Sex differences and endocrine regulation of auditory-evoked, neural responses in African clawed frogs (Xenopus)

Abstract

Mating depends on the accurate detection of signals that convey species identity and reproductive state. In African clawed frogs, Xenopus, this information is conveyed by vocal signals that differ in temporal patterns and spectral features between sexes and across species. We characterized spectral sensitivity using auditory evoked potentials (AEPs), commonly known as the auditory brainstem response, in males and females of four Xenopus species. In female X. amieti, X. petersii, and X. laevis, peripheral auditory sensitivity to their species own dyad- two, species-specific dominant frequencies in the male advertisement call – is enhanced relative to males. Males were most sensitive to lower frequencies including those in the male-directed release calls. Frequency sensitivity was influenced by endocrine state; ovariectomized females had male-like auditory tuning while dihydrotesosterone-treated, ovariectomized females maintained female-like tuning. Thus adult, female Xenopus demonstrate an endocrine-dependent sensitivity to the spectral features of conspecific male advertisement calls that could facilitate mating. Xenopus AEPs resemble those of other species in stimulus and level dependence, and in sensitivity to anesthetic (MS-222). AEPs were correlated with body size and sex within some species. A frequency following response, probably encoded by the amphibian papilla, might facilitate dyad source localization via interaural time differences.

Cold block of in vitro eyeblink reflexes: evidence supporting the use of hypothermia as an anesthetic in pond turtles

“…In one study of vestibulo-ocular reflexes in Xenopus tadpoles anesthetized with MS222 (0.05%) followed by euthanasia and isolation of a semi-intact in vitro preparation, investigators did not record from their preparations until 24 h after the dissection (Ramlochansingh et al, 2014), suggesting that strong depression of brain activity occurs after MS222 treatment. The detrimental effects of MS222 on electrophysiological experiments of anuran auditory evoked potentials have also been recently reported (Hall et al, 2016).…”

The return to water in ancestralXenopuswas accompanied by a novel mechanism for producing and shaping vocal signals

“…6 The peripheral auditory system of females is tuned to their species' own dyad: DF1, DF2 and the DF2/DF1 ratio. 34 These features of vocal production and perception should reinforce the divergence of populations during speciation by limiting gene flow. Xenopus evolution however has also been shaped by multiple rounds of interspecific hybridization resulting in genomic introgression and the numerous highly polyploid species of the phylogeny, particularly A clade species.…”

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

“…Axons from the ganglion extend centrally to enter the hindbrain and terminate in the dorsal medullary nucleus. Although both males and females are most acoustically sensitive to the dominant fre- quencies of the male advertisement call, across Xenopus species, peripheral (auditory ganglion) sensitivity is greater in females than in males (Hall et al, 2016). In X. laevis, this sex difference was abolished by ovariectomy and reinstated by androgen, the major circulating gonadal steroid in females (Lutz et al, 2001), indicating endocrine regulation of peripheral auditory sensitivity in females, perhaps because of androgen receptor expression in auditory ganglion neurons (Pérez et al, 1996).…”

“…Other hormones also influence communication pathways. Gonadotropins in males, for example, act on the testis to promote androgen synthesis and secretion, and also act on neurons directly via gonadotropin receptor expression in the central nucleus of the amygdala (CeA, formerly ventral striatum; Hall et al, 2016) to stimulate advertisement calling (Yang et al, 2007). Sex differences in the vocal system remain at least partially plastic into adulthood.…”

“…(Tobias et al, 2011(Tobias et al, , 2014. Examples of species differences are the divergence of membrane oscillations in fast trill neurons from X. laevis and X. petersii described by Barkan et al (2018) and the greater auditory sensitivity of female Xenopus to dyads composed of their own species-specific frequencies at group-specific ratios (Hall et al, 2016). Species differences should be reflected in the neural circuitry, from the auditory periphery to the larynx, and be expressed by both the signaler and the responder.…”