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Understanding the contribution of neuropeptide-containing neurons to variation in social behavior remains critically important. Galanin has gained increased attention because of the demonstration that galanin neurons in the preoptic area (POA) promote mating and parental care in mammals. How widespread these mechanisms are among vertebrates essentially remains unexplored, especially among teleost fishes, which comprise nearly one-half of living vertebrate species. Teleosts with alternative reproductive tactics exhibit stereotyped patterns of social behavior that diverge widely between individuals within a sex. This includes midshipman that have two male morphs. Type I males mate using either acoustic courtship to attract females to enter a nest they guard or cuckoldry during which they steal fertilizations from a nest-holding male using a sneak or satellite spawning tactic, whereas type II males only cuckold. Using the neural activity marker phospho-S6, we show increased galanin neuron activation in courting type I males during mating that is not explained by their courtship vocalizations, parental care of eggs, or nest defense against cuckolders. This increase is not observed during mating in cuckolders of either morph or females (none of which show parental care). Together with their role in mating in male mammals, the results demonstrate an unexpectedly specific and deep-rooted, phylogenetically shared behavioral function for POA galanin neurons. The results also point to galanin-dependent circuitry as a potential substrate for the evolution of divergent phenotypes within one sex and provide new functional insights into how POA populations in teleosts compare to the POA and anterior hypothalamus of tetrapods. SIGNIFICANCE STATEMENT Studies of neuropeptide regulation of vertebrate social behavior have mainly focused on the vasopressin-oxytocin family. Recently, galanin has received attention as a regulator of social behavior largely because of studies demonstrating that galanin neurons in the preoptic area (POA) promote mating and parental care in mammals. Species with alternative reproductive tactics (ARTs) exhibit robust, consistent differences in behavioral phenotypes between individuals within a sex. Taking advantage of this trait, we show POA galanin neurons are specifically active during mating in one of two male reproductive tactics, but not other mating-related behaviors in a fish with ARTs. The results demonstrate a deep, phylogenetically shared role for POA galanin neurons in reproductive-related social behaviors with implications for the evolution of ARTs., (Copyright © 2020 the authors.)

Vocalization is a behavioral feature that is shared among multiple vertebrate lineages, including fish. The temporal patterning of vocal communication signals is set, in part, by central pattern generators (CPGs). Toadfishes are well-established models for CPG coding of vocalization at the hindbrain level. The vocal CPG comprises three topographically separate nuclei: pre-pacemaker, pacemaker, motor. While the connectivity between these nuclei is well understood, their neurochemical profile remains largely unexplored. The highly vocal Gulf toadfish, Opsanus beta, has been the subject of previous behavioral, neuroanatomical and neurophysiological studies. Combining transneuronal neurobiotin-labeling with immunohistochemistry, we map the distribution of inhibitory neurotransmitters and neuromodulators along with gap junctions in the vocal CPG of this species. Dense GABAergic and glycinergic label is found throughout the CPG, with labeled somata immediately adjacent to or within CPG nuclei, including a distinct subset of pacemaker neurons co-labeled with neurobiotin and glycine. Neurobiotin-labeled motor and pacemaker neurons are densely co-labeled with the gap junction protein connexin 35/36, supporting the hypothesis that transneuronal neurobiotin-labeling occurs, at least in part, via gap junction coupling. Serotonergic and catecholaminergic label is also robust within the entire vocal CPG, with additional cholinergic label in pacemaker and prepacemaker nuclei. Likely sources of these putative modulatory inputs are neurons within or immediately adjacent to vocal CPG neurons. Together with prior neurophysiological investigations, the results reveal potential mechanisms for generating multiple classes of social context-dependent vocalizations with widely divergent temporal and spectral properties., (© 2018 The Authors The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.)

Temporal patterning is an essential feature of neural networks producing precisely timed behaviours such as vocalizations that are widely used in vertebrate social communication. Here we show that intrinsic and network properties of separate hindbrain neuronal populations encode the natural call attributes of frequency and duration in vocal fish. Intracellular structure/function analyses indicate that call duration is encoded by a sustained membrane depolarization in vocal prepacemaker neurons that innervate downstream pacemaker neurons. Pacemaker neurons, in turn, encode call frequency by rhythmic, ultrafast oscillations in their membrane potential. Pharmacological manipulations show prepacemaker activity to be independent of pacemaker function, thus accounting for natural variation in duration which is the predominant feature distinguishing call types. Prepacemaker neurons also innervate key hindbrain auditory nuclei thereby effectively serving as a call-duration corollary discharge. We propose that premotor compartmentalization of neurons coding distinct acoustic attributes is a fundamental trait of hindbrain vocal pattern generators among vertebrates.

The neuropeptide arginine vasotocin (AVT) is well known to modulate both aggression and affiliation, yet few studies relate individual behavioral state to a quantitative assessment of AVT distribution in the brain. Here, using a wild population of beaugregory damselfish, Stegastes leucostictus, we assess: (1) the effect of AVT on courtship, and (2) with reference to our previous study on AVT modulation of aggression in this species, the relationship between AVT-like immunoreactive (ir) fiber distribution in the forebrain's preoptic area and individual courtship and aggression levels. Exogenous AVT did not affect courtship, yet Manning compound, an arginine vasopressin (AVP) V1a receptor antagonist, significantly lowered but did not eradicate courtship. Consistent with AVT's known facilitation of aggression in this species, the density of AVT-ir fibers in the preoptic area was significantly negatively correlated to aggression. Our findings match similar behavioral and immunoreactive patterns of neuropeptide secretion in other taxa. Unlike aggression, preoptic AVT-ir fiber density was not significantly correlated to individual courtship levels. The results suggest a differential involvement of preoptic AVT neurons and/or their receptors in supporting the expression of aggression and courtship., (Copyright 2010 S. Karger AG, Basel.)

The macroevolutionary events leading to neural innovations for social communication, such as vocalization, are essentially unexplored. Many fish vocalize during female courtship and territorial defense, as do amphibians, birds, and mammals. Here, we map the neural circuitry for vocalization in larval fish and show that the vocal network develops in a segment-like region across the most caudal hindbrain and rostral spinal cord. Taxonomic analysis demonstrates a highly conserved pattern between fish and all major lineages of vocal tetrapods. We propose that the vocal basis for acoustic communication among vertebrates evolved from an ancestrally shared developmental compartment already present in the early fishes.

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.

Vocal behavior is multifaceted and requires that vocal-motor patterning be integrated at multiple brain levels with auditory, neuroendocrine, and other social behavior processes (e.g., courtship and aggression). We now provide anatomical evidence for an extensive vocal network in teleost fishes (Batrachoididae: Porichthys notatus; Opsanus beta) that is strongly integrated with neuroendocrine and auditory pathways and that exhibits striking similarities to the vocal-acoustic circuitry known for mammals. Biotin compound injections into neurophysiologically identified vocal regions of the forebrain (preoptic area and anterior hypothalamus) and of the midbrain (periaqueductal gray and paralemniscal tegmentum) reveal extensive connectivity within and between these regions, as well as reciprocal relationships with the auditory thalamus and/or auditory midbrain (torus semicircularis). Thus, specific components of the basal forebrain and midbrain are here designated as the forebrain vocal-acoustic complex (fVAC) and midbrain vocal-acoustic complex (mVAC), respectively. Biotin injections into the mVAC and a previously identified hindbrain vocal pattern generator likewise provide anatomical evidence for a distributed network of descending projections to the vocal pacemaker-motoneuron circuitry. Together, the present experiments establish a vocal-auditory-neuroendocrine network in teleost fish that links the forebrain and midbrain to the hindbrain vocal pattern generator (i.e., fVAC --> mVAC --> pattern generator) and provides an anatomical framework for the previously identified neuropeptide modulation of vocal activity elicited from the forebrain and midbrain, which contributes to the expression of sex- and male morph-specific behavior. We conclude with a broad comparison of these findings with those for other vertebrate taxa and suggest that the present findings provide novel insights into the structure of conserved behavioral regulatory circuits that have led to evolutionary convergence in vocal-acoustic systems., (Copyright 2002 Wiley-Liss, Inc.)

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. [ABSTRACT FROM AUTHOR]

This review will focus on recent developments in the sensorimotor integration of vocal communication. Two broad themes are emphasized: the evolution of vocal production and perception, and the role of social context. Advances include: a proposal for the emergence of vocal patterning during vertebrate evolution, the role of sensory mechanisms such as categorical perception in decoding communication signals, contributions of sensorimotor integration phenomena including mirror neurons and vocal learning, and mechanisms of hormone-dependent plasticity in both auditory and vocal systems. Transcriptional networks activated in humans but not in chimps by the FoxP2 gene suggest molecular mechanisms underlying vocal gestures and the emergence of human language. [ABSTRACT FROM AUTHOR]

Divergent steroid hormone profiles can shape the development of male versus female neural phenotypes, but whether they also determine differences in the short-term, neurophysiological patterning of behavior is unknown. We now show that steroid hormone-specific modulation of a vocal pattern generator (VPG) diverges between reproductive morphs in a teleost fish. Only type I male midshipman acoustically court females, whereas type II males steal fertilizations from type I males and, like females, generate only agonistic calls. The androgen 11-ketotestosterone (11kT), but not testosterone (T), rapidly (within 5 min) increases type I VPG output. As now shown, T, but not 11kT, rapidly increases VPG output in type II males and females, consistent with the predominant circulating androgen in type II males and females (T) versus type Is (11kT). Receptor and enzyme antagonists reveal an unexpected divergence in androgen- versus estrogen-dependent mechanisms in, respectively, type II males versus females. Cortisol, the main circulating glucocorticoid, also has divergent actions: suppressing versus increasing VPGoutput in, respectively, type II males and females versus type Is. In summary, rapid steroid action on VPG activity is uncoupled from gonadal phenotype (convergent between type II males and females), whereas the receptor-mediated mechanisms of androgen action are predicted by gonadal phenotype (both male morphs are sensitive to androgen receptor blockade, whereas females are not). A comparable mix of neuroendocrine traits may explain the widespread distribution of intrasexual behavioral phenotypes among teleosts and vertebrates in general. Moreover, the fundamental organization/activation principles that predict the steroid-dependent expression of "maleness" and "femaleness" may now include rapid steroid actions on the neurophysiological patterning of behavior. [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]