Julie Estelle Elie

Vocal communication in social animals involves the production and perception of various calls that ethologists categorize into call types based on their acoustical structure and behavioral context. Whether these categories indicate distinct meanings for the animals remains unknown. The zebra finch, a gregarious songbird, uses ~11 call types that are known to communicate hunger, danger, or social conflict and to establish social contact and bonding. Using auditory discrimination tasks, we show that the birds both discriminate and categorize all the call types in their vocal repertoire. In addition, systematic errors were more frequent between call types used in similar behavioral contexts than could be expected from their acoustic similarity. Thus, zebra finches organize their calls into categories and create a mental representation of the meaning of these sounds.

Vocal communication in social animals involves the production and perception of various calls that ethologists categorize into call-types, based on their acoustical structure and the behavioral context of production. Whether animals perceive these categories and associate distinct meanings to them remains unknown. The zebra finch, a gregarious songbird, uses approximately 11 call-types to communicate hunger, danger, social conflict, and establish social contact and bonding. Using auditory discrimination tasks, we show that the birds discriminate and categorize all the call-types in their vocal repertoire. In addition, systematic errors were more frequent between call-types used in similar behavioral contexts than could be expected from their acoustic similarity. Thus, zebra finches organize their calls into categories and create a mental representation of the meaning of these sounds.

Vocal production learning (“vocal learning”) is a convergently evolved trait in vertebrates. To identify brain genomic elements associated with mammalian vocal learning, we integrated genomic, anatomical, and neurophysiological data from the Egyptian fruit bat (Rousettus aegyptiacus) with analyses of the genomes of 215 placental mammals. First, we identified a set of proteins evolving more slowly in vocal learners. Then, we discovered a vocal motor cortical region in the Egyptian fruit bat, an emergent vocal learner, and leveraged that knowledge to identify active cis-regulatory elements in the motor cortex of vocal learners. Machine learning methods applied to motor cortex open chromatin revealed 50 enhancers robustly associated with vocal learning whose activity tended to be lower in vocal learners. Our research implicates convergent losses of motor cortex regulatory elements in mammalian vocal learning evolution.

Some species have evolved the ability to use the sense of hearing to modify existing vocalizations, or even create new ones. This ability corresponds to various forms of vocal production learning that are all possessed by humans, and independently displayed by distantly related species. Among mammals, a few species, including the Egyptian fruit-bat, would possess such vocal production learning abilities. Yet the necessity of an intact auditory system for the development of the Egyptian fruit-bat typical vocal repertoire has not been tested. Here we addressed this gap by eliminating pups’ sense of hearing at birth and assessing its effects on vocal production in adulthood. The deafening treatment enabled us to both causally test these bats vocal learning ability and discern learned from innate aspects of their vocalizations. Leveraging wireless individual audio recordings from freely interacting adults, we show that a subset of the Egyptian fruit-bat vocal repertoire necessitates auditory feedback. Intriguingly, these affected vocalizations belong to different acoustic groups in the vocal repertoire of males and females. These findings open the possibilities for targeted studies of the mammalian neural circuits that enable sexually dimorphic forms of vocal learning. Significance Vocal production learning is the rare capacity amongst animals where hearing is used to modify or create new vocalizations. The Egyptian fruit-bat is believed to possess this capacity, yet whether they need audition to achieve a mature vocal repertoire is unknown. Furthermore, a systematic causal examination of learned and innate aspects of the entire repertoire has never been performed in a vocal learner. Here, we addressed these major gaps directly by abolishing hearing in Egyptian fruit-bats at birth and investigating its effects on the vocal production in adulthood. Leveraging simultaneous individual wireless audio-recordings from freely interacting adult bats, we identify the subset of learned vocalizations and provide evidence that vocal learning is sexually dimorphic in that species.

Vocal learning, the ability to modify vocal behavior based on experience, is a convergently evolved trait in birds and mammals. To identify genomic elements associated with vocal learning, we integrated new experiments conducted in the brain of the Egyptian fruit bat with analyses of the genomes of 222 placental mammals. We first identified an anatomically specialized region of the bat motor cortex containing direct monosynaptic projections to laryngeal motoneurons. Using wireless neural recordings of this brain region in freely vocalizing bats, we verified that single neuron activity in this region relates to vocal production. We profiled the open chromatin of this vocal-motor region, which we used to train machine learning models to identify enhancers associated with vocal learning across mammals. We found 201 proteins and 45 candidate enhancers that display convergent evolution associated with vocal learning, many of which overlapped loci associated with human speech disability. One such locus contains the neurodevelopmental transcription factors TSHZ3 and ZNF536 and multiple candidate vocal learning-associated enhancers, suggesting the co-evolution of protein and regulatory sequences underlying vocal learning. One-Sentence Summary: Analyses of bat neural activity and epigenomic data in a brain region involved in vocal behavior were used to identify proteins and regulatory elements associated with vocal learning in mammals.

A mind’s-eye view of others: Social interaction among groups of individuals is a complex proposition. Not only must an animal keep track of various vocalizations and direct interactions in the present but likely also their knowledge of every other individual and their history of interaction with that individual. Two papers begin to unravel the neuronal process by which such complexities are managed (see the Perspective by Sliwa). Báez-Mendoza et al . tracked the interactional dynamics among three Rhesus macaques and found that neurons in the dorsomedial prefrontal cortex represent details of the interaction, such as identity, context, and interaction history. Rose et al . remotely recorded from freely interacting Egyptian fruit bats and similarly found coordinated neural activity among individuals, a relationship between brain activity patterns and social preference, and that single neurons in the prefrontal cortex distinguished between the vocalizations of specific individuals. Together these papers reveal clear evidence for neuronal encoding of social interaction and identity. —SNV

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Acoustic communication signals are typically generated to influence the behavior of conspecific receivers. In songbirds, for instance, such cues are routinely used by males to influence the behavior of females and rival males. There is remarkable diversity in vocalizations across songbird species, and the mechanisms of vocal production have been studied extensively, yet there has been comparatively little emphasis on how the receiver perceives those signals and uses that information to direct subsequent actions. Here, we emphasize the receiver as an active participant in the communication process. The roles of sender and receiver can alternate between individuals, resulting in an emergent feedback loop that governs the behavior of both. We describe three lines of research that are beginning to reveal the neural mechanisms that underlie the reciprocal exchange of information in communication. These lines of research focus on the perception of the repertoire of songbird vocalizations, evaluation of vocalizations in mate choice, and the coordination of duet singing.