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Current Neuropharmacology

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ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

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Research Article

It is all About the Chase: Neurosteroidogenesis in Male Rats is Driven by Control of Mating Pace

Author(s): Amy S. Kohtz* and Cheryl A. Frye

Volume 21, Issue 7, 2023

Published on: 13 March, 2023

Page: [1606 - 1616] Pages: 11

DOI: 10.2174/1570159X21666221019114535

Price: $65

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Abstract

Background: Masculine sexual behaviors are dependent on androstane-derived steroids; however, the modulatory effects of mating, and of mating control, on androstane neurosteroidogenesis remain largely unknown.

Objective: Herein, we investigated the effects of mating control, prior sexual experience, and age on brain region specific neurosteroidogenic responses in male rats.

Methods: Effects of acute sexual experience were tested in naïve male rats that either remained sexually- naïve, were exposed to a standard mating chamber, or were either given control of the mating pace in a standard mating chamber (male control) or mated wherein the female stimulus rat controlled the mating pace in a paced-mating chamber (female control). Aged (10-12 months) sexually responsive male rats were similarly euthanized from the homecage or engaged in male controlled or female controlled mating. All rats were euthanized immediately following exposure conditions for radioimmunoassay of steroids in midbrain, hypothalamus, hippocampus and cortex.

Results: Consummatory sexual behavior in male vs. female-controlled mating paradigms was altered by age and prior sexual experience. Male-controlled mating increased androstane neurosteroid metabolism, such that complementary increases in the testosterone (T) metabolite 5α-androstane-3α-17β- diol (3α-diol) in the midbrain and hypothalamus of male rats corresponded to decreases in the prohormone, T. 3α-diol were increased in the hippocampus in response to the context alone, and to a lesser degree in response to mating. Mating diminished neurosteroidogenesis in the cortex. Neurosteroidogenesis was overall reduced in aged male rats compared to naïve controls, however, these effects were more prominent in sexually non-responsive aged male rats.

Conclusion: Extending previous findings, these results indicate differential production of androstane neurosteroids in a mating exposure, age and brain region dependent manner.

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[1]
Arnold, A.; Breedlove, S.M. Organizational and activational effects of sex steroids on brain and behavior: A reanalysis. Horm. Behav., 1985, 19(4), 469-498.
[http://dx.doi.org/10.1016/0018-506X(85)90042-X] [PMID: 3910535]
[2]
McCarthy, M.M. How it’s made: organisational effects of hormones on the developing brain. J. Neuroendocrinol., 2010, 22(7), 736-742.
[http://dx.doi.org/10.1111/j.1365-2826.2010.02021.x] [PMID: 20646174]
[3]
Jennings, K.J.; de Lecea, L. Neural and Hormonal Control of Sexual Behavior. Endocrinology, 2020, 161(10), bqaa150.
[http://dx.doi.org/10.1210/endocr/bqaa150] [PMID: 32845294]
[4]
Ward, I.L.; Renz, F.J. Consequences of perinatal hormone manipulation on the adult sexual behavior of female rats. J. Comp. Physiol. Psychol., 1972, 78(3), 349-355.
[http://dx.doi.org/10.1037/h0032375] [PMID: 5016278]
[5]
Whalen, R.E.; Edwards, D.A. Hormonal determinants of the development of masculine and feminine behavior in male and female rats. Anat. Rec., 1967, 157(2), 173-180.
[http://dx.doi.org/10.1002/ar.1091570208] [PMID: 6034297]
[6]
Clemens, L.G.; Gladue, B.A. Feminine sexual behavior in rats enhanced by prenatal inhibition of androgen aromatization. Horm. Behav., 1978, 11(2), 190-201.
[http://dx.doi.org/10.1016/0018-506X(78)90048-X] [PMID: 750349]
[7]
Clemens, L.; Gladue, B.A.; Coniglio, L.P. Prenatal endogenous androgenic influences on masculine sexual behavior and genital morphology in male and female rats*1. Horm. Behav., 1978, 10(1), 40-53.
[http://dx.doi.org/10.1016/0018-506X(78)90023-5] [PMID: 658890]
[8]
Whalen, R.E.; Hardy, D.F. Induction of receptivity in female rats and cats with estrogen and testosterone. Physiol. Behav., 1970, 5(4), 529-533.
[http://dx.doi.org/10.1016/0031-9384(70)90262-3] [PMID: 5535507]
[9]
Pfaff, D. Nature of sex hormone effects on rat sex behavior: Specificity of effects and individual patterns of response. J. Comp. Physiol. Psychol., 1970, 73(3), 349-358.
[http://dx.doi.org/10.1037/h0030242] [PMID: 5514672]
[10]
Pfaff, D.F. Mating behavior of hypophysectomized rats. J. Comp. Physiol. Psychol., 1970, 72(1), 45-50.
[http://dx.doi.org/10.1037/h0029312] [PMID: 5424672]
[11]
Baker, H.W.G.; Burger, H.G.; Kretser, D.M.; Hudson, B.; O’Connor, S.; Wang, C.; Mirovics, A.; Court, J.; Dunlop, M.; Rennie, G.C. Changes in the pituitary-testicular system with age. Clin. Endocrinol. (Oxf.), 1976, 5(4), 349-372.
[http://dx.doi.org/10.1111/j.1365-2265.1976.tb01964.x] [PMID: 971543]
[12]
Vermeulen, A.; Rubens, R.; Verdonck, L. Testosterone secretion and metabolism in male senescence. J. Clin. Endocrinol. Metab., 1972, 34(4), 730-735.
[http://dx.doi.org/10.1210/jcem-34-4-730] [PMID: 5012774]
[13]
Bremner, W.J.; Vitiello, M.V.; Prinz, P.N. Loss of circadian rhythmicity in blood testosterone levels with aging in normal men. J. Clin. Endocrinol. Metab., 1983, 56(6), 1278-1281.
[http://dx.doi.org/10.1210/jcem-56-6-1278] [PMID: 6841562]
[14]
Davidson, J.M.; Chen, J.J.; Crapo, L.; Gray, G.D.; Greenleaf, W.J.; Catania, J.A. Hormonal changes and sexual function in aging men. J. Clin. Endocrinol. Metab., 1983, 57(1), 71-77.
[http://dx.doi.org/10.1210/jcem-57-1-71] [PMID: 6602143]
[15]
Finkelstein, J.S.; Lee, H.; Burnett-Bowie, S.A.M.; Pallais, J.C.; Yu, E.W.; Borges, L.F.; Jones, B.F.; Barry, C.V.; Wulczyn, K.E.; Thomas, B.J.; Leder, B.Z. Gonadal steroids and body composition, strength, and sexual function in men. N. Engl. J. Med., 2013, 369(11), 1011-1022.
[http://dx.doi.org/10.1056/NEJMoa1206168] [PMID: 24024838]
[16]
Sparrow, D.; Bosse, R.; Rowe, J.W. The influence of age, alcohol consumption, and body build on gonadal function in men. J. Clin. Endocrinol. Metab., 1980, 51(3), 508-512.
[http://dx.doi.org/10.1210/jcem-51-3-508] [PMID: 6773977]
[17]
Mendell, A.L.; MacLusky, N.J. Neurosteroid metabolites of gonadal steroid hormones in neuroprotection: Implications for sex differences in neurodegenerative disease. Front. Mol. Neurosci., 2018, 11, 359.
[http://dx.doi.org/10.3389/fnmol.2018.00359] [PMID: 30344476]
[18]
Edinger, K.L.; Frye, C.A. Sexual experience of male rats influences anxiety-like behavior and androgen levels. Physiol. Behav., 2007, 92(3), 443-453.
[http://dx.doi.org/10.1016/j.physbeh.2007.04.018] [PMID: 17544460]
[19]
Balfour, M.E.; Brown, J.L.; Yu, L.; Coolen, L.M. Potential contributions of efferents from medial prefrontal cortex to neural activation following sexual behavior in the male rat. Neuroscience, 2006, 137(4), 1259-1276.
[http://dx.doi.org/10.1016/j.neuroscience.2005.11.013] [PMID: 16388908]
[20]
Pfaus, J.G.; Damsma, G.; Nomikos, G.G.; Wenkstern, D.G.; Blaha, C.D.; Phillips, A.G.; Fibiger, H.C. Sexual behavior enhances central dopamine transmission in the male rat. Brain Res., 1990, 530(2), 345-348.
[http://dx.doi.org/10.1016/0006-8993(90)91309-5] [PMID: 2176121]
[21]
Damsma, G.; Pfaus, J.G.; Wenkstern, D.; Phillips, A.G.; Fibiger, H.C. Sexual behavior increases dopamine transmission in the nucleus accumbens and striatum of male rats: Comparison with novelty and locomotion. Behav. Neurosci., 1992, 106(1), 181-191.
[http://dx.doi.org/10.1037/0735-7044.106.1.181] [PMID: 1313243]
[22]
López, H.H.; Ettenberg, A. Exposure to female rats produces differences in c-fos induction between sexually-naïve and experienced male rats. Brain Res., 2002, 947(1), 57-66.
[http://dx.doi.org/10.1016/S0006-8993(02)02907-4] [PMID: 12144853]
[23]
Gréco, B.; Edwards, D.A.; Michael, R.P.; Clancy, A.N. Androgen receptors and estrogen receptors are colocalized in male rat hypothalamic and limbic neurons that express Fos immunoreactivity induced by mating. Neuroendocrinology, 1998, 67(1), 18-28.
[http://dx.doi.org/10.1159/000054294] [PMID: 9485165]
[24]
Frye, C.A.; Duncan, J.E.; Basham, M.; Erskine, M.S. Behavioral effects of 3a-androstanediol II: Hypothalamic and preoptic area actions via a GABAergic mechanism. Behav. Brain Res., 1996, 79(1-2), 119-130.
[http://dx.doi.org/10.1016/0166-4328(96)00005-8] [PMID: 8883823]
[25]
Kohtz, A.S.; Frye, C.A. Learning and the lifespan: What’s sex got to do with It? Front. Neurosci., 2020, 14, 216.
[http://dx.doi.org/10.3389/fnins.2020.00216] [PMID: 32265631]
[26]
Frye, C.A.; McCormick, C.M.; Coopersmith, C.; Erskine, M.S. Effects of paced and non-paced mating stimulation on plasma progesterone, 3α-diol and corticosterone. Psychoneuroendocrinology, 1996, 21(4), 431-439.
[http://dx.doi.org/10.1016/0306-4530(95)00059-3] [PMID: 8844881]
[27]
Rao, P.N.; Khan, A.H.; Moore, P.H., Jr Synthesis of new steroid haptens for radioimmunoassay. Part III. 15β-carboxyethylmer-captosteroid-bovine serum albumin conjugates. Specific antisera for radioimmunoassay of 5α-dihydrotestosterone, 5α-androstane-3β, 17β-diol and 5α-androstane-3α, 17β-diol. Steroids, 1977, 29(2), 171-184.
[http://dx.doi.org/10.1016/0039-128X(77)90037-X] [PMID: 841620]
[28]
Rodbard, D.; Hutt, D.M. International Atomic Energy Agency Symposium on Radioimmunoassay and Related Procedures in Medicine. Statistical analysis of radioimmunoassay and immunoradiometric assays: A generalized, weighted iterative, least squares method for logistic curve fitting, UniputNew York 1974, pp. 209-233.
[29]
Brown, G.R.; Kulbarsh, K.D.; Spencer, K.A.; Duval, C. Peripubertal exposure to testicular hormones organizes response to novel environments and social behaviour in adult male rats. Horm. Behav., 2015, 73, 135-141.
[http://dx.doi.org/10.1016/j.yhbeh.2015.07.003] [PMID: 26159287]
[30]
Espinosa, P.; Silva, R.A.; Sanguinetti, N.K.; Venegas, F.C.; Riquelme, R.; González, L.F.; Cruz, G.; Renard, G.M.; Moya, P.R.; Sotomayor-Zárate, R. Programming of dopaminergic neurons by neonatal sex hormone exposure: Effects on dopamine content and tyrosine hydroxylase expression in adult male rats. Neural Plast., 2016, 2016, 1-11.
[http://dx.doi.org/10.1155/2016/4569785] [PMID: 26904299]
[31]
Aubele, T.; Kritzer, M.F. Androgen influence on prefrontal dopamine systems in adult male rats: localization of cognate intracellular receptors in medial prefrontal projections to the ventral tegmental area and effects of gonadectomy and hormone replacement on glutamate-stimulated extracellular dopamine level. Cereb. Cortex, 2012, 22(8), 1799-1812.
[http://dx.doi.org/10.1093/cercor/bhr258] [PMID: 21940701]
[32]
Locklear, M.N.; Michaelos, M.; Collins, W.F.; Kritzer, M.F. Gonadectomy but not biological sex affects burst-firing in dopamine neurons of the ventral tegmental area and in prefrontal cortical neurons projecting to the ventral tegmentum in adult rats. Eur. J. Neurosci., 2017, 45(1), 106-120.
[http://dx.doi.org/10.1111/ejn.13380] [PMID: 27564091]
[33]
Dimeo, A.; Wood, R. ICV testosterone induces Fos in male Syrian hamster brain. Psychoneuroendocrinology, 2006, 31(2), 237-249.
[http://dx.doi.org/10.1016/j.psyneuen.2005.08.001] [PMID: 16157456]
[34]
Triemstra, J.L.; Sato, S.M.; Wood, R.I. Testosterone and nucleus accumbens dopamine in the male Syrian hamster. Psychoneuroendocrinology, 2008, 33(3), 386-394.
[http://dx.doi.org/10.1016/j.psyneuen.2007.12.006] [PMID: 18249072]
[35]
Pfaus, J.G.; Phillips, A.G. Role of dopamine in anticipatory and consummatory aspects of sexual behavior in the male rat. Behav. Neurosci., 1991, 105(5), 727-743.
[http://dx.doi.org/10.1037/0735-7044.105.5.727] [PMID: 1840012]
[36]
Fadel, J.; Bubser, M.; Deutch, A.Y. Differential activation of orexin neurons by antipsychotic drugs associated with weight gain. J. Neurosci., 2002, 22(15), 6742-6746.
[http://dx.doi.org/10.1523/JNEUROSCI.22-15-06742.2002] [PMID: 12151553]
[37]
Aston-Jones, G.; Smith, R.J.; Moorman, D.E.; Richardson, K.A. Role of lateral hypothalamic orexin neurons in reward processing and addiction. Neuropharmacology, 2009, 56(Suppl. 1), 112-121.
[http://dx.doi.org/10.1016/j.neuropharm.2008.06.060] [PMID: 18655797]
[38]
Oades, R.D.; Rivet, J.M.; Taghzouti, K.; Kharouby, M.; Simon, H.; Le Moal, M. Catecholamines and conditioned blocking: effects of ventral tegmental, septal and frontal 6-hydroxydopamine lesions in rats. Brain Res., 1987, 406(1-2), 136-146.
[http://dx.doi.org/10.1016/0006-8993(87)90778-5] [PMID: 3105812]
[39]
Burns, M.; Domjan, M. Topography of spatially directed conditioned responding: Effects of context and trial duration. J. Exp. Psychol. Anim. Behav. Process., 2001, 27(3), 269-278.
[http://dx.doi.org/10.1037/0097-7403.27.3.269] [PMID: 11497325]
[40]
Matthews, R.N.; Domjan, M.; Ramsey, M.; Crews, D. Learning effects on sperm competition and reproductive fitness. Psychol. Sci., 2007, 18(9), 758-762.
[http://dx.doi.org/10.1111/j.1467-9280.2007.01974.x] [PMID: 17760768]
[41]
Frye, C.A.; Edinger, K.L.; Lephart, E.D.; Walf, A.A. 3α-androstanediol, but not testosterone, attenuates age-related decrements in cognitive, anxiety, and depressive behavior of male rats. Front. Aging Neurosci., 2010, 2, 15.
[http://dx.doi.org/10.3389/fnagi.2010.00015] [PMID: 20552051]
[42]
Frye, CA; Edinger, KL; Seliga, AM; Wawrzycki, JM 5 alpha-reduced androgens may have actions in the hippocampus to enhance cognitive performance of male rats. Psychoneuroendocrinology, 2004, 29(8), 1019-27.
[http://dx.doi.org/10.1016/j.psyneuen.2003.10.004]
[43]
Frye, CA; Koonce, CJ; Edinger, KL; Osborne, DM; Walf, AA Androgens with activity at estrogen receptor beta have anxiolytic and cognitive-enhancing effects in male rats and mice. Hormones and Behavior, 2008, 54(5), 726-34.
[http://dx.doi.org/10.1016/j.yhbeh.2008.07.013]
[44]
Roselli, C.E.; Horton, L.E.; Resko, J.A. Time-course and steroid specificity of aromatase induction in rat hypothalamus-preoptic area. Biol. Reprod., 1987, 37(3), 628-633.
[http://dx.doi.org/10.1095/biolreprod37.3.628] [PMID: 3676409]
[45]
Buddenberg, T.E.; Komorowski, M.; Ruocco, L.A.; Silva, M.A.S.; Topic, B. Attenuating effects of testosterone on depressive-like behavior in the forced swim test in healthy male rats. Brain Res. Bull., 2009, 79(3-4), 182-186.
[http://dx.doi.org/10.1016/j.brainresbull.2009.02.008] [PMID: 19429189]
[46]
Frye, C.A.; Sturgis, J.D. Neurosteroids affect spatial/reference, working, and long-term memory of female rats. Neurobiol. Learn. Mem., 1995, 64(1), 83-96.
[http://dx.doi.org/10.1006/nlme.1995.1046] [PMID: 7582815]
[47]
Glasper, E.R.; LaMarca, E.A.; Bocarsly, M.E.; Fasolino, M.; Opendak, M.; Gould, E. Sexual experience enhances cognitive flexibility and dendritic spine density in the medial prefrontal cortex. Neurobiol. Learn. Mem., 2015, 125, 73-79.
[http://dx.doi.org/10.1016/j.nlm.2015.07.007] [PMID: 26188276]
[48]
Frye, C.A.; Van Keuren, K.R.; Erskine, M.S. Behavioral effects of 3α-androstanediol I: modulation of sexual receptivity and promotion of GABA-stimulated chloride flux. Behav. Brain Res., 1996, 79(1-2), 109-118.
[http://dx.doi.org/10.1016/0166-4328(96)00004-6] [PMID: 8883822]
[49]
Gee, K.W. Steroid modulation of the GABA/benzodiazepine receptor-linked chloride lonophore. Mol. Neurobiol., 1988, 2(4), 291-317.
[http://dx.doi.org/10.1007/BF02935636] [PMID: 2855977]

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