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
Genes including FOXP2, FOXP1, and CNTNAP2, have been implicated in human speech and language phenotypes, pointing to a role in the development of normal language‐related circuitry in the brain. Although speech and language are unique to humans a comparative approach is possible by addressing language‐relevant traits in animal systems. One such trait, vocal learning, represents an essential component of human spoken language, and is shared by cetaceans, pinnipeds, elephants, some birds and bats. Given their vocal learning abilities, gregarious nature, and reliance on vocalizations for social communication and navigation, bats represent an intriguing mammalian system in which to explore language‐relevant genes. We used immunohistochemistry to detail the distribution of FoxP2, FoxP1, and Cntnap2 proteins, accompanied by detailed cytoarchitectural histology in the brains of two vocal learning bat species; Phyllostomus discolor and Rousettus aegyptiacus. We show widespread expression of these genes, similar to what has been previously observed in other species, including humans. A striking difference was observed in the adult P. discolor bat, which showed low levels of FoxP2 expression in the cortex that contrasted with patterns found in rodents and nonhuman primates. We created an online, open‐access database within which all data can be browsed, searched, and high resolution images viewed to single cell resolution. The data presented herein reveal regions of interest in the bat brain and provide new opportunities to address the role of these language‐related genes in complex vocal‐motor and vocal learning behaviors in a mammalian model system.
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.
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