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

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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 dihydrotestosterone-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 (MS222). 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.

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Abbreviations

ABR:

Auditory brainstem response

AEP:

Auditory-evoked potential

ANOVA:

Analysis of variance

DF:

Dominant frequency

DHT:

Dihydrotestosterone

F1:

Frequency 1

F2:

Frequency 2

FFR:

Frequency following response

MS222:

Tricane methanesulfonate

N1:

First negative AEP peak

OVX:

Ovariectomized

OVX + DHT:

Ovariectomized and given DHT

P1:

First positive AEP peak

P2:

Second positive AEP peak

SOD:

Species own dyad

TDT:

Tucker Davis Technologies

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Acknowledgments

This research involved animals that were cared for and treated in accordance with Columbia University’s IACUC requirements. The authors declare that they have no conflict of interest. Charles H. Revson Foundation (ICH), National Institutes of Health GM103266 (ICH), National Institutes of Health NS28634 (DBK), National Institutes of Health DC009810 (SMNW). Jakob Christensen-Daalsgard, Catherine Carr, Caitlin Baxter, Hilary Bierman (AEP suggestions and training); Martha Tobias (collection and analysis of call features); David Schneider (MATLAB code).

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Authors and Affiliations

  1. Department of Biological Sciences, Columbia University, Fairchild Building, MC 2432, New York, NY, 10027, USA

    Ian C. Hall, Ursula Kwong-Brown & Darcy B. Kelley

  2. Department of Psychology, Columbia University, Schermerhorn Hall, MC 5501, New York, NY, 10027, USA

    Sarah M. N. Woolley

  3. Department of Biology, St. Mary’s College of Maryland, Schaeffer Hall 258, St. Mary’s City, MD, 20686, USA

    Ian C. Hall

  4. Center for New Music and Audio Technologies, University of California, Berkeley, CA, 94720, USA

    Ursula Kwong-Brown

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  1. Ian C. Hall
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  2. Sarah M. N. Woolley
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  3. Ursula Kwong-Brown
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  4. Darcy B. Kelley
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Correspondence to Ian C. Hall.

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Hall, I.C., Woolley, S.M.N., Kwong-Brown, U. et al. Sex differences and endocrine regulation of auditory-evoked, neural responses in African clawed frogs (Xenopus). J Comp Physiol A 202, 17–34 (2016). https://doi.org/10.1007/s00359-015-1049-9

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  • DOI: https://doi.org/10.1007/s00359-015-1049-9

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