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.
•Adult zebrafish strains have differing auditory sensitivity.•Sensitivity differences also correlate with fluorescent protein expression.•Larval Brn3c:mGFP fish have reduced auditory-evoked behavior and a potential defect in hair cell transduction.•Hair cell density does not differ between strains.•Caution is warranted when selecting a zebrafish line for auditory research.
The vocal plainfin midshipman fish (
Porichthys notatus) has become an excellent model for identifying neural mechanisms of auditory perception that may be shared by all vertebrates. Recent ...neuroethological studies of the midshipman fish have yielded strong evidence for the steroid-dependent modulation of hearing sensitivity that leads to enhanced coupling of sender and receiver in this vocal-acoustic communication system. Previous work shows that non-reproductive females treated with either testosterone or 17β-estradiol exhibit an increase in the degree of temporal encoding by the auditory saccular afferents to the dominant frequency content of male vocalizations produced during social-reproductive behaviors. The expanded frequency sensitivity of steroid treated females mimics the reproductive female’s auditory phenotype and is proposed to improve the detection and localization of calling conspecific mates during the summer breeding season. This review focuses on the novel form of steroid-dependent auditory plasticity that is found in the adult midshipman fish and its association with the reproductive biology and behavior of this species. Evidence for midshipman reproductive-state and steroid-dependent auditory plasticity is reviewed and the potential mechanisms that lead to this novel form of adaptive plasticity are discussed.
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.
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.
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.
The plainfin midshipman fish, Porichthys notatus, is a vocal species of teleost fish that generates acoustic signals for intraspecific communication during social and reproductive behaviors. All ...adult morphs (females and males) produce single short duration grunts important for agonistic encounters, but only nesting males produce trains of grunts and growls in agonistic contexts and long duration multiharmonic advertisement calls to attract gravid females for spawning. The midshipman fish uses the saccule as the main acoustic endorgan for hearing to detect and locate vocalizing conspecifics. Here, I examined the response properties of evoked potentials from the midshipman saccule to determine the frequency response and auditory threshold sensitivity of saccular hair cells to behaviorally-relevant single tone stimuli. Saccular potentials were recorded from the rostral, medial and caudal regions of the saccule while sound was presented by an underwater speaker. Saccular potentials of the midshipman, like other teleosts, were evoked greatest at a frequency that was twice the stimulus frequency. Results indicate that midshipman saccular hair cells of non-reproductive adults had a peak frequency sensitivity that ranged from 75 (lowest frequency tested) to 145 Hz and were best suited to detect the low frequency components (<=105 Hz) of midshipman vocalizations.
The plainfin midshipman fish (Porichthys notatus Girard, 1854) is a vocal species of batrachoidid fish that generates acoustic signals for intraspecific communication during social and reproductive ...activity and has become a good model for investigating the neural and endocrine mechanisms of vocal‐acoustic communication. Reproductively active female plainfin midshipman fish use their auditory sense to detect and locate “singing” males, which produce a multiharmonic advertisement call to attract females for spawning. The seasonal onset of male advertisement calling in the midshipman fish coincides with an increase in the range of frequency sensitivity of the female's inner ear saccule, the main organ of hearing, thus leading to enhanced encoding of the dominant frequency components of male advertisement calls. Non‐reproductive females treated with either testosterone or 17β‐estradiol exhibit a dramatic increase in the inner ear's frequency sensitivity that mimics the reproductive female's auditory phenotype and leads to an increased detection of the male's advertisement call. This novel form of auditory plasticity provides an adaptable mechanism that enhances coupling between sender and receiver in vocal communication. This review focuses on recent evidence for seasonal reproductive‐state and steroid‐dependent plasticity of auditory frequency sensitivity in the peripheral auditory system of the midshipman fish. The potential steroid‐dependent mechanism(s) that lead to this novel form of auditory and behavioral plasticity are also discussed.
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.
Vocal differentiation is widely documented in birds and mammals but has been poorly investigated in other vertebrates, including fish, which represent the oldest extant vertebrate group. Neural ...circuitry controlling vocal behaviour is thought to have evolved from conserved brain areas that originated in fish, making this taxon key to understanding the evolution and development of the vertebrate vocal-auditory systems. This study examines ontogenetic changes in the vocal repertoire and whether vocal differentiation parallels auditory development in the Lusitanian toadfish Halobatrachus didactylus (Batrachoididae). This species exhibits a complex acoustic repertoire and is vocally active during early development. Vocalisations were recorded during social interactions for four size groups (fry: <2 cm; small juveniles: 2-4 cm; large juveniles: 5-7 cm; adults >25 cm, standard length). Auditory sensitivity of juveniles and adults was determined based on evoked potentials recorded from the inner ear saccule in response to pure tones of 75-945 Hz. We show an ontogenetic increment in the vocal repertoire from simple broadband-pulsed 'grunts' that later differentiate into four distinct vocalisations, including low-frequency amplitude-modulated 'boatwhistles'. Whereas fry emitted mostly single grunts, large juveniles exhibited vocalisations similar to the adult vocal repertoire. Saccular sensitivity revealed a three-fold enhancement at most frequencies tested from small to large juveniles; however, large juveniles were similar in sensitivity to adults. We provide the first clear evidence of ontogenetic vocal differentiation in fish, as previously described for higher vertebrates. Our results suggest a parallel development between the vocal motor pathway and the peripheral auditory system for acoustic social communication in fish.
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.
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