Andrew H Bass

Cornell University | CU · Department of Neurobiology and Behavior

The relationship between sound complexity and the underlying morphology and physiology of the vocal organ anatomy is a fundamental component in the evolution of acoustic communication, particularly for fishes. Among vertebrates, the mammalian larynx and avian syrinx are the best-studied vocal organs, and their ability to produce complex vocalizatio...

Although optical microscopy has allowed scientists to study the entire brain in early developmental stages, access to the brains of live, adult vertebrates has been limited. Danionella, a genus of miniature, transparent fish closely related to zebrafish has been introduced as a neuroscience model to study the adult vertebrate brain. However, the ex...

Acoustic behavior is widespread across vertebrates, including among fishes. We report robust acoustic displays during aggressive interactions for a laboratory colony of Danionella dracula, a miniature and transparent species of teleost fish closely related to zebrafish (Danio rerio), which are hypothesized to be sonic based on the presence of a hyp...

Sound production by fishes has been recognized for millennia, but is typically regarded as comparatively rare and thus yet to be integrated into broader concepts of vertebrate evolution. We map the most comprehensive dataset of sound production yet assembled onto a family-level phylogeny of ray-finned fishes (Actinopterygii), a clade containing mor...

Although optical microscopy has allowed us to study the entire brain in early developmental stages, access to the brains of live, adult vertebrates has been limited. Danionella, a genus of miniature, transparent fish closely related to zebrafish has been introduced as a neuroscience model to study the entire adult vertebrate brain. However, the ext...

Individuals can reveal their relative competitive ability or mate quality through acoustic communication, varying signals in form and frequency to mediate adaptive interactions including competitive aggression. We report robust acoustic displays during aggressive interactions for a laboratory colony of Danionella dracula, a recently discovered mini...

Neuropeptides, including oxytocin-like peptides, are a conserved group of hormones that regulate a wide range of social behaviors, including vocal communication. In the current study, we evaluate whether putative brain sites for the actions of isotocin (IT), the oxytocin (OT) homolog of teleost fishes, are associated with vocal courtship and circui...

The communication behaviors of vocal fish and electric fish are among the vertebrate social behaviors best understood at the level of neural circuits. Both forms of signaling rely on midbrain inputs to hindbrain pattern generators that activate peripheral effectors (sonic muscles and electrocytes) to produce pulsatile signals that are modulated by...

For many animal species, vocal communication is a critical social behavior and often a necessary component of reproductive success. Additionally, vocalizations are often demanding motor acts. Wanting to know whether a specific molecular toolkit might be required for vocalization, we used RNA-sequencing to investigate neural gene expression underlyi...

Precise neuronal firing is especially important for behaviors highly dependent on the correct sequencing and timing of muscle activity patterns, such as acoustic signaling. Acoustic signaling is an important communication modality for vertebrates, including many teleost fishes. Toadfishes are well known to exhibit high temporal fidelity in synchron...

Mochokid catfish offer a distinct opportunity to study a communication system transitioning to a new signaling channel because some produce sounds and others electric discharges. Both signals are generated using an elastic spring system (ESS), which includes a protractor muscle innervated by motoneurons within the protractor nucleus that also has a...

For many animal species, vocal communication is a critical social behavior, often a necessary component of reproductive success. In addition to the role of vocal behavior in social interactions, vocalizations are often demanding motor acts. Through understanding the genes involved in regulating and permitting vertebrate vocalization, we can better...

Acoustic signaling by fishes has been recognized for millennia, but is typically regarded as comparatively rare within ray-finned fishes; as such, it has yet to be integrated into broader concepts of vertebrate evolution. We map the most comprehensive data set of volitional sound production of ray-finned fishes (Actinopterygii) yet assembled onto a...

To what extent do modifications in the nervous system and peripheral effectors contribute to novel behaviors? Using a combination of morphometric analysis, neuroanatomical tract tracing and intracellular neuronal recording, we address this question in a sound producing and a weakly electric species of synodontid catfish, Synodontis grandiops and S....

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 essenti...

Galanin is a peptide that regulates pituitary hormone release, feeding, and reproductive and parental care behaviors. In teleost fish, increased galanin expression is associated with territorial, reproductively active males. Prior transcriptome studies of the plainfin midshipman (Porichthys notatus), a highly vocal teleost fish with two male morphs...

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 (qP...

Plainfin midshipman fish (Porichthys notatus) have a remarkable capacity to generate long duration advertisement calls known as hums, each of which may last for close to two hours and be repeated throughout a night of courtship activity during the breeding season. The midshipman's striking sound production capabilities provide a unique opportunity...

Motivated by studies of speech deficits in humans, several studies over the past two decades have investigated the potential role of a forkhead domain transcription factor, FoxP2, in the central control of acoustic signaling/vocalization among vertebrates. Comparative neuroanatomical studies that mainly include mammalian and avian species have mapp...

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 topographica...

A male's reproductive success often depends on both his phenotypic quality and the quality of the resources he controls. An important and longstanding challenge for evolutionary biologists has been to disentangle these 2 often-correlated factors. Here, we present a large multiyear, multipopulation field study along with complementary laboratory exp...

Reproductive success relies on the coordination of social behaviours, such as territory defence, courtship and mating. Species with extreme variation in reproductive tactics are useful models for identifying the neural mechanisms underlying social behaviour plasticity. The plainfin midshipman (Porichthys notatus) is a teleost fish with two male rep...

A central goal of comparative and evolutionary neurobiology is to establish how phenotypic variation in neuronal phenotypes translates into naturally selected diversity in behavioral performance. In this context, can we establish how the vocal-acoustic phenotypes of tetrapods were built over evolutionary time by identifying behavioral, anatomical,...

Teleost fish exhibit a diversity of reproductive phenotypes, including alternative reproductive tactics used by male morphs that differ in a suite of behavioral, somatic, neural, and endocrine traits. The hormonal and neurophysiological underpinnings of intrasexual divergence in reproductive-related behaviors are well studied in species that depend...

Inhibitory and modulatory profile of the vocal central pattern generator in the Gulf-toadfish, Opsanus beta

The patterning of social acoustic signaling at multiple timescales, from day-night rhythms to acoustic temporal properties, enhances sender-receiver coupling and reproductive success [1, 2, 3, 4, 5, 6, 7, 8]. In diurnal birds, the nocturnal production of melatonin, considered the major vertebrate timekeeping hormone [9, 10], suppresses vocal activi...

This volume on Hearing and Hormones for the Springer Handbook of Auditory Research (SHAR) series provides a broad comparative overview of hormonal influences on the behavioral and neural mechanisms of hearing in vertebrates. The chapters provide coverage for each of the major lineages of vocal vertebrates that have been foci of investigations of he...

Fishes, the most species-rich group of living vertebrates, present remarkable opportunities to investigate neural mechanisms underlying the sense of hearing. While the sound-producing and hearing abilities of fishes have long been known, it was not until the turn of this century that the influence of hormones on audition was first reported for fish...

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...

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 simil...

Medullary motoneurons drive vocalization in many vertebrate lineages including fish, amphibians, birds, and mammals. The developmental history of vocal motoneuron populations in each of these lineages remains largely unknown. The highly conserved transcription factor Paired-like Homeobox 2b (Phox2b) is presumed to be expressed in all vertebrate hin...

Background Vocalization is a prominent social behavior among vertebrates, including in the midshipman fish, an established model for elucidating the neural basis of acoustic communication. Courtship vocalizations produced by territorial males are essential for reproductive success, vary over daily and seasonal cycles, and last up to hours per call....

A mathematical model has been developed for vocalizations of the three-spined toadfish (Batrachomoeus trispinosus) and the plainfin midshipman (Porichthys notatus); acoustically active fish species that have served as model systems for studying acoustic communication mechanisms among vertebrates. The toadfish has a vocal organ comprised of a pair o...

While studies of sonic mechanisms among vertebrates date back more than 100 years, the past 25 years have witnessed a burgeoning of interest in the bioacoustics and behavioral ecology of sound production among fishes, including in its neural basis. Here, we review the body of comparative literature on the neuroanatomical, neurophysiological, and ne...

Animals that generate acoustic signals for social communication are faced with two essential tasks: generate a temporally precise signal and inform the auditory system about the occurrence of one's own sonic signal. Recent studies of sound producing fishes delineate a hindbrain network comprised of anatomically distinct compartments coding equally...

Among fishes, acoustic communication is best studied in toadfishes, a single order and family that includes species commonly known as toadfish and midshipman. However, there is a lack of comparative anatomical and physiological studies, making it difficult to identify both shared and derived mechanisms of vocalization among toadfishes. Here, vocal...

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 which flows through large-conductance calcium activated potassium (BK) channels. Previous work in midshipman fish (Porichthys notatus) has sho...

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 spectro-temporal characters of their...

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 elusiv...

Melatonin is a well-documented time-keeping hormone that can entrain an individual's physiology and behavior to the day-night cycle, though surprisingly little is known about its influence on the neural basis of social behavior, including vocalization. Male midshipman fish (Porichthys notatus) produce several call types distinguishable by duration...

Estrogens play a salient role in the development and maintenance of both male and female nervous systems and behaviors. The plainfin midshipman (Porichthys notatus), a teleost fish, has two male reproductive morphs that follow alternative mating tactics and diverge in multiple somatic, hormonal and neural traits, including the central control of mo...

Sensory plasticity related to reproductive state, hormonal profiles, and experience is widespread among vertebrates, including humans [1-5]. Improvements in audio-vocal coupling that heighten the detection of conspecifics are part of the reproductive strategy of many nonmammalian vertebrates [6, 7]. Although seasonal changes in hearing are known [7...

The midbrain periaqueductal gray (PAG) plays a central role in the descending control of vocalization across vertebrates. The PAG has also been implicated in auditory-vocal integration, though its precise role in such integration remains largely unexplored. Courtship and territorial interactions in plainfin midshipman fish depend on vocal communica...

Behavioral and neuroendocrine mechanisms of social vocalization in teleost fish are influenced by the glucocorticoid cortisol and the androgen 11-ketotestosterone (11kT). The relative abundance of both 11kT, which binds to androgen receptors (ARα, ARβ), and cortisol, which binds to glucocorticoid receptors (GR-1, GR-2), is regulated by 11β-hydroxyl...

Acoustic signaling behaviors are widespread among bony vertebrates, which include the majority of living fishes and tetrapods. Developmental studies in sound-producing fishes and tetrapods indicate that central pattern generating networks dedicated to vocalization originate from the same caudal hindbrain rhombomere (rh) 8-spinal compartment. Togeth...

Rapid temporal modulation of acoustic signals among several vertebrate lineages has recently been shown to depend on the actions of superfast muscles. We hypothesized that such fast events, known to require synchronous activation of muscle fibers, would rely on motoneuronal properties adapted to generating a highly synchronous output to sonic muscl...

Fishes, the largest group of living vertebrates, have evolved a unique array of sound-producing (sonic and vocal) organs to produce acoustic signals (vocalizations) in various social contexts. Most fish generate sound by vibrating either the swimbladder or the pectoral girdle with fast-contracting drumming muscles, by rubbing pectoral spines in gro...

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. I...

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...

Acoustic signals play essential roles in social communication and show a strong selection for novel morphologies leading to increased call complexity in many taxa. Among vertebrates, repeated innovations in the larynges of frogs and mammals and the syrinx of songbirds have enhanced the spectro-temporal content, and hence the diversity of vocalizati...

Corticosteroid receptors include mineralocorticoid (MR) and glucocorticoid (GR) receptors. Teleost fishes have a single MR and duplicate GRs that show variable sensitivities to mineralocorticoids and glucocorticoids. How these receptors compare functionally to tetrapod MR and GR, and the evolutionary significance of maintaining two GRs, remains unc...

Andrew H. Bass is a professor of Neurobiology and Behavior at Cornell University, Ithaca, New York. His research interests focus broadly on the evolution and sexual differentiation of the behavioral and neural mechanisms of social communication among vertebrates, and more specifically on the production and auditory encoding of vocal signals among t...

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 a...

The major classes of chemicals and brain pathways involved in sexual arousal in mammals are well studied and are thought to be of an ancient, evolutionarily conserved origin. Here we discuss what is known of these neurochemicals and brain circuits in fishes, the oldest and most species-rich group of vertebrates from which tetrapods arose over 350 m...

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)...

Supplementary Movie 1 Pectoral motoneurons in embryonic midshipman fish, Porichthys notatus. A representative example of fluorescent retrograde labelling from the fin bud showing the location of pectoral motoneurons along the anterior-posterior axis and their alignment with myotomes.

Supplementary Movie 2 Alignment of pectoral, precerebellar and hindbrain motor neurons in transgenic zebrafish, Danio rerio. A representative example of double labelling from the fin bud and cerebellum in the isl1-GFP background showing the alignment of pectoral motoneurons with identified hindbrain neuronal subgroups.

Supplementary Movie 3 Lineage tracing using the photoconvertable protein Kaede. A representative example of lineage tracing of the neuroepithelium at the level of somite 4–5 (anterior spinal cord) showing that pectoral motoneurons originated in both hindbrain and spinal cord without anterior-posterior migration during early neurogenesis.

Supplementary Figures S1–S5

Motor innervation to the tetrapod forelimb and fish pectoral fin is assumed to share a conserved spinal cord origin, despite major structural and functional innovations of the appendage during the vertebrate water-to-land transition. In this paper, we present anatomical and embryological evidence showing that pectoral motoneurons also originate in...

Across all major vertebrate groups, androgen receptors (ARs) have been identified in neural circuits that shape reproductive-related behaviors, including vocalization. The vocal control network of teleost fishes presents an archetypal example of how a vertebrate nervous system produces social, context-dependent sounds. We cloned a partial cDNA of A...

Estrogens rapidly regulate neuronal activity within seconds-to-minutes, yet it is unclear how estrogens interact with neural circuits to rapidly coordinate behavior. This study examines whether 17-beta-estradiol interacts with an opioidergic network to achieve rapid modulation of a vocal control circuit. Adult plainfin midshipman fish emit vocaliza...

The vocalizing midshipman fish, Porichthys notatus, has two male morphs that exhibit alternative mating tactics. Only territorial males acoustically court females with long duration (minutes to >1h) calls, whereas sneaker males attempt to steal fertilizations. During the breeding season, morph-specific tactics are paralleled by a divergence in rela...

The plainfin midshipman Porichthys notatus has two male reproductive morphs, ‘Type I’ and ‘Type II’, which are distinguishable by their physical traits alone. Type I males are eight times larger in body mass than Type II males and have a six-fold larger relative sonic (vocal) muscle mass than Type II males. In contrast, the testicles of Type II mal...

In terms of species number, teleost fishes are the largest group of living vertebrates. Current estimates show that the majority of all known orders of teleosts include species that produce sound, many of which have clear social communication functions. Fishes exhibit a diverse range of musculoskeletal mechanisms that may have independently evolved...

Fish exhibit a level of variation in sexual behavior that is unrivaled among other vertebrates. The major brain areas and neuroendocrine factors that control the development and adult maintenance of reproductive behavior and physiology in fish do not differ substantially from those known in mammals, suggesting that the examination of fish provides...

Seasonal and circadian rhythms control fundamental physiological processes including neural excitability and synaptic plasticity that can lead to the periodic modulation of motor behaviors like social vocalizations. Parental male midshipman fish produce three call types during the breeding season: long duration (min to >1 h) advertisement 'hums', f...

Corticosteroid signaling mechanisms mediate a wide range of adaptive physiological responses, including those essential to reproduction. Here, we investigated the presence and relative abundance of corticosteroid receptors during the breeding season in the plainfin midshipman fish (Porichthys notatus), a species that has two male reproductive morph...

Toadfishes (Teleostei: Batrachoididae) are one of the best-studied groups for understanding vocal communication in fishes. However, sounds have only been recorded from a low proportion of taxa within the family. Here, we used quantitative bioacoustic, morphological and phylogenetic methods to characterize vocal behavior and mechanisms in the three-...

In a teleost fish, the midshipman Porichthys notatus, androgens and estrogen rapidly modulate vocal motor patterning and contribute to seasonal changes in the frequency encoding of the eighth nerve. To identify potential sites of action of these steroids, as well as local estrogen synthesis (via conversion from testosterone by the enzyme aromatase)...

Calcium-activated, large conductance potassium (BK) channels in tetrapods are encoded by a single slo1 gene, which undergoes extensive alternative splicing. Alternative splicing generates a high level of functional diversity in BK channels that contributes to the wide range of frequencies electrically tuned by the inner ear hair cells of many tetra...

Despite the fact that toadfishes are one of the best‐studied taxa for understanding fish vocal communication, vocalizations have only been recorded from a low proportion of taxa within the family. Here, we describe the diverse vocal repertoire and novel swimbladder morphology of a tropical Pacific euryhaline toadfish, Batrachomoeus trispinosus. B....