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Effects of Steroid Hormones on Hearing and Communication in Frogs

Part of the Springer Handbook of Auditory Research book series (SHAR,volume 57)

Abstract

The auditory system of frogs and toads differs between sexes, seasons, and reproductive state in a way that suggests a strong influence of reproductive steroid hormones on hearing. Although few studies have measured auditory response properties after manipulating testosterone or estrogen, those that have done so have shown that sex steroid hormones increase the sensitivity and response strength of the auditory system in adult anurans in a way that enhances the ability of the auditory system to detect and respond to the vocal signals that guide reproductive social behavior in these vertebrates. For males, this could translate into increased calling as they compete with other males, and, for females, into a change in their detection and assessment of male advertisement calls as they search for mates. Furthermore, hearing conspecific calls increases circulating sex steroid hormones in both males and females, suggesting that the acoustic context found during a frog’s breeding season could modify the properties of its auditory system through hormonal modulation. As a result of the reciprocal interaction of hearing and hormones, the auditory system of anurans is not fixed but varies in its sensitivity, response strength, and potentially in more complex aspects of auditory coding, as the levels of testosterone and estrogen change with season, reproductive state, and the acoustic influence of other calling frogs.

Keywords

  • Acoustic communication
  • Amphibians
  • Auditory system
  • Ear
  • Endocrinology
  • Estrogen
  • Gonadal steroids
  • Midbrain
  • Reproduction
  • Sex differences
  • Social behavior
  • Steroid receptors
  • Testosterone

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References

  • Aitken, P. G., & Capranica, R. R. (1984). Auditory input to a vocal nucleus in the frog Rana pipiens: Hormonal and seasonal effects. Experimental Brain Research, 57(1), 33–39. doi:10.1007/BF00231129.

    CAS  CrossRef  PubMed  Google Scholar 

  • Arch, V. S., & Narins, P. M. (2009). Sexual hearing: The influence of sex hormones on acoustic communication in frogs. Hearing Research, 252(1–2), 15–20. doi:10.1016/j.heares.2009.01.001.

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Bernal, X. E., Rand, A. S., & Ryan, M. J. (2007). Sex differences in response to nonconspecific advertisement calls: Receiver permissiveness in male and female túngara frogs. Animal Behaviour, 73(6), 955–964. doi:10.1016/j.anbehav.2006.10.018.

    CrossRef  Google Scholar 

  • Björnström, L., & Sjöberg, M. (2005). Mechanisms of estrogen receptor signaling: Convergence of genomic and nongenomic actions on target genes. Molecular Endocrinology, 19(4), 833–842. doi:10.1210/me.2004-0486.

    CrossRef  PubMed  Google Scholar 

  • Bosch, J., & Boyero, L. (2004). Reproductive stage and phonotactic preferences of female midwife toads (Alytes cisternasii). Behavioral Ecology and Sociobiology, 55(3), 251–256. doi:10.1007/s00265-003-0699-8.

    CrossRef  Google Scholar 

  • Buerkle, N. P., Schrode, K. M., & Bee, M. A. (2014). Assessing stimulus and subject influences on auditory evoked potentials and their relation to peripheral physiology in green treefrogs (Hyla cinerea). Comparative Biochemistry and Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 178, 68–81.

    CAS  CrossRef  Google Scholar 

  • Burmeister, S., & Wilczynski, W. (2000). Social signals influence hormones independently of calling behavior in the treefrog (Hyla cinerea). Hormones and Behavior, 38(4), 201–209. doi:10.1006/hbeh.2000.1605.

    CAS  CrossRef  PubMed  Google Scholar 

  • Burmeister, S. S., & Wilczynski, W. (2005). Social signals regulate gonadotropin-releasing hormone neurons in the green treefrog. Brain, Behavior and Evolution, 65(1), 26–32. doi:10.1159/000081108.

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Capranica, R. R., & Moffat, A. J. M. (1983). Neurobehavioral correlates of sound communication in anurans. In J. P. Ewert & R. R. Capranica (Eds.), Advances in vertebrate neuroethology (pp. 701–730). New York: Plenum Press.

    CrossRef  Google Scholar 

  • Caras, M. L. (2013). Estrogenic modulation of auditory processing: A vertebrate comparison. Frontiers in Neuroendocrinology, 34(4), 285–299. doi:10.1016/j.yfrne.2013.07.006.

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Chakraborty, M., & Burmeister, S. S. (2009). Estradiol induces sexual behavior in female túngara frogs. Hormones and Behavior, 55(1), 106–112. doi:10.1016/j.yhbeh.2008.09.001.

    CAS  CrossRef  PubMed  Google Scholar 

  • Chakraborty, M., & Burmeister, S. S. (2010). Sexually dimorphic androgen and estrogen receptor mRNA expression in the brain of túngara frogs. Hormones and Behavior, 58(4), 619–627. doi:10.1016/j.yhbeh.2010.06.013.

    CAS  CrossRef  PubMed  Google Scholar 

  • Chakraborty, M., & Burmeister, S. S. (2015). Effects of estradiol on neural responses to social signals in female túngara frogs. Journal of Experimental Biology, 218, 3671–3677.

    CrossRef  PubMed  Google Scholar 

  • Corey, D., & Hudspeth, A. (1983). Kinetics of the receptor current in bullfrog saccular hair cells. Journal of Neuroscience, 3(5), 962–976.

    CAS  PubMed  Google Scholar 

  • Davis, A. G., & Leary, C. J. (2015). Elevated stress hormone diminishes the strength of female preferences for acoustic signals in the green treefrog. Hormones and Behavior, 69, 119–122. doi:10.1016/j.yhbeh.2015.01.005.

    CAS  CrossRef  PubMed  Google Scholar 

  • Elliott, T. M., Christensen-Dalsgaard, J., & Kelley, D. B. (2011). Temporally selective processing of communication signals by auditory midbrain neurons. Journal of Neurophysiology, 105(4), 1620–1632. doi:10.1152/jn.00261.2009.

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Endepols, H., & Walkowiak, W. (2001). Integration of ascending and descending inputs in the auditory midbrain of anurans. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 186(12), 1119–1133. doi:10.1007/s003590000159.

    CAS  CrossRef  Google Scholar 

  • Feng, A. S., Narins, P. M., & Capranica, R. R. (1975). Three populations of primary auditory fibers in the bullfrog (Rana catesbeiana): Their peripheral origins and frequency sensitivities. Journal of Comparative Physiology, 100(3), 221–229. doi:10.1007/BF00614532.

    CrossRef  Google Scholar 

  • Gall, M. D., & Wilczynski, W. (2014). Prior experience with conspecific signals enhances auditory midbrain responsiveness to conspecific vocalizations. Journal of Experimental Biology, 217(11), 1977–1982.

    CrossRef  PubMed  Google Scholar 

  • Gall, M. D., & Wilczynski, W. (2015). Hearing conspecific vocal signals alters peripheral auditory sensitivity. Proceedings of the Royal Society of London B: Biological Sciences, 282(1808). doi:10.1098/rspb.2015.0749.

    Google Scholar 

  • Gall, M. D., Salameh, T. S., & Lucas, J. R. (2013). Songbird frequency selectivity and temporal resolution vary with sex and season. Proceedings of the Royal Society of London B: Biological Sciences, 280(1751), 20122296. doi:10.1098/rspb.2012.2296.

    CrossRef  Google Scholar 

  • Gerhardt, H. C. (1974). The significance of some spectral features in mating call recognition in the green treefrog (Hyla cinerea). Journal of Experimental Biology, 61, 229–241.

    CAS  PubMed  Google Scholar 

  • Gerhardt, H. C. (1976). Significance of two frequency bands in long distance vocal communication in the green treefrog. Nature, 261, 692–694.

    CrossRef  Google Scholar 

  • Gerhardt, H. C., & Huber, F. (2002). Acoustic communication in insects and anurans. Chicago: University of Chicago Press.

    Google Scholar 

  • Goense, J. B. M., & Feng, A. S. (2005). Seasonal changes in frequency tuning and temporal processing in single neurons in the frog auditory midbrain. Journal of Neurobiology, 65, 22–36.

    CrossRef  PubMed  Google Scholar 

  • Gordon, N. M., & Gerhardt, H. C. (2009). Hormonal modulation of phonotaxis and advertisement-call preferences in the gray treefrog (Hyla versicolor). Hormones and Behavior, 55(1), 121–127. doi:10.1016/j.yhbeh.2008.09.007.

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Hetherington, T. E. (1994). Sexual differences in the tympanic frequency responses of the American bullfrog (Rana catesbeiana). The Journal of the Acoustical Society of America, 96(2), 1186–1188. doi:10.1121/1.410326.

    CAS  CrossRef  PubMed  Google Scholar 

  • Hillary, C. M. (1984). Seasonality of two midbrain auditory responses in the treefrog, Hyla chrysoscelis. Copeia, 1984(4), 844–852.

    CrossRef  Google Scholar 

  • Höglund, J., & Alatalo, R. V. (1995). Leks. Princeton: Princeton University Press.

    Google Scholar 

  • Hoke, K. L., & Pitts, N. L. (2012). Modulation of sensory–motor integration as a general mechanism for context dependence of behavior. General and Comparative Endocrinology, 176(3), 465–471. doi:10.1016/j.ygcen.2012.02.014.

    CAS  CrossRef  PubMed  Google Scholar 

  • Hoke, K. L., Ryan, M. J., & Wilczynski, W. (2008). Candidate neural locus for sex differences in reproductive decisions. Biology Letters, 4(5), 518–521. doi:10.1098/rsbl.2008.0192.

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Hudspeth, A. J., & Lewis, R. S. (1988). A model for electrical resonance and frequency tuning in saccular hair cells of the bull-frog, Rana catesbeiana. Journal of Physiology, 400(1), 275–297. doi:10.1113/jphysiol.1988.sp017120.

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Kelley, D. B. (1980). Auditory and vocal nuclei in the frog brain concentrate sex hormones. Science, 207(4430), 553–555.

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Kelley, D. B., Lieberburg, I., McEwen, B. S., & Pfaff, D. W. (1978). Autoradiographic and biochemical studies of steroid hormone-concentrating cells in the brain of Rana pipiens. Brain Research, 140(2), 287–305. doi:10.1016/0006-8993(78)90461-4.

    CAS  CrossRef  PubMed  Google Scholar 

  • Lea, J., Halliday, T., & Dyson, M. (2000). Reproductive stage and history affect the phonotactic preferences of female midwife toads, Alytes muletensis. Animal Behaviour, 60(4), 423–427. doi:10.1006/anbe.2000.1482.

    CrossRef  PubMed  Google Scholar 

  • Leary, C. J. (2009). Hormones and acoustic communication in anuran amphibians. Integrative and Comparative Biology, 49(4), 452–470.

    CAS  CrossRef  PubMed  Google Scholar 

  • Leary, C. J., Edwards, C. J., & Rose, G. J. (2008). Midbrain auditory neurons integrate excitation and inhibition to generate duration selectivity: An in vivo whole-cell patch study in anurans. Journal of Neuroscience, 28(21), 5481–5493.

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Lewis, E. R., & Lombard, R. E. (1988). The amphibian inner ear. In B. Fritzsch, W. Walkowiak, M. J. Ryan, W. Wilczynski, & T. Heatherington (Eds.), The evolution of the amphibian auditory system (pp. 93–123). New York: Wiley.

    Google Scholar 

  • Liu, W.-R., Shen, J.-X., Zhang, Y.-J., Xu, Z.-M., Qi, Z., & Xue, M.-Q. (2014). Auditory sexual difference in the large odorous frog Odorrana graminea. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 200(4), 311–316. doi:10.1007/s00359-014-0885-3.

    CAS  CrossRef  PubMed  Google Scholar 

  • Lutterschmidt, D. I., & Wilczynski, W. (2012). Sexually dimorphic effects of melatonin on brain arginine vasotocin immunoreactivity in green treefrogs (Hyla cinerea). Brain, Behavior and Evolution, 80(3), 222–232. doi:10.1159/000341238000341238.

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Lynch, K. S., & Wilczynski, W. (2005). Gonadal steroids vary with reproductive stage in a tropically breeding female anuran. General and Comparative Endocrinology, 143(1), 51–56. doi:10.1016/j.ygcen.2005.02.023.

    CAS  CrossRef  PubMed  Google Scholar 

  • Lynch, K. S., & Wilczynski, W. (2006). Social regulation of plasma estradiol concentration in a female anuran. Hormones and Behavior, 50(1), 101–106. doi:10.1016/j.yhbeh.2006.01.010.

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Lynch, K. S., & Wilczynski, W. (2008). Reproductive hormones modify reception of species-typical communication signals in a female anuran. Brain, Behavior and Evolution, 71(2), 143–150. doi:10.1159/000111460.

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Lynch, K. S., Crews, D., Ryan, M. J., & Wilczynski, W. (2006). Hormonal state influences aspects of female mate choice in the túngara frog (Physalaemus pustulosus). Hormones and Behavior, 49(4), 450–457. doi:10.1016/j.yhbeh.2005.10.001.

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Mangiamele, L. A., & Burmeister, S. S. (2011). Auditory selectivity for acoustic features that confer species recognition in the túngara frog. Journal of Experimental Biology, 214(17), 2911–2918.

    CrossRef  PubMed  Google Scholar 

  • Mason, M. J., Lin, C. C., & Narins, P. M. (2003). Sex differences in the middle ear of the bullfrog (Rana catesbeiana). Brain, Behavior and Evolution, 61(2), 91–101.

    CAS  CrossRef  PubMed  Google Scholar 

  • McClelland, B. E., Wilczynski, W., & Rand, A. S. (1997). Sexual dimorphism and species differences in the neurophysiology and morphology of the acoustic communication system of two neotropical hylids. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 180(5), 451–462.

    CAS  CrossRef  Google Scholar 

  • Miranda, J. A., & Wilczynski, W. (2009a). Sex differences and androgen influences on midbrain auditory thresholds in the green treefrog, Hyla cinerea. Hearing Research, 252(1–2), 79–88. doi:10.1016/j.heares.2009.04.004.

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Miranda, J. A., & Wilczynski, W. (2009b). Female reproductive state influences the auditory midbrain response. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 195(4), 341–349. doi:10.1007/s00359-008-0410-7.

    CrossRef  PubMed  Google Scholar 

  • Narins, P. M. (2001). Ectothermy’s last stand: Hearing in the heat and cold. In M. J. Ryan (Ed.), Anuran communication (pp. 61–70). Washington, DC: Smithsonian Institution Press.

    Google Scholar 

  • Narins, P. M., & Capranica, R. R. (1976). Sexual difference in the auditory system of the treefrog Eleutherodactylus coqui. Science, 192, 378–380.

    CAS  CrossRef  PubMed  Google Scholar 

  • O’Connell, L. A., Ding, J. H., Ryan, M. J., & Hofmann, H. A. (2011). Neural distribution of the nuclear progesterone receptor in the túngara frog, Physalaemus pustulosus. Journal of Chemical Neuroanatomy, 41(3), 137–147. doi:10.1016/j.jchemneu.2011.01.002.

    CrossRef  PubMed  Google Scholar 

  • Penna, M., Capranica, R. R., & Somers, J. (1992). Hormone-induced vocal behavior and midbrain auditory sensitivity in the green treefrog, Hyla cinerea. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 170(1), 73–82. doi:10.1007/BF00190402.

    CAS  CrossRef  Google Scholar 

  • Ponnath, A., & Farris, H. E. (2014). Sound-by-sound thalamic stimulation modulates midbrain auditory excitability and relative binaural sensitivity in frogs. Frontiers in Neural Circuits, 8, 85. doi:10.3389/fncir.2014.00085.

  • Roberts, W., Jacobs, R., & Hudspeth, A. (1990). Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. Journal of Neuroscience, 10(11), 3664–3684.

    CAS  PubMed  Google Scholar 

  • Ryan, M. J., & Rand, A. S. (1995). Female responses to ancestral advertisement calls in the túngara frog. Science 269, 390–392.

    Google Scholar 

  • Schrode, K., Buerkle, N., Brittan-Powell, E., & Bee, M. (2014). Auditory brainstem responses in Cope’s gray treefrog (Hyla chrysoscelis): Effects of frequency, level, sex and size. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 200(3), 221–238. doi:10.1007/s00359-014-0880-8.

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Shen, J.-X., Xu, Z.-M., Yu, Z.-L., Wang, S., Zheng, D.-Z., & Fan, S.-C. (2011). Ultrasonic frogs show extraordinary sex differences in auditory frequency sensitivity. Nature Communications, 2, 342. http://www.nature.com/ncomms/journal/v2/n6/suppinfo/ncomms1339_S1.html.

    CrossRef  PubMed  Google Scholar 

  • Simmons, A. (2013). “To ear is human, to forgive is divine”: Bob Capranica’s legacy to auditory neuroethology. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 199(3), 169–182. doi:10.1007/s00359-012-0786-2.

    CrossRef  PubMed  Google Scholar 

  • Simmons, D. D., Meenderink, S. W. F., & Vassilakis, P. N. (2007). Anatomy, physiology, and function of the auditory end-organs in the frog inner ear. In P. M. Narins, A. S. Feng, R. R. Fay, & A. N. Popper (Eds.), Hearing and sound communication in amphibians (pp. 184–220). New York: Springer.

    Google Scholar 

  • Smotherman, M. S., & Narins, P. M. (2000). Hair cells, hearing and hopping: A field guide to hair cell physiology in the frog. Journal of Experimental Biology, 203(15), 2237–2246.

    CAS  PubMed  Google Scholar 

  • Walkowiak, W. (1980). The coding of auditory signals in the torus semicircularis of the fire-bellied toad and the grass frog: Responses to simple stimuli and to conspecific calls. Journal of Comparative Physiology, 138(2), 131–148. doi:10.1007/BF00680437.

    CrossRef  Google Scholar 

  • Wells, K. D. (1977). The social behaviour of anuran amphibians. Animal Behaviour, 25, 666–693.

    CrossRef  Google Scholar 

  • Wells, K. D. (2007). The ecology and behavior of amphibians. Chicago: University of Chicago Press.

    CrossRef  Google Scholar 

  • Wilczynski, W. (1986). Sexual differences in neural tuning and their effect on active space. Brain, Behavior and Evolution, 28(1-3), 83–94.

    CAS  CrossRef  PubMed  Google Scholar 

  • Wilczynski, W., & Capranica, R. R. (1984). The auditory system of anuran amphibians. Progress in Neurobiology, 22(1), 1–38.

    CAS  CrossRef  PubMed  Google Scholar 

  • Wilczynski, W., & Endepols, H. (2007). Central auditory pathways in anuran amphibians: The anatomical basis of hearing and sound communication. In P. M. Narins, A. S. Feng, R. R. Fay, & A. N. Popper (Eds.), Hearing and sound communication in amphibians (pp. 221–249). New York: Springer.

    Google Scholar 

  • Wilczynski, W., & Ryan, M. J. (2010). The behavioral neuroscience of anuran social signal processing. Current Opinion in Neurobiology, 20(6), 754–763. doi:10.1016/j.conb.2010.08.021.

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Wilczynski, W., Keddy-Hector, A. C., & Ryan, M. J. (1992). Call patterns and basilar papilla tuning in cricket frogs. I. Differences among populations and between sexes. Brain, Behavior and Evolution, 39(4), 229–237.

    CAS  CrossRef  PubMed  Google Scholar 

  • Wilczynski, W., Lynch, K. S., & O’Bryant, E. L. (2005). Current research in amphibians: Studies integrating endocrinology, behavior, and neurobiology. Hormones and Behavior, 48(4), 440–450. doi:10.1016/j.yhbeh.2005.06.001.

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Yang, E.-J., Nasipak, B. T., & Kelley, D. B. (2007). Direct action of gonadotropin in brain integrates behavioral and reproductive functions. Proceedings of the National Academy of Sciences of the USA, 104(7), 2477–2482.

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Yovanof, S., & Feng, A. S. (1983). Effects of estradiol on auditory evoked responses from the frog’s auditory midbrain. Neuroscience Letters, 36, 291–297.

    CAS  CrossRef  PubMed  Google Scholar 

  • Zakon, H., & Wilczynski, W. (1988). The physiology of the anuran eighth nerve. In B. Fritzsch, W. Walkowiak, M. J. Ryan, W. Wilczynski, & T. Heatherington (Eds.), The evolution of the amphibian auditory system (pp. 125–155). New York: Wiley.

    Google Scholar 

  • Zhang, D., Cui, J., & Tang, Y. (2012). Plasticity of peripheral auditory frequency sensitivity in Emei music frog. PLoS ONE, 7(9), e45792. doi:10.1371/journal.pone.0045792.

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Zornik, E., & Kelley, D. B. (2011). A neuroendocrine basis for the hierarchical control of frog courtship vocalizations. Frontiers in Neuroendocrinology, 32(3), 353–366. doi:10.1016/j.yfrne.2010.12.006.

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

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Wilczynski, W., Burmeister, S.S. (2016). Effects of Steroid Hormones on Hearing and Communication in Frogs. In: Bass, A., Sisneros, J., Popper, A., Fay, R. (eds) Hearing and Hormones. Springer Handbook of Auditory Research, vol 57. Springer, Cham. https://doi.org/10.1007/978-3-319-26597-1_3

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