Convergent and divergent neural circuit architectures that support acoustic communication

Abstract

Vocal communication is used across extant vertebrates, is evolutionarily ancient, and been maintained, in many lineages. Here I review the neural circuit architectures that support intraspecific acoustic signaling in representative anuran, mammalian and avian species as well as two invertebrates, fruit flies and Hawaiian crickets. I focus on hindbrain motor control motifs and their ties to respiratory circuits, expression of receptors for gonadal steroids in motor, sensory, and limbic neurons as well as divergent modalities that evoke vocal responses. Hindbrain and limbic participants in acoustic communication are highly conserved, while forebrain participants have diverged between anurans and mammals, as well as songbirds and rodents. I discuss the roles of natural and sexual selection in driving speciation, as well as exaptation of circuit elements with ancestral roles in respiration, for producing sounds and driving rhythmic vocal features. Recent technical advances in whole brain fMRI across species will enable real time imaging of acoustic signaling partners, tying auditory perception to vocal production.

Evolution of air‐borne vocalization: Insights from neural studies in the archeobatrachian species Bombina orientalis

“…In comparison to birds, mammals and anurans likely share the neural network architecture of vocal circuits due to their developmental and evolutionary origin (recently reviewed by Barkan & Zornik, 2020; Kelley, 2022). Our results suggest that the archeobatrachian species B. orientalis is an excellent model organism to study the basics of vocal pattern generation in tetrapods.…”

“…We hypothesize that these differences in the duration of activations should be shown also in an isolated brain preparation of B. orientalis , which has proven to have many advantages for neurobiological research (e.g., Barkan et al., 2017; Leininger & Kelley, 2015; Luksch & Walkowiak, 1998; Luksch et al., 1996). Fictive vocalizations in frogs are known to be elicited and triggered by stimulation of ventral forebrain areas (VFA) such as the extended amygdala as well as the preoptic area (Knorr, 1976; Schmidt, 1973; Brahic & Kelley 2003; Ballagh, 2014; Hall et al., 2013; Kelley, 2022; Kelley et al., 2020). Additionally, fictive vocalizations can be reliably elicited after stimulation of the statoacoustic nerve (N. VIII; Fig.…”

“…Accordingly, all choanates (lungfishes and tetrapods) are thought to use acoustic communication as a homologous trait and lung‐associated structures as the physical force generator of their calling behaviors (Jorgewich‐Cohen et al., 2022). Thus, it is likely that the anuran central pattern generator (CPG) for vocalization could be evolved from more ancient respiratory circuits and be made up of homologous components that generate breathing rhythms across vertebrates (Kelley, 2022; Kelley et al., 2020), although homologies of some nuclei are not clear, so far (Barkan & Zornik, 2020). Nevertheless, it is clear that the functional connection between respiration and vocalization is an evolutionary conserved feature but may be evolved independently in the different tetrapod clades (Barkan & Zornik, 2020; Chen & Wiens, 2020).…”

Two conserved vocal central pattern generators broadly tuned for fast and slow rates generate species-specific vocalizations inXenopusclawed frogs

“…Importantly, Schmidt discovered local field potential activity from the PBN accompanying fictive advertisement calling in the leopard frog, Rana pipiens (Schmidt, 1992), suggesting the conserved role of the PBN in generating vocalizations via exhalation of air in terrestrial species. Considering that the family Ranidae , which includes R. pipiens , diverged from the family Pipidae – which includes the Xenopus genus - ~ 205 million years ago (Roelants et al, 2007) and that amphibians diverged from the Amniota ~ 340 million years ago (Pardo et al, 2017), it is most parsimonious to assume that the involvement of the PBN in vocal production is an ancestral trait in Xenopus (Kelley, 2022). Interestingly, Schmidt observed that the bilateral transection between the PBN and the NA eliminated fictive advertisement calling but that fictive pulmonary respiration persisted in the caudal brainstem of R. pipiens .…”

The neurobiology of vocal communication in marmosets

“…The neural basis of primate vocal production has been hotly debated for many years. One recent model 114 states a division into two separate networks (Figure 3), distinguishing between the primary vocal motor network (PVMN), which exists across species, 149 and the volitional articulatory motor network (VAMN). The hypothesis suggests that the VAMN only exists in primate species 114 .…”