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The song control nucleus HVC of songbirds has emerged as a widespread model system to study adult neurogenesis and the factors that modulate the incorporation of new neurons, including seasonal state, sex differences or sex steroid hormone concentrations. However, the specific function of these new neurons born in adulthood remains poorly understood. We implemented a new procedure based on focal X-ray irradiation to deplete neural progenitors in the ventricular zone adjacent to HVC and study the functional consequences. A 23 Gy dose depleted by more than 50 percent the incorporation of BrdU in neural progenitors, a depletion that was confirmed by a significant decrease in doublecortin positive neurons. This depletion of neurogenesis significantly increased the variability of testosterone-induced songs in females and decreased their bandwidth. Expression of the immediate early gene ZENK in secondary auditory areas of the telencephalon that respond to song was also inhibited. These data provide evidence that new neurons in HVC play a role in both song production and perception and that X-ray focal irradiation represents an excellent tool to advance our understanding of adult neurogenesis.

Sound production in teleost fishes relies on diverse anatomical adaptations, yet convergent mechanisms involving extrinsic sonic muscles acting on the swim bladder are widespread. This study investigates the acoustic and morphological features of two priacanthid species, Indo-Pacific glasseye Heteropriacanthus carolinus and moontail bullseye Priacanthus hamrur to explore interspecific similarities in sound production. Using recordings and anatomical analyses, we show that both species rely on a forced-response mechanism, where the contraction rate of fast sonic muscles determines the fundamental frequency. This is corroborated by the smaller diameter of sonic fibres compared to epaxial fibres in both species. Despite belonging to different genera, both species exhibit extrinsic sonic muscles originating from the first pleural rib and inserting on the anterior swim bladder. However, P. hamrur displays anterior bladder projections potentially involved in enhanced hearing, absent in H. carolinus . Acoustic signals were broadly similar between species, suggesting that the morphological shift in muscle insertion does not affect sound structure. Comparative analysis across geographically distant populations of H. carolinus (Indian and Pacific Oceans) revealed variation in acoustic features that was size-dependent rather than region-specific. Juveniles emitted continuous pulse trains with high fundamental frequencies, whereas adults produced more segmented calls with lower frequencies. These ontogenetic differences reflect developmental modulation of vocal output, not anatomical changes. Overall, our findings highlight the conserved nature of sonic mechanisms in Priacanthidae, the influence of body size on acoustic variation, and the potential role of swim bladder morphology in auditory enhancement rather than sound generation.

Songbirds postnatally develop their skill to utter and to perceive a vocal signal for communication. How genetic and environmental influences act in concert to regulate the development of such skill is not fully understood. Here, we report the phenotype of transgenic songbirds with altered intrinsic activity of cAMP response element-binding protein (CREB) transcription factor. By viral vector-mediated modification of genomic DNA, we established germ line-transmitted lines of zebra finches, which exhibited enhanced or suppressed activity of CREB. Although intrinsically acquired vocalizations or their hearing ability were not affected, the transgenic birds showed reduced vocal learning quality of their own songs and impaired audio-memory formation against conspecific songs. These results thus demonstrate that appropriate activity of CREB is necessary for the postnatal acquisition of learned behavior in songbirds, and the CREB transgenic birds offer a unique opportunity to separately manipulate both genetic and environmental factors that impinge on the postnatal song learning. Significance In highly socialized animals such as humans or songbirds, individuals postnatally develop their skills to communicate with conspecifics under the social influence. Both genetic and environmental influences play a crucial role in the development of such abilities, but dissection of the influences has been difficult, because genetic manipulation of avian species is still a challenging issue. In this study, we applied transgenic technology to songbirds along with an experimental song-training paradigm to separately manipulate both genes and social environment, and found that appropriate activity of cAMP response element-binding protein (CREB) is necessary for the postnatal song learning in songbirds.

Animals produce vocalizations that range in complexity from a single repeated call to hundreds of unique vocal elements patterned in sequences unfolding over hours. Characterizing complex vocalizations can require considerable effort and a deep intuition about each species' vocal behavior. Even with a great deal of experience, human characterizations of animal communication can be affected by human perceptual biases. We present a set of computational methods for projecting animal vocalizations into low dimensional latent representational spaces that are directly learned from the spectrograms of vocal signals. We apply these methods to diverse datasets from over 20 species, including humans, bats, songbirds, mice, cetaceans, and nonhuman primates. Latent projections uncover complex features of data in visually intuitive and quantifiable ways, enabling high-powered comparative analyses of vocal acoustics. We introduce methods for analyzing vocalizations as both discrete sequences and as continuous latent variables. Each method can be used to disentangle complex spectro-temporal structure and observe long-timescale organization in communication.

Vocalization is an ancient vertebrate trait essential to many forms of communication, ranging from courtship calls to free verse. Vocalizations may be entirely innate and evoked by sexual cues or emotional state, as with many types of calls made in primates, rodents and birds; volitional, as with innate calls that, following extensive training, can be evoked by arbitrary sensory cues in non-human primates and corvid songbirds; or learned, acoustically flexible and complex, as with human speech and the courtship songs of oscine songbirds. This review compares and contrasts the neural mechanisms underlying innate, volitional and learned vocalizations, with an emphasis on functional studies in primates, rodents and songbirds. This comparison reveals both highly conserved and convergent mechanisms of vocal production in these different groups, despite their often vast phylogenetic separation. This similarity of central mechanisms for different forms of vocal production presents experimentalists with useful avenues for gaining detailed mechanistic insight into how vocalizations are employed for social and sexual signalling, and how they can be modified through experience to yield new vocal repertoires customized to the individual's social group. This article is part of the theme issue ‘What can animal communication teach us about human language?’

Rapid and reversible manipulations of neural activity in behaving animals are transforming our understanding of brain function. An important assumption underlying much of this work is that evoked behavioural changes reflect the function of the manipulated circuits. We show that this assumption is problematic because it disregards indirect effects on the independent functions of downstream circuits. Transient inactivations of motor cortex in rats and nucleus interface (Nif) in songbirds severely degraded task-specific movement patterns and courtship songs, respectively, which are learned skills that recover spontaneously after permanent lesions of the same areas. We resolve this discrepancy in songbirds, showing that Nif silencing acutely affects the function of HVC, a downstream song control nucleus. Paralleling song recovery, the off-target effects resolved within days of Nif lesions, a recovery consistent with homeostatic regulation of neural activity in HVC. These results have implications for interpreting transient circuit manipulations and for understanding recovery after brain lesions. Transient manipulation of neural activity is widely used to probe the function of specific circuits, yet such targeted perturbations could also have indirect effects on downstream circuits that implement separate and independent functions; a study to test this reveals that transient perturbations of specific circuits in mammals and songbirds severely impair learned skills that recover spontaneously after permanent lesions of the same brain areas. Confounding effects of optogenetics The development of optogenetics as a specific tool to probe the function of genetically defined neural circuits in the execution of specific behaviours has been a prominent field of recent growth in neuroscience. However, many of these studies disregard the potential for indirect effects of circuit manipulation on other downstream circuits operating independently in separate functions. Here, Bence Ölveczky and colleagues reveal how transient inactivation of specific circuits in mammals and songbirds can severely impair task-specific responses that otherwise spontaneously recover after permanent lesions of the same brain areas. This suggests that additional considerations must be taken into account when interpreting data from transient circuit manipulations of behaviour.

Communication plays an integral role in human social dynamics and is impaired in several neurodevelopmental disorders. Mice are used to study the neurobiology of social behavior; however, the extent to which mouse vocalizations influence social dynamics has remained elusive because it is difficult to identify the vocalizing animal among mice involved in a group interaction. By tracking the ultrasonic vocal behavior of individual mice and using an algorithm developed to group phonically similar signals, we showed that distinct patterns of vocalization emerge as male mice perform specific social actions. Mice dominating other mice were more likely to emit different vocal signals than mice avoiding social interactions. Furthermore, we showed that the patterns of vocal expression influence the behavior of the socially engaged partner but do not influence the behavior of other animals in the cage. These findings clarify the function of mouse communication by revealing a communicative ultrasonic signaling repertoire.A sound source localization system reveals behavior-dependent vocal emission and thereby unmasks functions of social vocalization.

Sperm whales ( Physeter macrocephalus ) are highly social mammals that communicate using sequences of clicks called codas. While a subset of codas have been shown to encode information about caller identity, almost everything else about the sperm whale communication system, including its structure and information-carrying capacity, remains unknown. We show that codas exhibit contextual and combinatorial structure. First, we report previously undescribed features of codas that are sensitive to the conversational context in which they occur, and systematically controlled and imitated across whales. We call these rubato and ornamentation. Second, we show that codas form a combinatorial coding system in which rubato and ornamentation combine with two context-independent features we call rhythm and tempo to produce a large inventory of distinguishable codas. Sperm whale vocalisations are more expressive and structured than previously believed, and built from a repertoire comprising nearly an order of magnitude more distinguishable codas. These results show context-sensitive and combinatorial vocalisation can appear in organisms with divergent evolutionary lineage and vocal apparatus. Sperm whales use sequences of clicks to communicate. Here, the authors show that these vocalizations are significantly more complex than previously believed-the “sperm whale phonetic alphabet\" has both combinatorial structure and call modulation dependent on the conversational context.

Many behaviors are learned through trial and error by matching performance to internal goals. Yet neural mechanisms of performance evaluation remain poorly understood. We recorded basal ganglia—projecting dopamine neurons in singing zebra finches as we controlled perceived song quality with distorted auditory feedback. Dopamine activity was phasically suppressed after distorted syllables, consistent with a worse-than-predicted outcome, and was phasically activated at the precise moment of the song when a predicted distortion did not occur, consistent with a better-than-predicted outcome. Error response magnitude depended on distortion probability. Thus, dopaminergic error signals can evaluate behaviors that are not learned for reward and are instead learned by matching performance outcomes to internal goals.

Bird song has historically been considered an almost exclusively male trait, an observation fundamental to the formulation of Darwin’s theory of sexual selection. Like other male ornaments, song is used by male songbirds to attract females and compete with rivals. Thus, bird song has become a textbook example of the power of sexual selection to lead to extreme neurological and behavioural sex differences. Here we present an extensive survey and ancestral state reconstruction of female song across songbirds showing that female song is present in 71% of surveyed species including 32 families, and that females sang in the common ancestor of modern songbirds. Our results reverse classical assumptions about the evolution of song and sex differences in birds. The challenge now is to identify whether sexual selection alone or broader processes, such as social or natural selection, best explain the evolution of elaborate traits in both sexes. Bird song is commonly seen as a male trait that plays a role in female attraction, but its origin and prevalence in females are unknown. Here, Odom et al. show that female song is widespread and that it was present in the common ancestor of modern songbirds.