Facilitation at the sexually differentiated laryngeal synapse of Xenopus laevis

Ruel, T. D.; Kelley, Darcy B.; Tobias, Martha L.

doi:10.1007/s003590050155

Cited by 14 publications

(10 citation statements)

References 16 publications

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“…Rapid, intensity-modulated calls require an entirely fast-twitch complement of muscle fibers, and a weak and facilitating neuromuscular synapse responsible for EMG potentiation (Ruel et al, 1998;Tobias et al, 1998). Given the widespread rapidity and intensity modulation of male advertisement calls in Xenopus and Silurana (Tobias et al, 2011), an entirely fast-twitch complement of laryngeal muscle fibers and a facilitating synapse may also represent the male ancestral state.…”

Section: Borealis Has Lost Certain Male-specific Laryngeal Charactersmentioning

confidence: 99%

Species-specific loss of sexual dimorphism in vocal effectors accompanies vocal simplification in African clawed frogs (Xenopus)

Leininger

Kitayama

Kelley

2015

Journal of Experimental Biology

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Phylogenetic studies can reveal patterns of evolutionary change, including the gain or loss of elaborate courtship traits in males. Male African clawed frogs generally produce complex and rapid courtship vocalizations, whereas female calls are simple and slow. In a few species, however, male vocalizations are also simple and slow, suggesting loss of male-typical traits. Here, we explore features of the male vocal organ that could contribute to loss in two species with simple, slow male calls. In Xenopus boumbaensis, laryngeal morphology is more robust in males than in females. Larynges are larger, have a more complex cartilaginous morphology and contain more muscle fibers. Laryngeal muscle fibers are exclusively fasttwitch in males but are both fast-and slow-twitch in females. The laryngeal electromyogram, a measure of neuromuscular synaptic strength, shows greater potentiation in males than in females. Malespecific physiological features are shared with X. laevis, as well as with a species of the sister clade, Silurana tropicalis, and thus are likely ancestral. In X. borealis, certain aspects of laryngeal morphology and physiology are sexually monomorphic rather than dimorphic. In both sexes, laryngeal muscle fibers are of mixed-twitch type, which limits the production of muscle contractions at rapid intervals. Muscle activity potentiation and discrete tension transients resemble female rather than male X. boumbaensis. The demasculinization of these laryngeal features suggests an alteration in sensitivity to the gonadal hormones that are known to control the sexual differentiation of the larynx in other Xenopus and Silurana species.

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Section: Borealis Has Lost Certain Male-specific Laryngeal Charactersmentioning

confidence: 99%

Species-specific loss of sexual dimorphism in vocal effectors accompanies vocal simplification in African clawed frogs (Xenopus)

Leininger

Kitayama

Kelley

2015

Journal of Experimental Biology

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“…Moreover, laryngeal neuromuscular synapses in females are mostly strong, whereas most synapses in males are weak and require facilitation to produce muscle action potentials Kelley, 1987, 1988). Facilitation parallels amplitude modulation of click trains in isolated male larynges (Ruel et al, 1998).…”

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confidence: 92%

Generating Sexually Differentiated Vocal Patterns: Laryngeal Nerve and EMG Recordings from Vocalizing Male and Female African Clawed Frogs (Xenopus laevis)

Yamaguchi

Kelley

2000

J. Neurosci.

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Male and female African clawed frogs (Xenopus laevis) produce sexually dimorphic vocalizations; for males these include advertisement, amplectant, and growling calls, whereas female calls include ticking. Previous studies have shown that the vocal organ, the larynx, of the sexes differs in physiological properties that parallel vocal differences. However, it was not clear whether these characteristics are sufficient to explain sex differences in vocal behavior. To examine the contribution of the CNS to generating vocal patterns, we developed a preparation in which both laryngeal nerve activity and electromyograms can be recorded from awake, vocalizing frogs. Recordings reveal that the CNS of the two sexes produces patterned activity that closely matches each vocalization whereas the larynx faithfully translates nerve activity into sound. Thus, the CNS is the source of sexually differentiated vocalizations in Xenopus laevis. Furthermore, detailed analyses of compound action potentials recorded from the nerve lead us to hypothesize that neuronal activity underlying different male call types is distinct; some calls are likely to be generated by synchronous firing of motoneuron populations of either constant size or progressively larger sizes, whereas others are generated by asynchronous activity of motoneurons, a pattern shared with vocal production in females. We suggest that these distinct neuronal activity patterns in males may be subserved by two populations of motor units in males that can be distinguished by the strength of the neuromuscular synapse.

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“…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]. At the CNS level, these differences are responsible for generating sexually dimorphic vocalizations, which are recorded in motor neurons [35].…”

Section: Discussionmentioning

confidence: 99%

Impact of Early Postnatal Androgen Exposure on Voice Development

Grisa

Leonel²,

Gonçalves

et al. 2012

PLoS ONE

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BackgroundThe impact of early postnatal androgen exposure on female laryngeal tissue may depend on certain characteristics of this exposure. We assessed the impact of the dose, duration, and timing of early androgen exposure on the vocal development of female subjects who had been treated for adrenocortical tumor (ACT) in childhood.MethodsThe long-term effects of androgen exposure on the fundamental vocal frequency (F0), vocal pitch, and final height and the presence of virilizing signs were examined in 9 adult (age, 18.4 to 33.5 years) and 10 adolescent (13.6 to 17.8 years) female ACT patients. We also compared the current values with values obtained 0.9 years to 7.4 years after these subjects had undergone ACT surgery, a period during which they had shown normal androgen levels.ResultsOf the 19 subjects, 17 (89%) had been diagnosed with ACT before 4 years of age, 1 (5%) at 8.16 years, and 1 (5%) at 10.75 years. Androgen exposure (2 to 30 months) was sufficiently strong to cause pubic hair growth in all subjects and clitoromegaly in 74% (14/19) of the subjects, but did not reduce their height from the target value. Although androgen exposure induced a remarkable reduction in F0 (132 Hz) and moderate pitch virilization in 1 subject and partial F0 virilization, resulting in F0 of 165 and 169 Hz, in 2 subjects, the majority had normal F0 ranging from 189 to 245 Hz.ConclusionsFemale laryngeal tissue is less sensitive to androgen exposure between birth and adrenarche than during other periods. Differential larynx sensitivity to androgen exposure in childhood and F0 irreversibility in adulthood are age-, concentration-, duration-, and timing-dependent events that may also be affected by exposure to inhibitory or stimulatory hormones. Further studies are required to better characterize each of these factors.

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Facilitation at the sexually differentiated laryngeal synapse of Xenopus laevis

Cited by 14 publications

References 16 publications

Species-specific loss of sexual dimorphism in vocal effectors accompanies vocal simplification in African clawed frogs (Xenopus)

Species-specific loss of sexual dimorphism in vocal effectors accompanies vocal simplification in African clawed frogs (Xenopus)

Generating Sexually Differentiated Vocal Patterns: Laryngeal Nerve and EMG Recordings from Vocalizing Male and Female African Clawed Frogs (Xenopus laevis)

Impact of Early Postnatal Androgen Exposure on Voice Development

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