What do mammals have to say about the neurobiology of acoustic communication?

Neuroethology utilizes species-specific characteristics to address particular research questions. Krogh's principle suggests that for many problems, there's an ideal animal model. While traditional approaches focus on a few genetically tractable models (mice, flies, worms), a comparative approach offers unique advantages. This review examines the classical songbird model for auditory communication and explores the potential of other mammalian models, particularly mice and bats, which offer genetic tractability and diverse vocalizations. By combining classical neuroethological approaches with modern techniques, we can gain deeper insights into the neural mechanisms underlying acoustic communication.

Songbirds have long been the primary model for studying vocal learning and acoustic communication, due to the complexity of their songs and their ability to learn them. Research in songbirds has revealed the importance of auditory feedback in maintaining stable songs, identified song-selective neurons, and demonstrated the role of acoustic features like spectral contrast in driving neural responses. However, the avian brain differs significantly from the mammalian brain. Therefore, broadening our scope to include mammals is crucial for a more comprehensive understanding of acoustic communication.

This review article employs a comparative approach, analyzing existing literature on acoustic communication across various mammalian species. It focuses on selected species exhibiting diverse vocal repertoires and experimental advantages: dolphins, marmosets, prairie voles, naked mole-rats, and Alston's singing mice. The review then delves into the detailed study of mice and bats as prominent mammalian models. For mice, the review examines the communicative functions of ultrasonic vocalizations (USVs), focusing on recent advancements in molecular tools for precise neuronal control and identification of vocalizing animals. The role of the periaqueductal gray (PAG) and lateral preoptic area (LPOA) in USV production is explored. For bats, the review highlights their echolocation abilities and their diverse social calls. It discusses how neural selectivity for communication calls is present across brain regions and the impact of social context on auditory processing. The review integrates findings from diverse research approaches, including behavioral observations, electrophysiology, and molecular genetic manipulations.

The review underscores that while songbirds provide valuable insights, a comparative approach using mammalian models is essential for a more complete understanding of the neurobiology of acoustic communication. Mice, with their diverse repertoire of ultrasonic and low-frequency vocalizations, serve as an excellent model to study the neural mechanisms of vocal production, particularly through the use of molecular tools to control specific neurons. Research on mice has revealed crucial roles for the PAG and LPOA in USV production and highlighted the potential link between motivational state and vocalization. Bats, with their complex echolocation and social communication systems, offer unique advantages for studying auditory processing. Their diverse vocalizations, including learned calls in some species, provide a rich dataset for investigating neural selectivity and the integration of auditory information. Recent advances in genetic tools for bats have further enhanced the potential of this model. A comparative analysis across different mammalian species, focusing on the conserved neural networks involved in vocal production, such as the PAG, could reveal fundamental principles underlying acoustic communication.

The findings highlight the value of a comparative approach in unraveling the complexities of acoustic communication across species. The convergence of findings across songbirds, mice, and bats emphasizes the potential for shared neural mechanisms. However, species-specific differences also exist, suggesting that comparative studies can reveal the neural adaptations supporting diverse forms of communication. The use of molecular tools and genetic manipulation in mice and bats provides unprecedented opportunities to dissect the neural circuitry underlying acoustic communication at a fine-grained level, revealing potential therapeutic targets for communication disorders.

This review emphasizes the importance of expanding beyond traditional models to include diverse mammalian species like mice and bats in the study of acoustic communication. These models offer unique strengths in terms of genetic tractability, behavioral complexity, and technological accessibility. Future research should focus on comparative studies leveraging the strengths of various mammalian models to further elucidate the conserved and divergent neural mechanisms underlying this crucial biological process. Such research could have implications for understanding human communication disorders and informing conservation efforts.

The review's scope is limited to selected mammalian species and does not encompass the full diversity of mammalian vocal communication. While the reviewed studies provide valuable insights, more research is needed to fully understand the intricate interactions between various brain regions and the influence of hormones and neurotransmitters on acoustic communication. Furthermore, the interpretation of vocalizations and their associated behaviors remains challenging, demanding further refinement of behavioral analysis.