Generation, Coordination, and Evolution of Neural Circuits for Vocal Communication

Abstract

In many species, vocal communication is essential for coordinating social behaviors including courtship, mating, parenting, rivalry, and alarm signaling. Effective communication requires accurate production, detection, and classification of signals, as well as selection of socially appropriate responses. Understanding how signals are generated and how acoustic signals are perceived is key to understanding the neurobiology of social behaviors. Here we review our long-standing research program focused on Xenopus, a frog genus which has provided valuable insights into the mechanisms and evolution of vertebrate social behaviors. In Xenopus laevis, vocal signals differ between the sexes, through development, and across the genus, reflecting evolutionary divergence in sensory and motor circuits that can be interrogated mechanistically. Using two ex vivo preparations, the isolated brain and vocal organ, we have identified essential components of the vocal production system: the sexually differentiated larynx at the periphery, and the hindbrain vocal central pattern generator (CPG) centrally, that produce sex-and species-characteristic sound pulse frequencies and temporal patterns, respectively. Within the hindbrain, we have described how intrinsic membrane properties of neurons in the vocal CPG generate species-specific vocal patterns, how vocal nuclei are connected to generate vocal patterns, as well as the roles of neurotransmitters and neuromodulators in activating the circuit. For sensorimotor integration, we identified a key forebrain node that links auditory and vocal production circuits to match socially appropriate vocal responses to acoustic features of male and female calls. The availability of a well supported phylogeny as well as reference genomes from several species now support analysis of the genetic architecture and the evolutionary divergence of neural circuits for vocal communication. Xenopus thus provides a vertebrate model in which to study vocal communication at many levels, from physiology, to behavior, and from development to evolution. As one of the most comprehensively studied phylogenetic groups within vertebrate vocal communication systems, Xenopus provides insights that can inform social communication across phyla.

Spontaneous social communication in laboratory mice - placing ultrasonic vocalizations in their behavioral context

“…Social communication regulates major biological functions under strong selective pressure, such as finding reproductive partners, raising progeny, group coordination for territory advertisement, and protection from predators (Bradbury and Vehrencamp, 2011). It is not yet clear whether the mechanisms underlying these functions are conserved during evolution, but an increasing number of species has been studied to identify genes and brain circuits related to social interaction and communication (e.g., (Arriaga et al, 2012;Chen and Hong, 2018;Kelley et al, 2020;Tu et al, 2019)). Such knowledge on the phylogeny and ontogeny of social communication abilities is also clinically important to better understand the causes underlying neuropsychiatric conditions.…”

Neurogenomic divergence during speciation by reinforcement of mating behaviors in chorus frogs (Pseudacris)

“…The genetic architecture of mating behaviors is understudied in anuran amphibians, with examples being largely limited to visual signals [ 114 , 115 ]. Information regarding the genetic basis of acoustic signaling and processing in frogs is even more scarce [ 116 ]. Nonetheless, insight can be gained from insects that exhibit temporal variation in elements of acoustic mating signals in a similar way to many frogs.…”

“…Quantitative trait mapping studies on Hawaiian crickets (genus Laupala ) have shown that candidate genes underlying temporal information in acoustic signals include genes encoding a cyclic nucleotide-gated ion channel, a calcium release-activated calcium channel, a signal peptide peptidase-like protein gene, a putative synaptic vesicle related protein [ 127 ], three of which fall within the bounds of synaptic transmission gene categories targeted in this study (Table 1 ). In frogs, [ 116 ], suggested that membrane currents of fast pulse rate neurons in the parabranchial nucleus of the brain are likely to mediate divergence of acoustic signals among Xenopus species and that these differences probably involve differential expression of ion channels. Though little is known about the genetic basis for species-specific acoustic differences, their ongoing work will examine gene expression differences within specific vocal and auditory neurons across this genus [ 116 ].…”

Vocal and Electric Fish: Revisiting a Comparison of Two Teleost Models in the Neuroethology of Social Behavior

“…Neuromodulators acting at select loci in neural circuits contribute to such plasticity in signal production. In frog ( Rhodes et al, 2007 ; Yu and Yamaguchi, 2010 ; Kelley et al, 2020 ) and bird vocal systems ( Wood et al, 2011 ), serotonin (5HT) is one such modulator. The organization of the serotonergic system is highly conserved among teleost fishes ( Lillesaar et al, 2007 ; Lillesaar, 2011 ; Lillesaar and Gaspar, 2019 ), and the widespread distribution of serotoninergic neurons in brains of this more ancestral vertebrate group suggests that 5HT may have played an important role in the evolution of neuroendocrine mechanisms regulating vertebrate communication behavior.…”