hearing thresholds were defined as the minimum prepulse tone level required to significantly reduce the startle response probability compared with the baseline (no-prepulse) condition. Larval zebrafish showed greatest auditory sensitivity from 90 to 310 Hz with corresponding mean thresholds of −19 to −10 dB re. 1 m s−2, respectively. Hearing thresholds of prepulse tones were considerably lower than previously predicted by startle response assays. The PPI assay was also used to investigate the relative contribution of the lateral line to the detection of acoustic stimuli. After aminoglycoside-induced neuromast hair-cell ablation, we found no difference in PPI thresholds between treated and control fish. We propose that this PPI assay can be used to screen for novel zebrafish hearing mutants and to investigate the ontogeny of hearing in zebrafish and other fishes.

Zebrafish are increasingly used in auditory studies, in part due to the development of several transgenic lines that express hair cell-specific fluorescent proteins. However, it is largely unknown how transgene expression influences auditory phenotype. We previously observed reduced auditory sensitivity in adult Brn3c:mGFP transgenic zebrafish, which express membrane-bound green fluorescent protein (GFP) in sensory hair cells. Here, we examine the auditory sensitivity of zebrafish from multiple transgenic and background strains. We recorded auditory evoked potentials in adult animals and observed significantly higher auditory thresholds in three lines that express hair cell-specific GFP. There was no obvious correlation between hair cell density and auditory thresholds, suggesting that reduced sensitivity was not due to a reduction in hair cell density. FM1-43 uptake was reduced in Brn3c:mGFP fish but not in other lines, suggesting that a mechanotransduction defect may be responsible for the auditory phenotype in Brn3c animals, but that alternate mechanisms underlie the increased AEP thresholds in other lines. We found reduced prepulse inhibition (a measure of auditory-evoked behavior) in larval Brn3c animals, suggesting that auditory defects develop early in this line. We also found significant differences in auditory sensitivity between adults of different background strains, akin to strain differences observed in mouse models of auditory function. Our results suggest that researchers should exercise caution when selecting an appropriate zebrafish transgenic or background strain for auditory studies.

Sounds provide fishes with important information used to mediate behaviors such as predator avoidance, prey detection, and social communication. How we measure auditory capabilities in fishes, therefore, has crucial implications for interpreting how individual species use acoustic information in their natural habitat. Recent analyses have highlighted differences between behavioral and electrophysiologically determined hearing thresholds, but less is known about how physiological measures at different auditory processing levels compare within a single species. Here we provide one of the first comparisons of auditory threshold curves determined by different recording methods in a single fish species, the soniferous Hawaiian sergeant fish Abudefduf abdominalis, and review past studies on representative fish species with tuning curves determined by different methods. The Hawaiian sergeant is a colonial benthic-spawning damselfish (Pomacentridae) that produces low-frequency, low-intensity sounds associated with reproductive and agonistic behaviors. We compared saccular potentials, auditory evoked potentials (AEP), and single neuron recordings from acoustic nuclei of the hindbrain and midbrain torus semicircularis. We found that hearing thresholds were lowest at low frequencies (~75-300 Hz) for all methods, which matches the spectral components of sounds produced by this species. However, thresholds at best frequency determined via single cell recordings were ~15-25 dB lower than those measured by AEP and saccular potential techniques. While none of these physiological techniques gives us a true measure of the auditory "perceptual" abilities of a naturally behaving fish, this study highlights that different methodologies can reveal similar detectable range of frequencies for a given species, but absolute hearing sensitivity may vary considerably.

Fish represent the largest group of vertebrates and display the greatest diversity of auditory structures. However, studies addressing how the form and function of the auditory system change during development to enhance perception of the acoustic environment are rather sparse in this taxon compared to other vertebrate groups. An ontogenetic perspective of the auditory system in fishes provides a readily testable framework for understanding structure-function relationships. Additionally, studying ancestral models such as fish can convey valuable comparable information across vertebrates, as early developmental events are often evolutionary conserved. This chapter reviews the literature on the morphological development of the fish auditory system, with particular focus on the inner ear structures that evolve from an otic placode during early embryonic development and then continue to undergo differentiation and maturation in the postembryonic phase. Moreover, the chapter provides a systematic overview of how auditory sensitivity develops during ontogeny. Although most studies indicate a developmental improvement in auditory sensitivity, there is considerably species-specific variation. Lastly, the paucity of information and literature concerning the development of auditory capabilities for social communication in fishes is also discussed. Further investigation on the development of structure and function of the fish auditory system is recommended in order to obtain a deeper understanding of how ontogenetic morphological changes in the auditory pathway relate to modifications in acoustic reception, auditory processing, and the capacity to communicate acoustically.

This paper reviews recent studies on the effects of hatchery rearing on the auditory and lateral line systems of salmonid fishes. Major conclusions are that (1) hatchery-reared juveniles exhibit abnormal lateral line morphology (relative to wild-origin conspecifics), suggesting that the hatchery environment affects lateral line structure, perhaps due to differences in the hydrodynamic conditions of hatcheries versus natural rearing environments, and (2) hatchery-reared salmonids have a high proportion of abnormal otoliths, a condition associated with reduced auditory sensitivity and suggestive of inner ear dysfunction.

A fundamental goal of neuroscience is to understand how hormones modulate neural circuits and behavior. Hearing and Hormones reviews the growing literature showing that hormones can regulate auditory physiology and anatomy, and the perception of acoustic signals across a broad range of animal taxa, including humans. · Hearing and Hormones: Paying Homage to the Comparative Approach by Andrew H. Bass · Hormone-Dependent Plasticity of Auditory Systems in Fishes by Paul M. Forlano, Karen P. Maruska, Joseph A. Sisneros, and Andrew H. Bass · Effects of Steroid Hormones on Hearing and Communication in Frogs by Walt Wilczynski and Sabrina S. Burmeister · Modulation of Peripheral and Central Auditory Processing by Estrogens in Birds by Melissa L. Caras and Luke Remage-Healey · Hormones and the Incentive Salience of Bird Song by Donna L. Maney and Carlos A. Rodriguez-Saltos · Hormone-Dependent and Experience-Dependent Auditory Plasticity for Social Communication by Kelly K. Chong and Robert C. Liu · Thyroid Hormone and the Mammalian Auditory System by Douglas Forrest and Lily Ng · Hormone Replacement Therapy and Its Effects on Human Hearing by Robert D. Frisina and D. Robert Frisina About the Editors: Andrew H. Bass is Professor in the Department of Neurobiology and Behavior, and Senior Associate Vice Provost for Research at Cornell University. Joseph A. Sisneros is Associate Professor in the Department of Psychology and an adjunct Associate Professor in the Department of Biology at the University of Washington. Richard R. Fay is Distinguished Research Professor of Psychology at Loyola University Chicago. Arthur N. Popper is Professor Emeritus and Research Professor in the Department of Biology at the University of Maryland, College Park. About the Series: The Springer Handbook of Auditory Research presents a series of synthetic reviews of fundamental topics dealing with auditory systems. Each volume is independent and authoritative; taken as a set, this series is the definitive resource in the field

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.

The Effects of Noise on Aquatic Life is an international conference series that was started by Arthur N. Popper and Anthony D. Hawkins in Nyborg, Denmark, in 2007. Volume 27 of POMA brings together articles based on many of the presentations at the fourth conference that took place in Dublin, Ireland, 2016. Underwater noise from pile driving, seismic surveying, shipping, but also non-anthropogenic sources such as wind was examined. The potential effects on animals ranging from plankton, shrimps and crabs, to lobsters, fishes, seals, dolphins, and whales were discussed. Reported effects include behavioral responses, auditory masking, cardiac rate changes, stress, a temporary loss of hearing, and perhaps more serious tissue and organ damage. Short-term and long-term, individual and population-level effects were portrayed. Several studies also looked at the fundamentals of animal sound production and perception. One session dealt with the regulation and management of underwater noise. The social program was intended to encourage more leisurely discussions amongst conference participants in order to facilitate networking and the strengthening of relationships. The feedback from conference delegates (submitted via an online survey after the meeting) was very positive.

Evidence suggests that the capacity for sound source localization is common to mammals, birds, reptiles, and amphibians, but surprisingly it is not known whether fish locate sound sources in the same manner (e.g., combining binaural and monaural cues) or what computational strategies they use for successful source localization. Directional hearing and sound source localization in fishes continues to be important topics in neuroethology and in the hearing sciences, but the empirical and theoretical work on these topics have been contradictory and obscure for decades. This chapter reviews the previous behavioral work on directional hearing and sound source localization in fishes including the most recent experiments on sound source localization by the plainfin midshipman fish (Porichthys notatus), which has proven to be an exceptional species for fish studies of sound localization. In addition, the theoretical models of directional hearing and sound source localization for fishes are reviewed including a new model that uses a time-averaged intensity approach for source localization that has wide applicability with regard to source type, acoustic environment, and time waveform.

On May 25, 2013, a special symposium was held at the Mote Marine Laboratory in Sarasota, FL to honor the outstanding careers of Drs. Richard R. Fay and Arthur N. Popper, a “dynamic duo” of scientists who were pioneers in the field of contemporary fish hearing and bioacoustics. The present article details the research, academic life, and “other side” of Richard Rozzell Fay, a most interesting man of science who is known to all as a kind, gentle, wise, and introspective scientist.

The plainfin midshipman fish (Porichthys notatus) is a well-studied model to understand the neural and endocrine mechanisms underlying vocal-acoustic communication across vertebrates. It is well established that steroid hormones such as estrogen drive seasonal peripheral auditory plasticity in female Porichthys in order to better encode the male’s advertisement call. However, little is known of the neural substrates that underlie the motivation and coordinated behavioral response to auditory social signals. Catecholamines, which include dopamine and noradrenaline, are good candidates for this function, as they are thought to modulate the salience of and reinforce appropriate behavior to socially relevant stimuli. This chapter summarizes our recent studies which aimed to characterize catecholamine innervation in the central and peripheral auditory system of Porichthys as well as test the hypotheses that innervation of the auditory system is seasonally plastic and catecholaminergic neurons are activated in response to conspecific vocalizations. Of particular significance is the discovery of direct dopaminergic innervation of the saccule, the main hearing end organ, by neurons in the diencephalon, which also robustly innervate the cholinergic auditory efferent nucleus in the hindbrain. Seasonal changes in dopamine innervation in both these areas appear dependent on reproductive state in females and may ultimately function to modulate the sensitivity of the peripheral auditory system as an adaptation to the seasonally changing soundscape. Diencephalic dopaminergic neurons are indeed active in response to exposure to midshipman vocalizations and are in a perfect position to integrate the detection and appropriate motor response to conspecific acoustic signals for successful reproduction.