Actions of testosterone in prepubertal and postpubertal male hamsters: dissociation of effects on reproductive behavior and brain androgen receptor immunoreactivity
Abstract
This study was conducted to determine whether there is a increase in responsiveness to the activating effects of testosterone on male reproductive behavior during puberty in male golden hamsters and whether responsiveness to behavioral actions of testosterone is correlated with the ability of testosterone to upregulate brain androgen receptor immunoreactivity (AR-ir). Sexually naive male hamsters were castrated at 21 or 42 days of age and implanted subcutaneously with a pellet containing 0, 2.5, or 5 mg of testosterone. One week later, males were given a 10-min mating test with a receptive female. Animals were euthanized 1 hr after the behavioral test, and blood samples and brains were collected. Plasma testosterone levels were equivalent in prepubertal and adult males that had been administered the same dose of testosterone. However, adult males exhibited more mounts, intromissions, and ejaculations than prepubertal males, demonstrating that postpubertal males are more responsive than prepubertal males to the effects of testosterone on sexual behavior. In both age groups, testosterone increased the number of AR-ir cells per unit area in several brain regions involved in male sexual behavior, including the medial preoptic nucleus (MPN), medial amygdala, posteromedial bed nucleus of the stria terminalis, and magnocellular preoptic nucleus (MPNmag). Surprisingly, testosterone increased AR-ir in the latter three regions to a greater extent in prepubertal males than in adults. Thus, prepubertal males are more responsive to the effects of testosterone on AR-ir in these regions. In a separate experiment, a pubertal increase in the number of AR-ir cells per unit area was found in both the MPN and MPNmag of intact male hamsters. These results indicate that a testosterone-dependent increase in brain AR during puberty may be necessary, but is not sufficient, to induce an increase in behavioral responsiveness to testosterone.
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Recent studies demonstrate that organizational changes occur during adolescence and may be critical for activational changes to take place.
“recent studies have demonstrated that there are organizational changes occurring during adolescence as well, and, moreover, that these organizational changes may be critical for activational changes to take place”
From Impact of socio-emotional context, brain development, and pubertal maturation on adolescent risk-taking (2013) · cites this paper as Meek et al., 1997
Cites
The physiology of male sexual behavior
Meisel, R. (1994) · Medical Entomology and Zoology · Cited by 988 · see citing works
Immunohistochemical Localization of the Androgen Receptor in Rat and Human Tissues*
Sar, M., Lubahn, D. B., French, F. S., & Wilson, E. M. (1990) · Endocrinology · doi:10.1210/endo-127-6-3180 · Cited by 489 · see citing works
Kemppainen, J., Lane, M. V., Sar, M., & Wilson, E. M. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)48380-9 · Cited by 430 · see citing works
Roy, A. K., Lavrovsky, Y., Song, C., Chen, S., Jung, M. H., Velu, N., Bi, B., & Chatterjee, B. (1998) · Vitamins and hormones · doi:10.1016/s0083-6729(08)60938-3 · Cited by 412 · see citing works
Kerr, J. E., Allore, R., Beck, S. G., & Handa, R. J. (1995) · Endocrinology · doi:10.1210/endo.136.8.7628354 · Cited by 296 · see citing works
Zhou, L., Blaustein, J. D., & De Vries, G. J. (1994) · Endocrinology · doi:10.1210/endo.134.6.8194487 · Cited by 189 · see citing works
Lehman, M. N., & Winans, S. S. (1982) · Brain Research · doi:10.1016/0006-8993(82)90641-2 · Cited by 188 · see citing works
Androgens Regulate Brain Aromatase Activity in Adult Male Rats through a Receptor Mechanism*
Roselli, C. E., & Resko, J. A. (1984) · Endocrinology · doi:10.1210/endo-114-6-2183 · Cited by 186 · see citing works
MPOA and BNST lesions in male Syrian hamsters
Powers, J. B., Newman, S. W., & Bergondy, M. L. (1987) · Behavioural Brain Research · doi:10.1016/0166-4328(87)90019-2 · Cited by 177 · see citing works
Fernandez-Fewell, G. D., & Meredith, M. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-06-03643.1994 · Cited by 176 · see citing works
Wood, R. I., & Newman, S. W. (1993) · Brain Research · doi:10.1016/0006-8993(93)91019-o · Cited by 135 · see citing works
Syms, A. J., Norris, J. S., Panko, W. B., & Smith, R. G. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)89753-8 · Cited by 134 · see citing works
PHOTOPERIODIC REGULATION OF COPULATORY BEHAVIOUR IN THE MALE HAMSTER
Morin, L. P., & Zucker, I. (1978) · Journal of Endocrinology · doi:10.1677/joe.0.0770249 · Cited by 119 · see citing works
Up-regulation of androgen receptor immunoreactivity in the rat brain by androgenic-anabolic steroids
Menard, C. S., & Harlan, R. E. (1993) · Brain Research · doi:10.1016/0006-8993(93)90823-6 · Cited by 114 · see citing works
Nosrat, C. A., Ebendal, T., & Olson, L. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19961223)376:4 · Cited by 114 · see citing works
Self-citationPheromones induce c-fos in limbic areas regulating male hamster mating behavior
Fiber, J. M., Adames, P., & Swann, J. M. (1993) · Neuroreport · doi:10.1097/00001756-199307000-00008 · Cited by 113 · see citing works
Baum, M. J., Tobet, S. A., Starr, M. S., & Bradshaw, W. G. (1982) · Hormones and Behavior · doi:10.1016/0018-506x(82)90020-4 · Cited by 111 · see citing works
Prins, G. S., & Birch, L. A. (1993) · Endocrinology · doi:10.1210/endo.132.1.8419121 · Cited by 108 · see citing works
Kollack, S. S., & Newman, S. W. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90270-h · Cited by 102 · see citing works
Wood, R. I., & Newman, S. W. (1993) · Journal of Neurobiology · doi:10.1002/neu.480240706 · Cited by 96 · see citing works
Shan, L., Hardy, D. O., Catterall, J. F., & Hardy, M. P. (1995) · Endocrinology · doi:10.1210/endo.136.4.7895679 · Cited by 90 · see citing works
Sexual behavior in developing male rats
Södersten, P., DAMASSA, D. A., & Smith, E. R. (1977) · Hormones and Behavior · doi:10.1016/0018-506x(77)90006-x · Cited by 89 · see citing works
Krey, L. C., & McGinnis, M. Y. (1990) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(90)90247-p · Cited by 85 · see citing works
Freeman, L. M., Padgett, B., Prins, G. S., & Breedlove, S. M. (1995) · Journal of Neurobiology · doi:10.1002/neu.480270106 · Cited by 78 · see citing works
CAMPBELL, C., Finkelstein, J. N., & TUREK, F. (1978) · Physiology & Behavior · doi:10.1016/0031-9384(78)90101-4 · Cited by 77 · see citing works
Albert, D. J., Jonik, R. H., Watson, N. V., Gorzalka, B. B., & Walsh, M. L. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90336-3 · Cited by 65 · see citing works
Auger, A., & Blaustein (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-03-02272.1995 · Cited by 62 · see citing works
Critical exposure time for androgen activation of male sexual behavior in rats
McGinnis, M. Y., Mirth, M. C., Zebrowski, A. F., & Dreifuss, R. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90249-7 · Cited by 58 · see citing works
Precocious mating in male rats following treatment with androgen or estrogen.
Baum, M. J. (1972) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0032288 · Cited by 55 · see citing works
González-Cadavid, N. F., Vernet, D. A., Navarro, A. F., Rodríguez, J. A., Swerdloff, R. S., & Rajfer, J. (1993) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(93)90155-d · Cited by 55 · see citing works
Sisk, C. L., & Turek, F. W. (1983) · Endocrinology · doi:10.1210/endo-112-4-1208 · Cited by 54 · see citing works
Self-citationClancy, A. N., Whitman, C., Michael, R. P., & Albers, H. E. (1994) · Brain Research Bulletin · doi:10.1016/0361-9230(94)90201-1 · Cited by 48 · see citing works
Testicular hormone and developmental changes in mating behavior of the male rat.
Larsson, K. (1967) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0024358 · Cited by 47 · see citing works
lqbal, J., Swanson, J. J., Prins, G. S., & Jacobson, C. D. (1995) · Brain Research · doi:10.1016/0006-8993(95)00983-3 · Cited by 43 · see citing works
Prins, G. S. (1993) · Endocrinology · doi:10.1210/en.132.1.169 · Cited by 42 · see citing works
Androgenic regulation of chemoinvestigatory behaviors in male and female hamsters
Powers, J. B., & Bergondy, M. L. (1983) · Hormones and Behavior · doi:10.1016/0018-506x(83)90013-2 · Cited by 40 · see citing works
Development of responses to vaginal secretion and other substances in golden hamsters
Johnston, R. E., & Coplin, B. (1979) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(79)90242-5 · Cited by 35 · see citing works
Photoperiodic Influences on Sexual Behavior in Male Syrian Hamsters
Powers, J. B., Steel, E., Hutchison, J. B., Hastings, M. H., Herbert, J., & Walker, A. P. (1989) · Journal of Biological Rhythms · doi:10.1177/074873048900400105 · Cited by 32 · see citing works
Androgen receptor immunoreactivity in intact and castrate guinea pig using antipeptide antibodies
Choate, J. V. A., & Resko, J. A. (1992) · Brain Research · doi:10.1016/0006-8993(92)91504-8 · Cited by 27 · see citing works
Regulation of Brain Androgen Receptor Immunoreactivity by Androgen in Prepubertal Male Ferrets1
Kashon, M. L., Hayes, M. J., Shek, P. P., & Sisk, C. L. (1995) · Biology of Reproduction · doi:10.1095/biolreprod52.5.1198 · Cited by 26 · see citing works
Self-citationKashon, M. L., & Sisk, C. L. (1994) · Developmental Brain Research · doi:10.1016/0165-3806(94)90031-0 · Cited by 23 · see citing works
Self-citationBittman, E. L., & Krey, L. C. (2008) · Neuroendocrinology · doi:10.1159/000124892 · Cited by 21 · see citing works
Photoperiod Modulates Pubertal Shifts in Behavioral Responsiveness to Testosterone
Sisk, C. L., Berglund, L. A., Tang, Y. P., & Venier, J. E. (1992) · Journal of Biological Rhythms · doi:10.1177/074873049200700406 · Cited by 21 · see citing works
Self-citationPrins, G. S., Bartke, A., & Steger, R. W. (2008) · Neuroendocrinology · doi:10.1159/000125636 · Cited by 13 · see citing works
Photoperiod times ontogeny of androgen receptor-immunoreactive cells in ferrets*
Kashon, M. L., & Sisk, C. L. (1995) · Neuroreport · doi:10.1097/00001756-199501000-00028 · Cited by 2 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Sexual dimorphism of brain developmental trajectories during childhood and adolescence
Lenroot, R. K., Gogtay, N., Greenstein, D. K., Wells, E. M., Wallace, G. L., Clasen, L. S., Blumenthal, J. D., Lerch, J., Zijdenbos, A. P., Evans, A. C., et al. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.03.053 · Cited by 1,309 · see citing works
The neural basis of puberty and adolescence
Sisk, C. L., & Foster, D. L. (2004) · Nature Neuroscience · doi:10.1038/nn1326 · Cited by 1,085 · see citing works
Self-citationPubertal hormones organize the adolescent brain and behavior
Sisk, C. L., & Zehr, J. L. (2005) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2005.10.003 · Cited by 1,082 · see citing works
Self-citationPuberty and the human brain: insights into adolescent development
Vijayakumar, N., Op de Macks, Z., Shirtcliff, E. A., & Pfeifer, J. H. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.06.004 · Cited by 437 · see citing works
The organizing actions of adolescent gonadal steroid hormones on brain and behavioral development
Schulz, K. M., & Sisk, C. L. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.036 · Cited by 316 · see citing works
Self-citationPuberty and structural brain development in humans
Herting, M. M., & Sowell, E. R. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.12.003 · Cited by 305 · see citing works
Romeo, R. D. (2003) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2003.01106.x · Cited by 233 · see citing works
Self-citationSmith, A. R., Chein, J., & Steinberg, L. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.03.006 · Cited by 214 · see citing works
Testosterone Cannot Activate an Adult-Like Stress Response in Prepubertal Male Rats
Romeo, R. D., Lee, S. H., Chhua, N., McPherson, C. R., & McEwen, B. S. (2004) · Neuroendocrinology · doi:10.1159/000077270 · Cited by 197 · see citing works
Self-citationAndrogen Receptor in Mouse Brain: Sex Differences and Similarities in Autoregulation 1
Lu, S., McKenna, S., Cologer–Clifford, A., Nau, E. A., & Simon, N. G. (1998) · Endocrinology · doi:10.1210/endo.139.4.5863 · Cited by 183 · see citing works
Schulz, K. M., Richardson, H. N., Zehr, J. L., Osetek, A. J., Menard, T. A., & Sisk, C. L. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2003.12.007 · Cited by 169 · see citing works
Self-citationSchulz, K. M., & Sisk, C. L. (2006) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2006.04.025 · Cited by 154 · see citing works
Self-citationPuberty and the maturation of the male brain and sexual behavior: recasting a behavioral potential
Romeo, R. D., Richardson, H. N., & Sisk, C. L. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(02)00009-x · Cited by 152 · see citing works
Self-citationDendritic pruning of the medial amygdala during pubertal development of the male Syrian hamster
Zehr, J. L., Todd, B. J., Schulz, K. M., McCarthy, M. M., & Sisk, C. L. (2006) · Journal of Neurobiology · doi:10.1002/neu.20251 · Cited by 145 · see citing works
Self-citationChemosignals, hormones and mammalian reproduction
Petrulis, A. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.03.011 · Cited by 142 · see citing works
Adolescents and androgens, receptors and rewards
Sato, S. M., Schulz, K. M., Sisk, C. L., & Wood, R. I. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.01.010 · Cited by 124 · see citing works
Self-citationTestosterone Programs Adult Social Behavior before and during, But Not after, Adolescence
Schulz, K. M., Zehr, J. L., Salas-Ramirez, K. Y., & Sisk, C. L. (2009) · Endocrinology · doi:10.1210/en.2008-1708 · Cited by 105 · see citing works
Self-citationPuberty: A finishing school for male social behavior
SISK, C. L., SCHULZ, K. M., & ZEHR, J. L. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1286.019 · Cited by 89 · see citing works
Self-citationChemosignals and hormones in the neural control of mammalian sexual behavior
Petrulis, A. (2013) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.07.007 · Cited by 75 · see citing works
Sexual experience affects reproductive behavior and preoptic androgen receptors in male mice
Swaney, W. T., Dubose, B. N., Curley, J. P., & Champagne, F. A. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.001 · Cited by 73 · see citing works
Androgen receptor expression in the developing male and female rat visual and prefrontal cortex
Nuñez, J. L., Huppenbauer, C. B., McAbee, M. D., Juraska, J. M., & DonCarlos, L. L. (2003) · Journal of Neurobiology · doi:10.1002/neu.10236 · Cited by 71 · see citing works
Alexanderson, C., Eriksson, E., Stener-Victorin, E., Lystig, T., Gabrielsson, B., Lönn, M., & Holmäng, A. (2007) · Endocrinology · doi:10.1210/en.2007-0305 · Cited by 69 · see citing works
Hormonal Processes in the Development and Expression of Aggressive Behavior
Simon, N. G. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50007-x · Cited by 69 · see citing works
Pubertal and seasonal plasticity in the amygdala
Romeo, R. D., & Sisk, C. L. (2001) · Brain Research · doi:10.1016/s0006-8993(00)03111-5 · Cited by 67 · see citing works
Self-citationLaroche, J., Gasbarro, L., Herman, J. P., & Blaustein, J. D. (2009) · Endocrinology · doi:10.1210/en.2009-0099 · Cited by 65 · see citing works
Evuarherhe, O., Leggett, J. D., Waite, E. J., Kershaw, Y. M., Atkinson, H. C., & Lightman, S. L. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.168393 · Cited by 61 · see citing works
Williamson, M., Bingham, B., & Viau, V. (2005) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2005.08.009 · Cited by 58 · see citing works
Schulz, K. M., Menard, T. A., Smith, D. A., Albers, H. E., & Sisk, C. L. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.006 · Cited by 57 · see citing works
Self-citationMohr, M. A., & Sisk, C. L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219443110 · Cited by 51 · see citing works
Self-citationNeuroendocrine and Behavioral Development during Puberty: A Tale of Two Axes
Romeo, R. D. (2005) · Vitamins and hormones · doi:10.1016/s0083-6729(05)71001-3 · Cited by 51 · see citing works
Self-citationDopamine Mediates Testosterone-Induced Social Reward in Male Syrian Hamsters
Bell, M. R., & Sisk, C. L. (2013) · Endocrinology · doi:10.1210/en.2012-2042 · Cited by 47 · see citing works
Self-citationSimon, N. G., & Lu, S. (2005) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195168761.003.0009 · Cited by 43 · see citing works
Pedersen, K. E., Letcher, R. J., Sonne, C., Dietz, R., & Styrishave, B. (2016) · Environment International · doi:10.1016/j.envint.2016.07.015 · Cited by 44 · see citing works
Testosterone, puberty, and the pattern of male aggression in Syrian hamsters
Romeo, R. D., Schulz, K. M., Nelson, A. L. A., Menard, T. A., & Sisk, C. L. (2003) · Developmental Psychobiology · doi:10.1002/dev.10125 · Cited by 44 · see citing works
Self-citationSalas-Ramirez, K. Y., Montalto, P. R., & Sisk, C. L. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.11.004 · Cited by 41 · see citing works
Self-citationRomeo, R. D., Parfitt, D. B., Richardson, H. N., & Sisk, C. L. (1998) · Hormones and Behavior · doi:10.1006/hbeh.1998.1463 · Cited by 41 · see citing works
Self-citationApostolinas, S., Rajendren, G. V., Dobrjansky, A., & Gibson, M. J. (1999) · Brain Research · doi:10.1016/s0006-8993(98)01180-9 · Cited by 41 · see citing works
Richardson, H. N., Nelson, A. L. A., Ahmed, E. I., Parfitt, D. B., Romeo, R. D., & Sisk, C. L. (2004) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2004.06.008 · Cited by 38 · see citing works
Self-citationDihydrotestosterone activates sexual behavior in adult male hamsters but not in juveniles
Romeo, R. D., Cook-Wiens, E., Richardson, H. N., & Sisk, C. L. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00499-1 · Cited by 39 · see citing works
Self-citationSchulz, K. M., Richardson, H. N., Romeo, R. D., Morris, J. A., Lookingland, K. J., & Sisk, C. L. (2003) · Brain Research · doi:10.1016/s0006-8993(03)03358-4 · Cited by 37 · see citing works
Self-citationHolmes, M. M., & Wade, J. D. (2005) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2005.01339.x · Cited by 36 · see citing works
The effects of puberty and its hormones on subcortical brain development
Vijayakumar, N., Youssef, G. J., Allen, N. B., Anderson, V. A., Efron, D., Mundy, L. K., Patton, G. C., Simmons, J. G., Silk, T. J., & Whittle, S. (2021) · Comprehensive Psychoneuroendocrinology · doi:10.1016/j.cpnec.2021.100074 · Cited by 35 · see citing works
Topper, V. Y., Walker, D. M., & Gore, A. C. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.07.013 · Cited by 35 · see citing works
Cordes, M. A., Stevenson, S. A., Driessen, T. M., Eisinger, B. E., & Riters, L. V. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.09.029 · Cited by 33 · see citing works
Relationship between Sexual Satiety and Brain Androgen Receptors
Romano-Torres, M., Phillips-Farfán, B. V., Chavira, R., Rodrı́guez–Manzo, G., & Fernández‐Guasti, A. (2007) · Neuroendocrinology · doi:10.1159/000099250 · Cited by 32 · see citing works
Olesen, K. M., Ismail, N., Merchasin, E. D., & Blaustein, J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.06.005 · Cited by 34 · see citing works
Romeo, R. D., Wagner, C. K., Jansen, H. T., Diedrich, S. L., & Sisk, C. L. (2002) · Behavioral Neuroscience · doi:10.1037//0735-7044.116.2.198 · Cited by 31 · see citing works
Self-citationLorme, K. C. D., Bell, M. R., & Sisk, C. L. (2013) · Current Directions in Psychological Science · doi:10.1177/0963721413479607 · Cited by 26 · see citing works
Self-citationIslam, M. N., Sakimoto, Y., Jahan, M. R., Ishida, M., Tarif, A. M. M., Nozaki, K., Masumoto, K., Yanai, A., Mitsushima, D., & Shinoda, K. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.05.025 · Cited by 25 · see citing works
Bittman, E. L., Ehrlich, D. A., Ogdahl, J. L., & Jetton, A. E. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.102.010900 · Cited by 22 · see citing works
Romeo, R. D., Wade, J., Venier, J. E., & Sisk, C. L. (1999) · Endocrinology · doi:10.1210/endo.140.1.6420 · Cited by 21 · see citing works
Self-citationBell, M. R., Lorme, K. C. D., Figueira, R. J., Kashy, D. A., & Sisk, C. L. (2012) · European Journal of Neuroscience · doi:10.1111/ejn.12058 · Cited by 20 · see citing works
Self-citationLeishman, E., Kokesh, K. J., & Bradshaw, H. B. (2013) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12081 · Cited by 20 · see citing works
Cordes, M. A., Stevenson, S. A., & Riters, L. V. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.02.010 · Cited by 20 · see citing works
Piekarski, D. J., Place, N. J., & Zucker, I. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012749 · Cited by 20 · see citing works
Johnson, M. A., Cohen, R. E., Vandecar, J. R., & Wade, J. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.05.004 · Cited by 20 · see citing works
Richardson, H. N., Gore, A. C., Venier, J. E., Romeo, R. D., & Sisk, C. L. (2003) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2003.11.013 · Cited by 18 · see citing works
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Godwin, J., Hartman, Nag, & Crews (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00513.x · Cited by 17 · see citing works
Islam, M. N., Sakimoto, Y., Jahan, M. R., Miyasato, E., Tarif, A. M. M., Nozaki, K., Masumoto, K., Yanai, A., Mitsushima, D., & Shinoda, K. (2021) · Brain Sciences · doi:10.3390/brainsci11020239 · Cited by 16 · see citing works
He, F., Tai, F.-D., Zhang, Y.-H., & Zhang, X. (2012) · Journal of Comparative Physiology · doi:10.1007/s00359-012-0713-6 · Cited by 16 · see citing works
A role for the androgen receptor in the sexual differentiation of the olfactory system in mice
Bodo, C. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.08.008 · Cited by 16 · see citing works
Richardson, H. N., Parfitt, D. B., Thompson, R. C., & Sisk, C. L. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.0007-1331.2002.00787.x · Cited by 16 · see citing works
Self-citationSpool, J. A., Stevenson, S. A., Angyal, C. S., & Riters, L. V. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.09.004 · Cited by 15 · see citing works
Estrogen receptor immunoreactivity in prepubertal and adult male Syrian hamsters
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McEwen, B. S. (1997) · Humana Press eBooks · doi:10.1007/978-1-59259-641-6_5 · Cited by 6 · see citing works
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Baum, M. J. (2006) · Springer eBooks · doi:10.1007/978-0-387-30405-2_1 · Cited by 3 · see citing works
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Cooke, B. M., & Woolley, C. S. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00066-8 · Cited by 2 · see citing works
Piekarski, D. J., Jarjisian, S. G., & Zucker, I. (2012) · Chronobiology International · doi:10.3109/07420528.2012.699125 · Cited by 2 · see citing works
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Schulz, K. M., & Sisk, C. L. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00105-x
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Piekarski, D. J. (2012) · eScholarship (California Digital Library)
Schulz, K. M., Chavez, M. C., & Forrester-Fronstin, Z. (2024) · Physiology & Behavior · doi:10.1016/j.physbeh.2025.114862
DeCaluwe, H. B. (2012) · University Libraries (University of Maryland)
Vihtelic, T. S., & Hyde, D. R. (2000) · Journal of Neurobiology · doi:10.1002/1097-4695(20000905)44:3
Self-citation
- Authors
- Meek, L. R., Romeo, R. D., Novak, C. M., & Sisk, C. L.
- Affiliations
- Michigan State University (US)
- Corresponding author
- Sisk, Cheryl L.
- Venue
- Hormones and Behavior
- Publisher
- Elsevier BV
- Published
- 1997-02
- Volume
- 31
- Issue
- 1
- Pages
- 75-88
- ISSN
- 0018-506X (ISSN-L)
- OpenAlex
- W2035916440
- Cited by
- 91
- References
- 45
- Citations by year
- 2025: 1 · 2024: 2 · 2021: 4 · 2020: 2 · 2018: 1 · 2017: 1 · 2016: 5 · 2015: 4 · 2014: 5 · 2013: 8 · 2012: 7
- FWCI
- 2.70
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hormones and Behavior (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Kementerian Pendidikan Nasional
- National Institutes of Health (1k04hd000950-01)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD-26483, R01HD026483, HD-00950)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- testosterone, puberty, male reproductive behavior, androgen receptor, prepubertal males, golden hamster, medial preoptic nucleus, magnocellular preoptic nucleus, medial amygdala, bed nucleus of the stria terminalis, castration, testosterone implants, sexual behavior
- MeSH terms
- Animals, Brain, Female, Cricetinae, Immunohistochemistry, Male, Receptors, Androgen, Sexual Behavior, Animal, Sexual Maturation, Testosterone
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