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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., (Copyright © 2014 Elsevier Inc. All rights reserved.)

Corollary discharge is essential to an animal's ability to filter self-generated from external stimuli. This includes acoustic communication, although direct demonstration of a corollary discharge that both conveys a vocal motor signal and informs the auditory system about the physical attributes of a self-generated vocalization has remained elusive for vertebrates. Here, we show the underlying synaptic activity of a neuronal vocal corollary discharge pathway in the hindbrain of a highly vocal species of fish. Neurons carrying the vocal corollary discharge are specifically adapted for the transmission of duration information, a predominant acoustic cue. The results reveal that vertebrates, like some insects, have a robust corollary discharge conveying call duration. Along with evidence for the influence of vocal duration on auditory encoding in mammals, these new findings suggest that linking vocal motor and corollary discharge pathways with pattern generating, call duration neurons is a shared network character across the animal kingdom.

Sensory plasticity related to reproductive state, hormonal profiles, and experience is widespread among vertebrates, including humans. Improvements in audio-vocal coupling that heighten the detection of conspecifics are part of the reproductive strategy of many nonmammalian vertebrates. Although seasonal changes in hearing are known, molecular mechanisms determining this form of adult sensory plasticity remain elusive. Among both nonmammals and mammals, large-conductance, calcium-activated potassium (BK) channels underlie a primary outward current having a predominant influence on frequency tuning in auditory hair cells. We now report an example from fish showing that increased BK channel abundance can improve an individual's ability to hear vocalizations during the breeding season. Pharmacological manipulations targeting BK channels, together with measures of BK transcript abundance, can explain the seasonal enhancement of auditory hair cell sensitivity to the frequency content of calls. Plasticity in ion channel expression is a simple, evolutionarily labile solution for sculpting sensory bandwidth to maximize the detection of conspecific signals during reproductive cycles., (Copyright © 2013 Elsevier Ltd. All rights reserved.)

For seasonally breeding vertebrates, reproductive cycling is often coupled with changes in vocalizations that function in courtship and territoriality. Less is known about changes in auditory sensitivity to those vocalizations. Here, we show that nonreproductive female midshipman fish treated with either testosterone or 17beta-estradiol exhibit an increase in the degree of temporal encoding of the frequency content of male vocalizations by the inner ear that mimics the reproductive female's auditory phenotype. This sensory plasticity provides an adaptable mechanism that enhances coupling between sender and receiver in vocal communication.

Female midshipman fish (Porichthys notatus) use the auditory sense to detect and locate vocalizing males during the breeding season. Detection of conspecific vocal signals is essential to their reproductive success and can evoke strong phonotactic responses in gravid females but not in spent females that have released all of their eggs. Here, we test the hypothesis that seasonal variation in reproductive state affects the neurophysiological response properties of the peripheral auditory system in female midshipman fish. Iso-intensity responses of eighth nerve afferents from the sacculus, the main auditory end organ of the inner ear, to individual tones were measured for spike rate and vector strength (VS) of synchronization. Most auditory saccular units in reproductive, summer females showed robust temporal encoding up to 340 Hz, whereas nonreproductive winter females showed comparable encoding only up to 100 Hz. The dramatic upward shift in temporal encoding among summer fish was paralleled by increases in best frequency (BF), maximum evoked spike rate at BF, VS values at BF, and the percentage of units that showed significant VS to iso-intensity tones >140 Hz. Reproductive summer females were best suited to encode the higher harmonic components of male advertisement calls. This first demonstration of a natural cyclicity in peripheral auditory frequency sensitivity among vertebrates may represent, in this case, an adaptive plasticity of the female midshipman's auditory system to enhance the acquisition of auditory information needed for mate identification and localization during the breeding season.

Sound communication is not unique to humans but rather is a trait shared with most non-mammalian vertebrates. A practical way to address questions of vocal signal encoding has been to identify mechanisms in non-mammalian model systems that use acoustic communication signals in their social behavior. Teleost fishes, the largest group of living vertebrates, include both vocal and non-vocal species that exploit a wide range of acoustic niches. Here, we focus on those vocal species where combined behavioral and neurobiological studies have recently begun to elucidate a suite of adaptations for both the production and the perception of acoustic signals essential to their reproductive success and survival. Studies of these model systems show that teleost fish have the vocal-acoustic behaviors and neural systems both necessary and sufficient to solve acoustic problems common to all vertebrates. In particular, behavioral studies demonstrate that temporal features within a call, including pulse duration, rate and number, can all be important to a call's communicative value. Neurobiological studies have begun to show how these features are produced by a vocal motor system extending from forebrain to hindbrain levels and are encoded by peripheral and central auditory neurons. The abundance and variety of vocal fish present unique opportunities for parallel investigations of neural encoding, perception, and communication across a diversity of natural, acoustic habitats. As such, investigations in teleosts contribute to our delineating the evolution of the vocal and auditory systems of both non-mammalian and mammalian species, including humans.

Melatonin plays a central role in entraining activity to the day–night cycle in vertebrates. Here, we investigate neuroanatomical substrates of melatonin‐dependent vocal–acoustic behavior in the nocturnal and highly vocal teleost fish, the plainfin midshipman (Porichthys notatus). Using in situ hybridization (ISH) and quantitative real‐time PCR (qPCR), we assess the mRNA distribution and transcript abundance of melatonin receptor subtype 1B (mel1b), shown to be important for vocalization in midshipman fish and songbirds. ISH shows robust mel1b expression in major nodes of the central vocal and auditory networks in the subpallium, preoptic area (POA), anterior hypothalamus, dorsal thalamus, posterior tuberculum, midbrain torus semicircularis and periaqueductal gray, and hindbrain. Mel1b label is also abundant in secondary targets of the olfactory, visual, and lateral line systems, as well as telencephalic regions that have been compared to the amygdala, extended amygdala, striatum, septum, and hippocampus of tetrapods. Q‐PCR corroborates mel1b abundance throughout the brain and shows significant increases in the morning compared with nighttime in tissue samples inclusive of the telencephalon and POA, but remains stable in other brain regions. Plasma melatonin levels show expected increase at night. Our findings support the hypothesis that melatonin's stimulatory effects on vocal–acoustic mechanisms in midshipman is mediated, in part, by melatonin binding in vocal, auditory, and neuroendocrine centers. Together with robust mel1b expression in multiple telencephalic nuclei and sensory systems, the results further indicate an expression pattern comparable to that in birds and mammals that is indicative of melatonin's broad involvement in the modulation of physiology and behavior. We investigated the mRNA distribution and transcript abundance of melatonin receptor subtype 1B, known to be important for vocalization in fish and songbirds. Robust expression occurs in major nodes of the vocal–acoustic network, and other sensory sites and multiple telencephalic regions, indicative of melatonin's broad involvement in modulating physiology and behavior. [ABSTRACT FROM AUTHOR]

Background: Successful animal communication depends on a receiver's ability to detect a sender's signal. Exemplars of adaptive sender-receiver coupling include acoustic communication, often important in the context of seasonal reproduction. During the reproductive summer season, both male and female midshipman fish (Porichthys notatus) exhibit similar increases in the steroid-dependent frequency sensitivity of the saccule, the main auditory division of the inner ear. This form of auditory plasticity enhances detection of the higher frequency components of the multi-harmonic, long-duration advertisement calls produced repetitively by males during summer nights of peak vocal and spawning activity. The molecular basis of this seasonal auditory plasticity has not been fully resolved. Here, we utilize an unbiased transcriptomic RNA sequencing approach to identify differentially expressed transcripts within the saccule's hair cell epithelium of reproductive summer and non-reproductive winter fish. Results: We assembled 74,027 unique transcripts from our saccular epithelial sequence reads. Of these, 6.4 % and 3.0 % were upregulated in the reproductive and non-reproductive saccular epithelium, respectively. Gene ontology (GO) term enrichment analyses of the differentially expressed transcripts showed that the reproductive saccular epithelium was transcriptionally, translationally, and metabolically more active than the non-reproductive epithelium. Furthermore, the expression of a specific suite of candidate genes, including ion channels and components of steroid-signaling pathways, was upregulated in the reproductive compared to the non-reproductive saccular epithelium. We found reported auditory functions for 14 candidate genes upregulated in the reproductive midshipman saccular epithelium, 8 of which are enriched in mouse hair cells, validating their hair cell-specific functions across vertebrates. Conclusions: We identified a suite of differentially expressed genes belonging to neurotransmission and steroid-signaling pathways, consistent with previous work showing the importance of these characters in regulating hair cell auditory sensitivity in midshipman fish and, more broadly, vertebrates. The results were also consistent with auditory hair cells being generally more physiologically active when animals are in a reproductive state, a time of enhanced sensory-motor coupling between the auditory periphery and the upper harmonics of vocalizations. Together with several new candidate genes, our results identify discrete patterns of gene expression linked to frequency- and steroid-dependent plasticity of hair cell auditory sensitivity. [ABSTRACT FROM AUTHOR]

Non-mammalian vertebrates rely on electrical resonance for frequency tuning in auditory hair cells. A key component of the resonance exhibited by these cells is an outward calcium-activated potassium current that flows through large-conductance calcium-activated potassium (BK) channels. Previous work in midshipman fish (Porichthys notatus) has shown that BK expression correlates with seasonal changes in hearing sensitivity and that pharmacologically blocking these channels replicates the natural decreases in sensitivity during the winter non-reproductive season. To test the hypothesis that reducing BK channel function is sufficient to change auditory thresholds in fish, morpholino oligonucleotides (MOs) were used in larval zebrafish (Danio rerio) to alter expression of slola and slolb, duplicate genes coding for the pore-forming a-subunits of BK channels. Following MO injection, microphonic potentials were recorded from the inner ear of larvae. Quantitative real-time PCR was then used to determine the MO effect on slola and slolb expression in these same fish. Knockdown of either slola or slolb resulted in disrupted gene expression and increased auditory thresholds across the same range of frequencies of natural auditory plasticity observed in midshipman. We conclude that interference with the normal expression of individual slol genes is sufficient to increase auditory thresholds in zebrafish larvae and that changes in BK channel expression are a direct mechanism for regulation of peripheral hearing sensitivity among fishes. [ABSTRACT FROM AUTHOR]

Toadfishes are among the best-known groups of sound-producing (vocal) fishes and include species commonly known as toadfish and midshipman. Although midshipman have been the subject of extensive investigation of the neural mechanisms of vocalization, this is the first comprehensive, quantitative analysis of the spectrotemporal characters of their acoustic signals and one of the few for fishes in general. Field recordings of territorial, nest-guarding male midshipman during the breeding season identified a diverse vocal repertoire composed of three basic sound types that varied widely in duration, harmonic structure and degree of amplitude modulation (AM): 'hum', 'grunt' and 'growl'. Hum duration varied nearly 1000-fold, lasting for minutes at a time, with stable harmonic stacks and little envelope modulation throughout the sound. By contrast, grunts were brief, ~30-140 ms, broadband signals produced both in isolation and repetitively as a train of up to 200 at intervals of ~0.5-1.0s. Growls were also produced alone or repetitively, but at variable intervals of the order of seconds with durations between those of grunts and hums, ranging 60-fold from ~200 ms to 12 s. Growls exhibited prominent harmonics with sudden shifts in pulse repetition rate and highly variable AM patterns, unlike the nearly constant AM of grunt trains and flat envelope of hums. Behavioral and neurophysiological studies support the hypothesis that each sound type's unique acoustic signature contributes to signal recognition mechanisms. Nocturnal production of these sounds against a background chorus dominated constantly for hours by a single sound type, the multiharmonic hum, reveals a novel underwater soundscape for fish. [ABSTRACT FROM AUTHOR]

Vertebrates displaying seasonal shifts in reproductive behavior provide the opportunity to investigate bidirectional plasticity in sensory function. The midshipman teleost fish exhibits steroid-dependent plasticity in frequency encoding by eighth nerve auditory afferents. In this study, evoked potentials were recorded in vivo from the saccule, the main auditory division of the inner ear of most teleosts, to test the hypothesis that males and females exhibit seasonal changes in hair cell physiology in relation to seasonal changes In plasma levels of steroids. Thresholds across the predominant frequency range of natural vocalizations were significantly less in both sexes in reproductive compared with non-reproductive conditions, with differences greatest at frequencies corresponding to call upper harmonics. A subset of non-reproductive males exhibiting ar intermediate saccular phenotype had elevated testosterone levels, supporting the hypothesis that rising steroid levels induce non-reproductive to reproductive transitions in saccular physiology. We propose that elevated levels of steroids act via Ion j-term (days to weeks) signaling pathways to upregulate ion channel expression generating higher resonant frequencies characteristic of non- mammalian auditory hair cells, thereby lowering acoustic thresholds. [ABSTRACT FROM AUTHOR]

The auditory system of adult midshipman fish Porichthys notatus Girard is an important sensory receiver system used during intraspecific social communication to encode conspecific vocalizations, but the response properties and function of this system in the pre-adult stages are unknown. Midshipman fish, like other teleosts, use the saccule as the main acoustic end organ of the inner ear. In this study, we examined the discharge properties and the frequency response dynamics of auditory saccular afferent neurons in p re-adult midshipman (-4-12 months of age) to determine whether encoding of auditory information, inclusive of conspecific vocalizations, changes across life history stages. Extracellular single unit recordings were made from saccular afferents while sound was presented via an underwater speaker. Comparisons with adult data show that the resting discharge rate and auditory threshold sensitivity increased with age/size, while temporal encoding of frequency did not show any significant shifts. The results indicate that the saccular afferents of juveniles, like those of non-reproductive adults, are best adapted to temporally encode the low frequency components (⩽100 Hz) of midshipman vocalizations. This report represents the first in vivo investigation of age-related changes in the encoding properties of individual auditory neurons for any fish species. [ABSTRACT FROM AUTHOR]

All sonic vertebrates face the problem of sound production interfering with their ability to detect and process external acoustic signals, including conspecific vocalizations. Direct efferent inputs to the inner ear of all vertebrates, and the lateral line system of some aquatic vertebrates, represent a potential mechanism to adjust peripheral sensitivity during sound production. We recorded from single efferent neurons that innervate the inner ear and lateral line in a sound-producing teleost fish while evoking fictive vocalizations predictive of the temporal features of natural vocalizations. The majority of efferent neurons showed an increase in activity that occurred in-phase with modulations in the fine temporal structure of the fictive vocalizations. Many of these neurons also showed a decrease in activity at fictive vocal offset. Efferents to the sacculus, the main auditory end organ, showed features especially well adapted for maintaining sensitivity to external acoustic signals during sound production. These included robust phase locking of efferent activity to each cycle of a fictive vocalization and a long-duration rebound suppression after each fictive vocalization that could provide a rapid, long-lasting period of sensitization to external acoustic stimuli such as the call of a conspecific. These results suggest that efferent activation by the vocal motor system can directly modulate auditory sensitivity to self-generated sounds and maintain sensitivity to ongoing external sounds. Given the conserved organization of the auditory efferent system across vertebrates, such mechanisms may be operative among all sonic vertebrates. [ABSTRACT FROM AUTHOR]

Unique patterns of spike activity across neuron populations have been implicated in the coding of complex sensory stimuli. Delineating the patterns of neural activity in response to varying stimulus parameters and their relationships to the tuning characteristics of individual neurons is essential to ascertaining the nature of population coding within the brain. Here, we address these points in the midbrain coding of concurrent vocal signals of a sound-producing fish, the plainfin midshipman. Midshipman produce multiharmonic vocalizations which frequently overlap to produce beats. We used multivariate statistical analysis from single-unit recordings across multiple animals to assess the presence of a temporal population code. Our results show that distinct patterns of temporal activity emerge among midbrain neurons in response to concurrent signals that vary in their difference frequency. These patterns can serve to code beat difference frequencies. The patterns directly result from the differential temporal coding of difference frequency by individual neurons. Difference frequency encoding, based on temporal patterns of activity, could permit the segregation of concurrent vocal signals on time scales shorter than codes requiring averaging. Given the ubiquity across vertebrates of auditory midbrain tuning to the temporal structure of acoustic signals, a similar temporal population code is likely present in other species. [ABSTRACT FROM AUTHOR]

The organization of the descending and secondary octaval nuclei in the hindbrain of the Gulf toadfish, Opsanus beta, was revealed following the injection of biotin compounds into a physiologically identified auditory region of the torus semicircularis. The results show retrogradely-filled neurons mainly in a dorsomedial division of the descending octaval nucleus, and dorsal and ventral divisions of a secondary octaval nucleus; minor labeling also appeared in dorsolateral and rostromedial intermediate divisions of the descending nucleus. The pattern identified is consistent with that reported in other teleosts, including both vocal and non-vocal species, and clarifies earlier reports of the organization of hindbrain octaval nuclei in toadfish and the closely related midshipman fish.Copyright © 2001 S. Karger AG, Basel [ABSTRACT FROM AUTHOR]

Abstract: This review highlights recent studies of the anatomical and functional implications of brain aromatase (estrogen synthase) expression in two vertebrate lineages, teleost fishes and songbirds, that show remarkably high levels of adult brain aromatase activity, protein and gene expression compared to other vertebrate groups. Teleosts and birds have proven to be important neuroethological models for investigating how local estrogen synthesis leads to changes in neural phenotypes that translate into behavior. Region-specific patterns of aromatase expression, and thus estrogen synthesis, include the vocal and auditory circuits that figure prominently into the life history adaptations of vocalizing teleosts and songbirds. Thus, by targeting, for example, vocal motor circuits without inappropriate steroid exposure to other steroid-dependent circuits, such as those involved in either copulatory or spawning behaviors, the neuroendocrine system can achieve temporal and spatial specificity in its modulation of neural circuits that lead to the performance of any one behavior. [Copyright &y& Elsevier]