Inspiring song: The role of respiratory circuitry in the evolution of vertebrate vocal behavior

Abstract

Vocalization is a common means of communication across vertebrates, but the evolutionary origins of the neural circuits controlling these behaviors are not clear. Peripheral mechanisms of sound production vary widely: fish produce sounds with a swimbladder or pectoral fins; amphibians, reptiles, and mammalians vocalize using a larynx; birds vocalize with a syrinx. Despite the diversity of vocal effectors across taxa, there are many similarities in the neural circuits underlying the control of these organs. Do similarities in vocal circuit structure and function indicate that vocal behaviors first arose in a single common ancestor, or have similar neural circuits arisen independently multiple times during evolution? In this review, we describe the hindbrain circuits that are involved in vocal production across vertebrates. Given that vocalization depends on respiration in most tetrapods, it is not surprising that vocal and respiratory hindbrain circuits across distantly related species are anatomically intermingled and functionally linked. Such vocal‐respiratory circuit integration supports the hypothesis that vocal evolution involved the expansion and functional diversification of breathing circuits. Recent phylogenetic analyses, however, suggest vocal behaviors arose independently in all major tetrapod clades, indicating that similarities in vocal control circuits are the result of repeated co‐options of respiratory circuits in each lineage. It is currently unknown whether vocal circuits across taxa are made up of homologous neurons, or whether vocal neurons in each lineage arose from developmentally and evolutionarily distinct progenitors. Integrative comparative studies of vocal neurons across brain regions and taxa will be required to distinguish between these two scenarios.

Mapping the vocal circuitry of Alston's singing mouse with pseudorabies virus

“…Perhaps more closely related to the current study, the cell groups of A5 and A6 also play antagonistic roles in the regulation of respiratory rhythms (Guyenet et al., 1993; Hilaire et al., 2004). The neural circuitry underlying breathing is obviously of broad relevance to vocalization in general (Barkan & Zornik, 2020), and in singing mice, each note of its song is accompanied by a short breath (Okobi, 2016; Pasch et al., 2011a)…”

“…Among the many forms of display, perhaps none is more widespread or well‐studied than vocalization (Barkan & Zornik, 2020; Zhang & Ghazanfar, 2020). Phylogenetic studies reveal that vocalization is common and arose only a few times during vertebrate evolution (Z. Chen & Wiens, 2020).…”

Proposing a neural framework for the evolution of elaborate courtship displays

“…While much is still to be learned about the neural circuitry underlying the most complex courtship behaviors (e.g. those produced by the manakins), much progress has been made in our understanding of the neural control of acoustic displays ( Barkan and Zornik, 2020 ; Ladich and Winkler, 2017 ; Suthers et al, 2004 ). In fact, close examination of the neural underpinnings of acoustic courtship provides important hints about mechanistic principles that can be applied to elaborate courtship behavior more broadly.…”

Data_Sheet_1.docx

“…The ability to vocalize is an essential form of communication in nearly all vertebrates (Barkan and Zornik, 2020). Analysis of laboratory rodent ultrasonic vocalizations (USVs) has served as a powerful model system for understanding the neural circuits underlying vocal communication, social and affiliative behaviors, and neurodevelopmental disorders (Hofer, 1996;Holy and Guo, 2005;Scattoni et al, 2009;Fischer and Hammerschmidt, 2011;Wöhr and Schwarting, 2013;Portfors and Perkel, 2014;Segbroeck et al, 2017).…”

“…Analysis of laboratory rodent ultrasonic vocalizations (USVs) has served as a powerful model system for understanding the neural circuits underlying vocal communication, social and affiliative behaviors, and neurodevelopmental disorders (Hofer, 1996;Holy and Guo, 2005;Scattoni et al, 2009;Fischer and Hammerschmidt, 2011;Wöhr and Schwarting, 2013;Portfors and Perkel, 2014;Segbroeck et al, 2017). Much of the circuitry responsible for innate vocalization (e.g., rodent USVs, cries, and other non-verbal emotional utterances) is evolutionarily conserved in mammals, and develops prenatally, allowing infants and rodent pups to vocalize readily after birth (Hofer, 1996;Roubertoux et al, 1996;Arriaga et al, 2012;Hernandez-Miranda et al, 2017;Barkan and Zornik, 2020). Identifying the precise molecular instructive signals that are required for the development of neural-mediated vocal function will provide a foundational understanding of the circuitry underlying vocal production and has implications for understanding how communication deficits arise.…”