Neuroeffectors for vocalization in Xenopus laevis: Hormonal regulation of sexual dimorphism

Abstract

South African clawed frogs use sex-specific vocalizations during courtship. In the male, vocalizations are under the control of gonadal androgen. Though females have moderate levels of circulating androgen, they do not give male-typical mate calls. Both muscles of the vocal organ and neurons of the central nervous system (CNS) vocal pathway are sexually dimorphic and androgen-sensitive. Recent studies suggest that the failure of androgen to masculinize adult females results from a male-specific, androgen-regulated developmental program. At metamorphosis the larynx is sexually monomorphic and feminine in morphology, muscle fiber number and androgen receptor content. During the next six months, under the influence of increasing androgen titers and high receptor levels, myoblasts proliferate in the male and muscle fibers increase at an average rate of 100/day. Females have much lower hormone levels, receptor values decline and they display no net addition of fibers. At metamorphosis, both males and females have approximately 4000 muscle fibers. By adulthood, males have eight times the female fiber number. In the CNS, adult laryngeal motor neurons are more numerous with larger somata and dendritic trees in males than in females. Certain connections of neurons in the vocal pathway are also less robust in females. Unlike the periphery, motor neuron number does not appear to be established by androgen-induced proliferation. Our current hypothesis is that androgen acts at the level of laryngeal muscle to produce more muscle fibers and thus provide more target for motor neurons in the male. This process could regulate cell number by ontogenetic cell death. In the CNS, androgen-target neurons become capable of accumulating hormone shortly before metamorphosis. Androgen receptor in laryngeal motor neurons may permit the dendritic growth characteristic of males by increasing sensitivity to afferent stimuli. Such a process could account for the observed differences in CNS vocal "circuitry" in X. laevis and thus behavioral differences between the sexes.

Central pattern generators for social vocalization: Androgen-dependent neurophysiological mechanisms

“…Sites of androgen receptors in vocal nuclei have long been well-documented for amphibians ( Fig. 1B; Kelley, 1986;Perez et al, 1996). Although this review does not focus on birds, they are among the most extensively studied group of vocal vertebrates for the mapping of steroid receptor sites and so we show the avian vocal nuclei that contain androgen receptors to provide a broader comparative context ( Fig.…”

“…Among frogs (Fig. 1B), androgen target vocal nuclei include the motor nucleus IX-X that innervates laryngeal muscles (also have abundant androgen receptors), the adjacent reticular formation, and DTAM (Kelley, 1986;Perez et al, 1996). For songbirds and hummingbirds (Fig.…”

“…In particular, the mVAC includes the midbrain's periaqueductal gray that directly links forebrain vocal sites in the anterior hypothalamus to the vocal CPG. (B) Amphibians (adapted from Wetzel et al, 1985 andKelley, 1986 Bass et al, 1996). Following application of biocytin to the cut end of the vocal nerve that innervates a single vocal muscle, both the midline vocal motor nucleus (VMN) and the adjacent column of pacemaker neurons (VPN) are labeled bilaterally (v, fourth ventricle).…”

Act locally and think globally: Intracerebral testosterone implants induce seasonal-like growth of adult avian song control circuits

“…(ii) T may directly stimulate the syringeal muscles, which have AR (29)(30)(31). The motor neurons in nXIIts innervate these muscles and might derive retrograde trophic support from them, as observed in the spinal nucleus of the bulbocavernosus of rats (61,62) and the laryngeal motor nucleus of Xenopus (63). (iii) Neurons in nXIIts receive afferent input from the dorsomedial portion of the intercollicular nucleus (ICo), which has AR (e.g., ref.…”

Courtship and copulation in the adult male green anole: Effects of season, hormone and female contact on reproductive behavior and morphology

“…Similarly, mammalian copulation involves muscles surrounding the base of the penis that are innervated by motoneurons in the caudal spinal cord [13]. Many of these structures exhibit plasticity that parallel seasonal or T-induced changes in behavior [10,12,14,20,49,62,65,82,83,92], and they have provided valuable insights about relationships between behavior and morphology. However, full appreciation for key mechanisms may be diminished by studying courtship and copulatory neuromuscular circuits in separate vertebrate groups.…”