Abstract
In many vertebrates, the production and reception of species-typical courtship signals occurs when gonadotropin and gonadal hormone levels are elevated. These hormones may modify sensory processing in the signal receiver in a way that enhances behavioral responses to the signal. We examined this possibility in female túngara frogs (Physalaemus pustulosus) by treating them with either gonadotropin (which elevated estradiol) or saline and exposing them to either mate choruses or silence. Expression of an activity-dependent gene, egr-1, was quantified within two sub-nuclei of the auditory midbrain to investigate whether gonadotropin plus chorus exposure induced greater egr-1 induction than either of these stimuli alone. The laminar nucleus (LN), a sub-nucleus of the torus semicircularis that contains steroid receptors, exhibited elevated egr-1 induction in response to chorus exposure and gonadotropin treatment. Further analysis revealed that neither chorus exposure nor gonadotropin treatment alone elevated egr-1 expression in comparison to baseline levels whereas gonadotropin + chorus exposure did. This suggests that mate signals and hormones together produce an additive effect so that together they induce more egr-1 expression than either alone. Our previously published studies of female túngara frogs reveal that (1) gonadotropin-induced estradiol elevations also increase behavioral responses to male signals, and (2) reception of male signals elevates estradiol levels in the female. Here, we report data that reveal a novel mechanism by which males exploit female sensory processing to increase behavioral responses to their courtship signals.
References
1.
Allison JD (1992) Acoustic modulation of neural activity in the preoptic area and ventral hypothalamus of the green treefrog (Hyla cinerea). J Comp Physiol A 171:387–395.
2.
Ball GF, Castelino CB, Maney DL, Appeltants D, Balthazart J (2003) The activation of birdsong by testosterone: Multiple sites of action and the role of ascending catecholamine projections. Ann NY Acad Sci 1007:211–231.
3.
Bass AH, Zakon HH (2005) Sonic and electric fish: At the crossroads of neuroethology and behavioral neuroendocrinology. Horm Behav 48:360–372.
4.
Burmeister SS, Wilczynski W (2000) Social signals influence hormones independently of calling behavior in the treefrog (Hyla cinerea). Horm Behav 38:201–209.
5.
Burmeister SS, Wilczynski W (2001) Social context influences androgenic effects on calling in the green treefrog (Hyla cinerea). Horm Behav 40:550–558.
6.
Costagliola S, Urizar E, Mendive F, Vassart G (2005) Specificity and promiscuity of gonadotropin receptors. Reproduction 130:275–281.
7.
Chakraborty M, Burmeister S (2006) Estradiol induces female receptivity to conspecific calls in the túngara frog. Soc Int Comp Bio Abst 20.7.
8.
Chu J, Wilczynski W (2001) Social influences on androgen levels in the southern leopard frog, Rana sphenocephala. Gen Comp Endocrinol 121:66–73.
9.
Clayton DF (2000) The genomic action potential. Neurobiol Learn Mem 74:185–216.
10.
di Meglio M, Morrell JI, Pfaff DW (1987) Localization of steroid-concentrating cells in the central nervous system of the frog Rana esculenta. Gen Comp Endocrinol 67:149–154.
11.
Elkind-Hirsch KE, Stoner WR, Stach BA, Jerger JF (1992) Estrogen influences auditory brainstem responses during the normal menstrual cycle. Hear Res 60:143–148.
12.
Endepols H, Walkowiak W (1999) Influence of descending forebrain projections on processing of acoustic signals and audiomotor integration in the anuran midbrain. Eur J Morphol 37:182–184.
13.
Endpols H, Walkowiak W (2001) Integration of ascending and descending inputs in the auditory midbrain of anurans. J Comp Physiol A 186:1119–1133.
14.
Endepols H, Feng S, Gerhardt HC, Schul J, Walkowiak W (2003) Roles of the auditory midbrain and thalamus in selective phonotaxis in female gray treefrogs (Hyla versicolor). Behav Brain Res 145:63–77.
15.
Gentner TQ, Hulse SH, Duffy D, Ball GF (2000) Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. J Neurobiol 46:48–58.
16.
Hinde RA, Steele E (1964) Effect of exogenous hormones on the tactile sensitivity of the canary brood patch. J Endocrinol 30:355–359.
17.
Hoke KL, Burmeister SS, Fernald RD, Rand AS, Ryan MJ, Wilczynski W (2004) Functional mapping of the auditory midbrain during mate call reception. J Neurosci 24:11264–11272.
18.
Hoke KL, Ryan MJ, Wilczynski W (2005) Social cues shift functional connectivity in the hypothalamus. Proc Nat Acad Sci USA 102:10712–10717.
19.
Hoke KL, Ryan MJ, Wilczynski W (2007) Integration of sensory and motor processing underlying social behaviour in túngara frogs. Proc R Soc Lond B 274:641–649.
20.
Kelley DB (1980) Auditory and vocal nuclei in the frog brain concentrate sex hormones. Science 207:553–555.
21.
Kelley DB (1982) Female sex behaviors in the South African clawed frog, Xenopus laevis: Gonadotropin-releasing, gonadotropic and steroid hormones. Horm Behav 16:158–174.
22.
Kelley DB, Lieberburg I, McEwan BS, Pfaff DW (1978) Autoradiographic and biochemical studies of steroid hormone-concentrating cells in the brain of Rana pipiens. Brain Res 140:287–305.
23.
Kelley DB, Morrell JI, Pfaff DW (1975) Autoradiographic localization of hormone concentrating cells in the brain of an amphibian, Xenopus laevis. I. Testosterone. J Comp Neurol 164:47–59.
24.
Komisaruk BR, Adler NT, Hutchinson J (1972) Genital sensory field: enlargement by estrogen treatment in female rats. Science 178:1295–1298.
25.
Leitner S, Voigt C, Metzdorf R, Catchpole CK (2005) Immediate early gene (ZENK, Arc) expression in the auditory forebrain of female canaries varies in response to male song quality. J Neurobiol 64:275–284.
26.
Lynch KS, Wilczynski W (2005) Gonadal steroids vary with reproductive stage in a tropically breeding female Anuran. Gen Comp Endocrinol 143:51–66.
27.
Lynch KS, Wilczynski W (2006) Social regulation of plasma estradiol concentration in a female anuran. Horm Behav 50:101–106.
28.
Lynch KS, Crews DC, Ryan MJ, Wilczynski W (2006) Hormonal state influences aspects of female mate choice in the túngara frog (Physalaemus pustulosus) Horm Behav 49:450–457.
29.
Maney DL, Cho E, Goode CT (2006) Estrogen-dependent selectivity of genomic responses to birdsong. Eur J Neurosci 23:1523–1529.
30.
Maney DL, MacDougall-Shackelton EA, MacDougall-Shackelton SA, Ball GF, Hahn TP (2003) Immediate early gene response to hearing song correlates with receptive behavior and depends on dialect in a female songbird. J Comp Physiol A 189:667–674.
31.
Marler CA, Ryan MJ (1996) Energetic constraints and steroid hormone correlates of male calling behaviour in the túngara frog. J Zool 240:397–409.
32.
Mello CV, Velho TAF, Pinaud R (2004) Song-induced gene expression: A window on song auditory processing and perception. Ann NY Acad Sci 1016:263–281.
33.
Morrell JI, Kelley DB, Pfaff DW (1975) Autoradiographic localization of hormone-concentrating cells in the brain of an amphibian, Xenopus laevis. II. Estradiol. J Comp Neurol 164:63–77.
34.
Penna M, Capranica RR, Somers J (1992) Hormone-induced vocal behavior and midbrain auditory sensitivity in the green treefrog, Hyla cinerea. J Comp Physiol A 170:73–82.
35.
Potter HD (1965) Mesencephalic auditory regions of the bullfrog. J Neurophysiol 28:1132–1154.
36.
Rose JD, Moore FL (2002) Behavioral neuroendorinology of vasotocin and vasopressin and the sensorimotor processing hypothesis. Front Neuroendocrinol 23:317–341.
37.
Ryan MJ (1980) Female mate choice in a neotropical frog. Science 209:523–525.
38.
Ryan MJ, Rand AS (1998) Evoked vocal response in male túngara frogs: Preexisting biases in male responses? Anim Behav 56:1509–1516.
39.
Schmidt RS (1984) Mating call phonotaxis in the female American toad: Induction by hormones. Gen Comp Endocrinol 55:150–156.
40.
Schmidt RS (1985) Prostaglandin-induced mating call phonotaxis in female American toad: facilitation by progesterone and arginine vasotocin. J Comp Physiol A 156:823–829.
41.
Searcy WA (1992) Measuring responses of female birds to male songs. In: Playback Studies of Animal Communication (McGregor PK, ed), pp 175–182. New York: Plenum Press.
42.
Sisneros JA, Forlano PM, Deitcher DL, Bass AH (2004) Steroid-dependent auditory plasticity leads to adaptive coupling of sender and receiver. Science 305:404–407.
43.
Sockman KW, Gentner TQ, Ball GF (2002) Recent experience modulates forebrain gene-expression in response to mate-choice cues in European starlings. Proc R Soc Lond B 269:2479–2485.
44.
Thompson RR, Moore FL (2000) Vasotocin stimulates appetitive responses to the visual and phermonal stimuli used by male roughskin newts during courtship. Horm Behav 38:75–85.
45.
Thompson RR, Moore FL (2003) The effects of sex steroids and vasotocin on behavioral responses to visual and olfactory sexual stimuli in ovariectomized female roughskin newts. Horm Behav 44:311–318.
46.
Walpurger V, Pietrowsky R, Kirshbaum C, Wolf O (2004) Effects of menstrual cycle on auditory event-related potential. Horm Behav 46:600–606.
47.
Wells KD (1977) The social behaviour of anuran amphibians. Anim Behav 25:666–693.
48.
Wilczynski W (1988) Brainstem auditory pathways in anuran amphibians. In: The Evolution of the Amphibian Auditory System (Fritzsch B, Ryan MJ, Wilczynski W, Hetherington TE, Walkowiak W, eds), pp 209–231. New York: Wiley.
49.
Wilczynski W, Allison JD (1989) Acoustic modulation of neural activity in the hypothalamus of the leopard frog. Brain Behav Evol 33:317–324.
50.
Wilczynski W, Endepols H (2007) Central auditory pathways in anuran amphibians: The anatomical basis of hearing and sound communication. In: Hearing and Sound Communication in Amphibians: Springer Handbook of Auditory Research, vol. 28 (Popper AN, Feng AS, Narins PN, eds). Berlin: Springer-Verlag.
51.
Wilczynski W, Allison JD, Marler CA (1993) Sensory pathways linking social and environmental cues to endocrine control regions of amphibian forebrains. Brain Behav Evol 42:252–264.
52.
Wilczynski W, Lynch KS, O’Bryant EL (2005) Current research in amphibians: Studies integrating endocrinology, behavior, and neurobiology. Horm Behav 48:440–450.
53.
Wright P, Crow RA (1973) Menstrual cycle: effect on sweetness preferences in women. Horm Behav 4:387–391.
54.
Yang EJ, Nasipak BT, Kelley DB (2007) Direct action of gonadotropin in brain integrates behavioral and reproductive functions. Proc Nat Acad Sci USA 104:2477–2482.
55.
Zakon HH, Smith GT (2002) Weakly electric fish: Behavior, neurobiology and neuroendocrinology. In: Hormones, Brain and Behavior vol. 3 (Pfaff AP, Arnold AM, Etgen SE, Fahrbach RT, Rubin DW, eds), pp 349–375. London: Academic Press, Elsevier Science.
56.
Zar JH (1996) Biostatisical Analysis, 3rd edition. Upper Saddle River, NJ: Prentice Hall.
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