Sexually distinct development of vocal pathways in Xenopus laevis

Abstract

Deterministic rules, rather than experience, are thought to regulate the development of simple behaviors in vertebrates and invertebrates. We revisited this issue through examination of the sexually distinct vocalizations of African clawed frogs (Xenopus laevis), a reproductive behavior used by sexually mature males and females. We discovered that, as expected for simple behavior, female vocalizations develop through deterministic rules r. The rare calls of juvenile females are indistinguishable from those of adult females. The vocal pathways of juvenile females, as measured by the contractile properties of the laryngeal muscles (the vocal muscles) and the laryngeal motoneuron somata (vocal motoneurons) size, are the developmental default and do not differentiate as they mature. Male Xenopus, in contrast, produce extensive vocalizations with rudimentary acoustic structure before reaching sexual maturity. Moreover, the functional properties of the vocal central pattern generator mature before muscle fibers and motoneuron size are fully masculinized. The results suggest that neuronal activity during development may be important in organizing the contractile properties of the muscle fibers in male, but not in female Xenopus.

Adeno-Associated Viral Tools to Trace Neural Development and Connectivity Across Amphibians

“…Both AAV5 and AAVrg efficiently transduced neurons around the injection site, as visible in coronal and horizontal sections ( Figure 5A-C) . Labeling efficiency in Xenopus was comparable in both small ( Figure 5A-B ) and larger sexually mature ( Figure 5C ) 95 frogs, as well as in animals at varying stages of intermediate maturity ( Table S1 and S2 ). In contrast, injection of AAV2, AAVrg, AAV1, AAV5, AAV9, or AAV-PHP.eB in the telencephalon (intracerebroventricular injections) of wild-caught adult Pelophylax bedriagae did not produce any GFP expression ( Table S1 ).…”

Impact of Early Postnatal Androgen Exposure on Voice Development

“…Current knowledge of the mechanism by which steroids induce sexual differentiation of vocal production at the brain level is limited to animal models, particularly songbirds [34] and female African clawed frogs ( Xenopus laevis ) [35], [36]. The female laryngeal muscle differs from the male laryngeal muscle [37], as most female laryngeal neuromuscular synapses are stronger than the corresponding male synapses [38]–[40].…”

A neuroendocrine basis for the hierarchical control of frog courtship vocalizations

“…During this period, females rarely vocalize, but when they do, calls are indistinguishable from adult female ticking [26]. In contrast, maturing males produce rudimentary vocalizations that fall into three broad categories.…”

“…Only a small fraction of these animals still produced fast trills, and even those calls were acoustically abnormal: truncated or with reduced sound intensity. Many castrated males produced only isolated slow trills, a pattern that has not been observed in mature males [17; 18; 19], but does resemble vocal patterns observed in developing juvenile males [26] and testosterone-treated females [28]. Changes in components of the vocal circuit that could be responsible for these behavioral alterations include decreased input from the CeA, a degraded CPG, a demasculinized larynx, or a combination.…”

“…One reasonable hypothesis is that stages in the masculinization of calls in T-treated females reflect the appearance of I h or I KL , two male-typical motor neuron conductances. Similarly, upregulation of NMDA-R expression in PbN neurons, necessary for fast trill production [66], may also support the switch from isolated slow trill production to biphasic calling in both juvenile males and TFs [26; 29]. The role of specific ion channels in the physiological properties of male and female motor neurons can be tested directly by transfection of cDNAs in the vocal slice preparation.…”