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

Biology

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

A. Salles and J. Neunuebel

Dive into the fascinating world of auditory communication with insights from Angeles Salles and Joshua Neunuebel. This research explores the neurobiology of acoustic communication, highlighting the unique traits of songbirds, mice, and bats, and delving into comparative approaches across mammalian species. Discover the secrets of how diverse vocal repertoires unravel fundamental principles of communication!... show more
Introduction

The paper frames the study of acoustic communication within neuroethology and advocates expanding beyond traditional model systems (e.g., songbirds) to comparative mammalian approaches. Grounded in Krogh’s principle, the authors argue that combining innate behaviors in diverse species with modern systems and molecular neuroscience can reveal general principles of auditory communication. They position songbirds as foundational for understanding vocal learning and neural selectivity but note differences between avian and mammalian brains. The purpose is to leverage insights from birds while emphasizing mammals (with a focus on mice and bats) to uncover conserved and divergent neural mechanisms of vocal production and auditory processing in social contexts.

Literature Review

Songbirds: Longstanding models for vocal learning with complex, learned songs that parallel aspects of human speech. Stable song requires auditory feedback; neurons selective for species-specific sounds reside in caudomedial nidopallium and Field L (auditory cortex homolog), with responses modulated by social context and experience. Selectivity is driven by discrete frequency components and spectral contrast rather than harmonicity, and temporal/spectral modulations are especially salient. Experience-dependent tuning and top-down influences are prominent in medial caudal mesopallium and other auditory forebrain areas. Mammalian landscape: Multiple taxa provide complementary windows into communication processing. Delphinids exhibit complex vocal learning with evolutionary interest (hippo-whale clade). Marmosets possess rich repertoires and premotor cortical vocal-only neurons. Prairie voles link hormones (e.g., oxytocin) to affiliative behaviors and vocalizations. Naked mole-rats display antiphonal calling, large repertoires, and colony-specific soft chirps suggestive of cultural transmission. Alston’s singing mice engage in temporally precise, cortically dependent, socially modulated vocal interactions. Collectively these species highlight opportunities to map circuits connecting perception, motivation, hormones, and vocal motor control.

Methodology
Key Findings
  • Mice: Use both audible squeaks and ultrasonic vocalizations (USVs) in context-dependent ways (e.g., pup isolation calls, adult courtship and social interactions). Both sexes can produce USVs during courtship when sound source localization is applied. Mouse models with FOXP2 mutations and autism-related genes exhibit altered USV structure and sequencing, supporting translational relevance. Circuit studies identify LPOA neurons (ER1+) projecting to the PAG that evoke naturalistic USVs; PAG neuron activation gates vocal output and interfaces with downstream patterning circuits. Motivational state is hypothesized to shape vocal classes, but its circuit implementation remains unresolved.
  • Bats: Audio-vocal specialists with adaptable ultrasonic emissions for echolocation and rich social repertoires, including in some species vocal learning. Neural selectivity for communication calls occurs across inferior colliculus and auditory cortex, with population dynamics supporting call categorization; affective regions (amygdala and PAG) also encode social calls. Frontal cortex can integrate auditory information for identity coding in social groups. Molecular era advances include Bat1K genomes and the first transgenic bat (manipulating FoxP2). Neuromodulators and stress hormones in the amygdala respond to distress calls during live interactions. Several species demonstrate vocal learning and babbling-like behaviors (e.g., Saccopteryx bilineata, Rousettus aegyptiacus, Phyllostomus discolor), enabling developmental studies of learning.
  • Comparative circuit opportunity: The PAG is a conserved hub receiving POA and amygdala inputs and projecting to laryngeal/expiratory motor neurons. Mouse and bat experiments show PAG involvement in social call emission; in bats, additional parallel circuits exist for echolocation (e.g., PLA stimulation elicits echolocation but not communication calls), suggesting separable pathways for different vocal modes. Mice possess a PLA, but its role in vocalization is unknown.
  • General principle: Social context, experience, and salient acoustic features shape neural selectivity and behavior across taxa; modern genetic, chemogenetic, connectomic, and computational tools now enable unified, cross-species investigations.
Discussion

The review argues that expanding beyond the bird paradigm to mammalian models addresses the central question of how neural circuits support acoustic communication by leveraging conserved structures (e.g., PAG-centered vocal circuits) and species-specific specializations (e.g., bat echolocation). Findings in mice demonstrate genetically and anatomically tractable circuits for vocal production and social modulation; bats reveal rich social call processing and learning, with affective and frontal regions contributing to categorization and identity coding. Together, these insights suggest that auditory communication emerges from interactions among sensory selectivity, motivational/affective states, learning/experience, and motor patterning circuits. A comparative approach promises to identify shared circuit motifs (e.g., POA/Amg→PAG→motor pathways) and divergent solutions (e.g., bat PLA pathways for echolocation) that clarify principles generalizable to humans and other mammals.

Conclusion

The paper synthesizes foundational songbird research with emerging mammalian work to propose a comparative framework for studying the neurobiology of acoustic communication. Key contributions include highlighting conserved midbrain vocal hubs (PAG), delineating mouse circuits for USV control, documenting bat call selectivity across auditory and affective pathways, and emphasizing molecular advances (e.g., Bat1K, transgenic bats). Future directions include: cross-species, standardized experimental designs; causal dissection of motivation and hormonal modulation in vocal circuits; mapping parallel pathways for different vocal modes (communication vs echolocation); integrating genetics (e.g., FOXP2 and other candidates) with systems-level measurements; and applying insights to human communication disorders and conservation biology.

Limitations

As a narrative review, the paper does not present new experimental data. Cross-taxa comparisons are constrained by heterogeneous methodologies and analytic frameworks across studies. Circuit-level mechanisms for motivational state, hormonal modulation, and social context are incompletely resolved, particularly in mice (e.g., motivation-to-circuit mapping) and in bats (e.g., functional role of the PLA in non-echolocating mammals, breadth of molecular toolkits across species). Differences between avian and mammalian brain architectures limit direct generalization from songbirds. The field remains nascent for some mammalian taxa, and more standardized, causal, and longitudinal studies are needed.

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