A Study of the Role of the Postnatal Testes in Determining the Ontogeny of Gonadotropin Secretion in the Male Rhesus Monkey (Macaca mulatto)*
Abstract
To further examine the role of the testes in determining the ontogeny of gonadotropin secretion in the male rhesus monkey, the time courses of circulating LH and FSH concentrations were determined using established RIAs in daytime and nighttime blood samples collected at weekly intervals from birth until 4 yr of age in intact animals (n = 7) and in males orchidectomized at approximately 1 week of age (n = 6). Estimates of plasma androgen (A) concentrations were obtained on nonchromatographed samples with a RIA that reacts with testosterone and other androgens. Plasma PRL concentrations were also determined by RIA, and body weight was monitored at weekly intervals. Testicular volumes were measured at weekly intervals after 1.8 yr of age in five animals. In intact animals, mean daytime plasma A concentrations during the first 3 months of infantile development ranged from 1-6 ng/ml. Daytime plasma A concentrations then declined to reach 0.5-1 ng/ml by 9 months of age, where they were maintained usually until 3 yr of age when circulating levels progressively increased to reach, by approximately 3.5 yr of age, mean levels (6 ng/ml) characteristic of fully mature males. During the transition from infantile to prepubertal development, circulating LH and FSH concentrations snowed a pattern similar to that of A, with elevations during the first 2 months of life followed by a decline to undetectable concentrations. In contrast to A, however, distinct pubertal increments in circulating LH and FSH concentrations were not observed in daytime samples from intact animals. The first indication of the pubertal reactivation of the hypothalamic-pituitary-testicular axis was provided by a reemergence of nocturnal elevations in plasma A concentrations between 2-3 yr of age. These were followed shortly thereafter by detectable plasma LH concentrations in nighttime samples. Orchidectomy at 1 week of age resulted in a progressive and dramatic rise in circulating gonadotropin concentrations, which plateaued approximately 3 weeks later at values 1 order of magnitude greater than those observed in intact animals. This hypersecretion of LH and FSH was not sustained, however, and by 10 months of age, plasma gonadotropin concentrations in agonadal animals were indistinguishable from those in agematched intact controls. These low levels of the gonadotropic hormones were maintained, in the absence of the testes, for approximately 2 yr until a second or “pubertal” postcastration hypersecretion of LH and FSH was observed. Circulating gonadotropin levels rose dramatically to reach, by 3 yr of age, concentrations similar to those observed in orchidectomized infantile monkeys and in adults castrated postpubertally. These observations provide further evidence to support the view that, in higher primates, the hiatus in gonadotropin secretion during prepubertal development is occasioned by mechanisms of extragonadal origin. Thus, it would appear that the gonadostat hypothesis, which proposes that the restraint of LH and FSH secretion during prepubertal development is occasioned by the inhibitory action of gonadal hormones on a hypersensitive hypothalamic-hypophysial apparatus, should no longer be invoked as the fundamental mechanism underlying the protracted delay in the onset of puberty in higher primates. The reactivation of the hypothalamic-pituitary apparatus in neonatally orchidectomized monkeys at an age (2V2 yr) when the initiation of the pubertal process may have been anticipated had the animals remained intact also suggests that testicular hormones have little impact on the postnatal ontogeny of central neural mechanisms that govern the intermittent release of hypothalamic GnRH. Striking circannual like fluctuations in serum PRL concentrations were observed, after 1 yr of age, in both intact and agonadal animals throughout prepubertal and peripubertal development. On several occasions, the first evidence of a pubertal reactivation of gonadotropin secretion, namely the onset of nocturnal A secretion in intact animals and the reinitiation of FSH secretion in agonadal animals, was associated with a nadir in plasma PRL concentrations. Thus, it is possible that PRL may play a role in determining the precise timing of the onset of the pubertal process in this species. (Endocrinology116: 1341-1350,1985)
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The developmental mechanisms that account for major remodeling of connectivity occur before the onset of adolescence, i.e., before postnatal day 28 (PD28) in rodents, 9 months in cats, and 3 years in non-human primates.
“The developmental mechanisms that account for major remodeling of connectivity occur before the onset of adolescence, i.e., before postnatal day 28 (PD28) in rodents, 9 months in cats, and 3 years in non-human primates15, 16, 17”
From A role for synaptic plasticity in the adolescent development of executive function (2013) · cites this paper as [16]
Cites
Statistical principles in experimental design.
Winer, B. J. (1962) · McGraw-Hill Book Company · doi:10.1037/11774-000 · Cited by 27,137 · see citing works
Sexual Differentiation of the Central Nervous System
MacLusky, N. J., & Naftolin, F. (1981) · Science · doi:10.1126/science.6163211 · Cited by 1,469 · see citing works
Belchetz, P. E., Plant, T. M., Nakai, Y., Keogh, E. J., & Knobil, E. (1978) · Science · doi:10.1126/science.100883 · Cited by 1,385 · see citing works
Self-citationKrey, L. C., Butler, W. R., & Knobil, E. (1975) · Endocrinology · doi:10.1210/endo-96-5-1073 · Cited by 473 · see citing works
The later development of the brain and its vulnerability
Dobbing, J. (1982) · Journal of Inherited Metabolic Disease · doi:10.1007/bf01805569 · Cited by 353 · see citing works
Experimental Induction of Puberty in the Infantile Female Rhesus Monkey
Wildt, L., Marshall, G. R., & Knobil, E. (1980) · Science · doi:10.1126/science.6986658 · Cited by 349 · see citing works
Human puberty. Simultaneous augmented secretion of luteinizing hormone and testosterone during sleep
Boyar, R. M., Rosenfeld, R. S., Kapen, S., Finkelstein, J. W., Roffwarg, H. P., Weitzman, E. D., & Hellman, L. (1974) · Journal of Clinical Investigation · doi:10.1172/jci107798 · Cited by 317 · see citing works
Recent Advances in the Endocrinology of Puberty
Ojeda, S. R., Andrews, W. W., Advis, J. P., & WHITE, S. S. (1980) · Endocrine Reviews · doi:10.1210/edrv-1-3-228 · Cited by 298 · see citing works
A diphasic pattern of gonadotropin secretion in patients with the syndrome of gonadal dysgenesis
CONTE, F. A., GRUMBACH, M. M., & KAPLAN, S. L. (1975) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-40-4-670 · Cited by 276 · see citing works
Induced LH Surges in the Rhesus Monkey: Strength-Duration Characteristics of the Estrogen Stimulus12
Karsch, F. J., Weick, R. F., Butler, W. R., Dierschke, D. J., Krey, L. C., Weiss, G., Hotchkiss, J., YAMAJI, T., & Knobil, E. (1973) · Endocrinology · doi:10.1210/endo-92-6-1740 · Cited by 188 · see citing works
Physical growth of the rhesus monkey (Macaca mulatta)
WAGENEN, G. V., & CATCHPOLE, H. R. (1956) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330140219 · Cited by 180 · see citing works
Toran‐Allerand, C. D. (1980) · Brain Research · doi:10.1016/0006-8993(80)90101-8 · Cited by 176 · see citing works
Postnatal growth of nonhuman primates: the problem of the adolescent spurt.
Watts, E. S., & Gavan, J. A. (1982) · PubMed · Cited by 158 · see citing works
Plant, T. M. (1981) · Biology of Reproduction · doi:10.1095/biolreprod25.2.244 · Cited by 131 · see citing works
Self-citationEndocrine Correlates of Sexual Development in the Male Monkey, Macaca fascicularis*
Steiner, R. A., & Bremner, W. J. (1981) · Endocrinology · doi:10.1210/endo-109-3-914 · Cited by 111 · see citing works
Testosterone and the Control of Gonadotropin Secretion in the Male Rhesus Monkey (Macaca mulatto)*
Plant, T. M., Hess, D. L., Hotchkiss, J., & Knobil, E. (1978) · Endocrinology · doi:10.1210/endo-103-2-535 · Cited by 94 · see citing works
Self-citationMatsumoto, A., & Arai, Y. (2008) · Neuroendocrinology · doi:10.1159/000123223 · Cited by 87 · see citing works
THE NOCTURNAL RISE OF PLASMA TESTOSTERONE IN PUBERTAL BOYS.
Judd, H. L., PARKER, D. C., Siler, T. M., & Yen, S. S. C. (1974) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-38-4-710 · Cited by 74 · see citing works
Rapisarda, J., BERGMAN, K. S., Steiner, R. A., & Foster, D. L. (1983) · Endocrinology · doi:10.1210/endo-112-4-1172 · Cited by 72 · see citing works
SIMULTANEOUS AUGMENTED SECRETION OF LUTEINIZING HORMONE AND TESTOSTERONE DURING SLEEP
BOYAR, R. M., Rosenfeld, R. S., Kapen, S., Finkelstein, J. W., Roffwarg, H. P., Weitzman, E. D., & HELLMAN, L. (1974) · Cited by 68 · see citing works
RESKO, J. A., KALEEM QUADRI, S., & SPIES, H. G. (1977) · Endocrinology · doi:10.1210/endo-101-1-215 · Cited by 63 · see citing works
Testicular development in the rhesus monkey
WAGENEN, G. V., & Simpson, M. E. (1954) · The Anatomical Record · doi:10.1002/ar.1091180209 · Cited by 59 · see citing works
Neonatal Hormone Patterns In the Macaque. I. Steroids1
Robinson, J. A., & Bridson, W. E. (1978) · Biology of Reproduction · doi:10.1095/biolreprod19.4.773 · Cited by 55 · see citing works
Plant, T. M. (1980) · Endocrinology · doi:10.1210/endo-106-5-1451 · Cited by 52 · see citing works
Self-citationBercu, B. B., Lee, B. C., Pineda, J. L., Spiliotis, B. E., Denman, D. W., Hoffman, H. J., Brown, T. J., & Sachs, H. C. (1983) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-56-6-1214 · Cited by 50 · see citing works
Radioimmunoassay of Rhesus Monkey Follicle— Stimulating Hormone (RhFSH)
YAMAJI, T., PECKHAM, W. D., Atkinson, L. E., Dierschke, D. J., & Knobil, E. (1973) · Endocrinology · doi:10.1210/endo-92-6-1652 · Cited by 43 · see citing works
Frawley, L. S., & Neill, J. D. (1979) · Biology of Reproduction · doi:10.1095/biolreprod20.5.1147 · Cited by 43 · see citing works
A Radioimmunoassay for Rhesus Monkey Luteinizing Hormone (RhLH)
Monroe, S. E., PECKHAM, W. D., Neill, J. D., & Knobil, E. (1970) · Endocrinology · doi:10.1210/endo-86-5-1012 · Cited by 41 · see citing works
Pulsatile luteinizing hormone secretion in the neonatal male rhesus monkey ( Macaca mulatta )
Plant, T. M. (1982) · Journal of Endocrinology · doi:10.1677/joe.0.0930071 · Cited by 33 · see citing works
Self-citationA New Substance Resembling Luteinizing Hormone in the Blood of Rhesus Monkeys
PECKHAM, W. D., Foster, D. L., & Knobil, E. (1977) · Endocrinology · doi:10.1210/endo-100-3-826 · Cited by 28 · see citing works
Bercu, B. B., Lee, B. C., Spiliotis, B. E., Pineda, J. L., Denman, D. W., Hoffman, H. J., & Brown, T. J. (1983) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-56-6-1227 · Cited by 25 · see citing works
Plant, T. M. (2008) · Neuroendocrinology · doi:10.1159/000123409 · Cited by 22 · see citing works
Self-citationBeck, W. A., & Wuttke, W. (1979) · Journal of Endocrinology · doi:10.1677/joe.0.0830131 · Cited by 21 · see citing works
Plant, T. M., & Zorub, D. S. (1982) · PubMed · Cited by 21 · see citing works
Self-citationPlant, T. M., & Zorub, D. S. (1984) · Endocrinology · doi:10.1210/endo-114-2-560 · Cited by 19 · see citing works
Self-citationSex-Dependent Gonadotropin Concentrations in Infant Chimpanzees and Rhesus Monkeys
Fuller, G. B., Faiman, C., Winter, J. S. D., Reyes, F. I., & Hobson, W. C. (1982) · Experimental Biology and Medicine · doi:10.3181/00379727-169-41380 · Cited by 19 · see citing works
Plant, T. M., & Zorub, D. S. (1982) · Journal of Animal Science · doi:10.2527/1982.55supplement_ii43x · Cited by 17 · see citing works
Self-citationCryptorchid Rhesus Macaques: Long Term Studies on Changes in Gonadotropins and Gonadal Steroids*
Resko, J. A., Jackson, G. L., Huckins, C., Stadelman, H. L., & Spies, H. G. (1980) · Endocrinology · doi:10.1210/endo-107-4-1127 · Cited by 11 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Kisspeptins and Reproduction: Physiological Roles and Regulatory Mechanisms
Pinilla, L., Aguilar, E., Diéguez, C., Millar, R. P., & Tena‐Sempere, M. (2012) · Physiological Reviews · doi:10.1152/physrev.00037.2010 · Cited by 802 · see citing works
Neurobiological Mechanisms of the Onset of Puberty in Primates
Terasawa, E., & Fernandez, D. L. (2001) · Endocrine Reviews · doi:10.1210/edrv.22.1.0418 · Cited by 568 · see citing works
A role for synaptic plasticity in the adolescent development of executive function
Selemon, L. D. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.7 · Cited by 439 · see citing works
Mehlman, P. T., Higley, J. D., Faucher, I., Lilly, A. A., Taub, D. M., Vickers, J. H., Suomi, S. J., & Linnoila, M. (1994) · American Journal of Psychiatry · doi:10.1176/ajp.151.10.1485 · Cited by 375 · see citing works
Rosenberg, D. R., & Lewis, D. A. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903580306 · Cited by 319 · see citing works
Ramaswamy, S., Guerriero, K. A., Gibbs, R. B., & Plant, T. M. (2008) · Endocrinology · doi:10.1210/en.2008-0438 · Cited by 279 · see citing works
Self-citationRamaswamy, S., Seminara, S. B., Ali, B., Ciofi, P., Amin, N. A., & Plant, T. M. (2010) · Endocrinology · doi:10.1210/en.2010-0223 · Cited by 267 · see citing works
Self-citationThe neuroendocrine timing of puberty
Ebling, F. J. P. (2005) · Reproduction · doi:10.1530/rep.1.00367 · Cited by 250 · see citing works
Puberty in monkeys is triggered by chemical stimulation of the hypothalamus.
Plant, T. M., GAY, V. L., Marshall, G. R., & Arslan, M. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.7.2506 · Cited by 252 · see citing works
Self-citationMitsushima, D., HEI, D. L., & Terasawa, E. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.1.395 · Cited by 246 · see citing works
Somatotropic and Gonadotropic Axes Linkages in Infancy, Childhood, and the Puberty-Adult Transition
Veldhuis, J. D., Roemmich, J. N., Richmond, E. J., & Bowers, C. Y. (2006) · Endocrine Reviews · doi:10.1210/er.2005-0006 · Cited by 235 · see citing works
Seminara, S. B., DiPietro, M. J., Ramaswamy, S., Crowley, W. F., & Plant, T. M. (2006) · Endocrinology · doi:10.1210/en.2005-1550 · Cited by 232 · see citing works
Self-citationNeuroendocrine control of the onset of puberty
Plant, T. M. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.04.002 · Cited by 213 · see citing works
Self-citationA Role for Glucocorticoids in Stress-Impaired Reproduction: Beyond the Hypothalamus and Pituitary
Whirledge, S., & Cidlowski, J. A. (2013) · Endocrinology · doi:10.1210/en.2013-1652 · Cited by 209 · see citing works
Neurobiological mechanisms of puberty in higher primates
Plant, T. M. (2004) · Human Reproduction Update · doi:10.1093/humupd/dmh001 · Cited by 187 · see citing works
Self-citationRosenberg, D. R., & Lewis, D. A. (1994) · Biological Psychiatry · doi:10.1016/0006-3223(94)90610-6 · Cited by 174 · see citing works
Jahnukainen, K., Ehmcke, J., Hergenrother, S. D., & Schlatt, S. (2006) · Human Reproduction · doi:10.1093/humrep/del471 · Cited by 144 · see citing works
Ramaswamy, S., Seminara, S. B., & Plant, T. M. (2011) · Neuroendocrinology · doi:10.1159/000329045 · Cited by 132 · see citing works
Self-citationMarshall, G. R., & Plant, T. M. (1996) · Biology of Reproduction · doi:10.1095/biolreprod54.6.1192 · Cited by 125 · see citing works
Self-citationHypothalamic control of the male neonatal testosterone surge
Clarkson, J., & Herbison, A. E. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0115 · Cited by 123 · see citing works
Puberty in Nonhuman Primates and Humans
Plant, T. M., & Witchel, S. F. (2006) · Elsevier eBooks · doi:10.1016/b978-012515400-0/50045-2 · Cited by 123 · see citing works
Self-citationKeen, K. L., Burich, A. J., Mitsushima, D., Kasuya, E., & Terasawa, E. (1999) · Endocrinology · doi:10.1210/endo.140.11.7139 · Cited by 109 · see citing works
Control of luteinizing hormone-releasing hormone pulse generation in nonhuman primates
Terasawa, E. (1995) · Cellular and Molecular Neurobiology · doi:10.1007/bf02069563 · Cited by 105 · see citing works
Leptin, Nutrition, and Reproduction: Timing Is Everything
Hileman, S. M., Pierroz, D. D., & Flier, J. S. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.2.6490 · Cited by 103 · see citing works
Epigenetic regulation of puberty via Zinc finger protein-mediated transcriptional repression
Lomniczi, A., Wright, H., Castellano, J. M., Matagne, V., Toro, C. A., Ramaswamy, S., Plant, T. M., & Ojeda, S. R. (2015) · Nature Communications · doi:10.1038/ncomms10195 · Cited by 102 · see citing works
Self-citationKisspeptin and Puberty in Mammals
Terasawa, E., Guerriero, K. A., & Plant, T. M. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-6199-9_12 · Cited by 103 · see citing works
Self-citationSuter, K. J., Pohl, C. R., & Wilson, M. E. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.2.6371 · Cited by 109 · see citing works
Neuroendocrine Regulation of Puberty
Ojeda, S. R., & Bilger, M. (2000) · Humana Press eBooks · doi:10.1007/978-1-59259-707-9_12 · Cited by 93 · see citing works
Central Mechanism Controlling Pubertal Onset in Mammals: A Triggering Role of Kisspeptin
Uenoyama, Y., Inoue, N., Nakamura, S., & Tsukamura, H. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00312 · Cited by 89 · see citing works
Claypool, L. E., Kasuya, E., Saitoh, Y., Marzban, F., & Terasawa, E. (2000) · Endocrinology · doi:10.1210/endo.141.1.7231 · Cited by 82 · see citing works
de Rooij, D. G., van de Kant, H. J. G., Dol, R., Wagemaker, G., van Buul, P. P. W., van Duyn-Goedhart, A., de Jong, F. H., & Broerse, J. J. (2002) · Biology of Reproduction · doi:10.1095/biolreprod66.2.486 · Cited by 81 · see citing works
Neuroanatomical Framework of the Metabolic Control of Reproduction
Hill, J. W., & Elias, C. F. (2018) · Physiological Reviews · doi:10.1152/physrev.00033.2017 · Cited by 79 · see citing works
ENDOCRINOLOGY AND ADOLESCENCE: Deciphering puberty: novel partners, novel mechanisms
Tena‐Sempere, M. (2012) · European Journal of Endocrinology · doi:10.1530/eje-12-0669 · Cited by 76 · see citing works
Harris, G. C., & Levine, J. E. (2002) · Endocrinology · doi:10.1210/en.2002-220767 · Cited by 76 · see citing works
Puberty as a life history transition
Ellison, P. T., Reiches, M. W., Shattuck-Faegre, H., Breakey, A., Konecna, M., Urlacher, S., & Wobber, V. (2012) · Annals of Human Biology · doi:10.3109/03014460.2012.693199 · Cited by 73 · see citing works
Metabolic control of female puberty: potential therapeutic targets
Castellano, J. M., & Tena‐Sempere, M. (2016) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2016.1212015 · Cited by 65 · see citing works
The role of testosterone in spermatogenesis
O’Donnell, L., & McLachlan, R. I. (2012) · Cambridge University Press eBooks · doi:10.1017/cbo9781139003353.007 · Cited by 64 · see citing works
Neuroendocrine Regulation of Puberty
Ojeda, S. R., & Terasawa, E. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50077-9 · Cited by 62 · see citing works
The neurobiology of reproductive development
Ebling, F. J. P., & Cronin, A. S. (2000) · Neuroreport · doi:10.1097/00001756-200011090-00002 · Cited by 61 · see citing works
Suter, K. J., Pohl, C. R., & Plant, T. M. (1998) · Endocrinology · doi:10.1210/endo.139.6.6055 · Cited by 61 · see citing works
Self-citationDubey, A. K., Cameron, J. L., Steiner, R. A., & Plant, T. M. (1986) · Endocrinology · doi:10.1210/endo-118-2-518 · Cited by 60 · see citing works
Self-citationRecent Discoveries on the Control of Gonadotrophin‐Releasing Hormone Neurones in Nonhuman Primates
Terasawa, E., Kurian, J. R., Guerriero, K. A., Kenealy, B. P., Hutz, E. D., & Keen, K. L. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.02027.x · Cited by 58 · see citing works
Ramaswamy, S., Plant, T. M., & Marshall, G. R. (2000) · Biology of Reproduction · doi:10.1095/biolreprod63.1.82 · Cited by 59 · see citing works
Self-citationSexual Differentiation of the Brain Requires Perinatal Kisspeptin-GnRH Neuron Signaling
Clarkson, J., Busby, E. R., Kirilov, M., Schütz, G., Sherwood, N. M., & Herbison, A. E. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3061-14.2014 · Cited by 57 · see citing works
Lowry, C. A., Richardson, C., Zoeller, T. R., Miller, L. J., Muske, L. E., & Moore, F. L. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970818)385:1 · Cited by 56 · see citing works
Self-citationBODY SIZE, SPERM COMPETITION, AND DETERMINANTS OF REPRODUCTIVE SUCCESS IN MALE SAVANNA BABOONS
Bercovitch, F. B. (1989) · Evolution · doi:10.1111/j.1558-5646.1989.tb02600.x · Cited by 54 · see citing works
Adrenarche in nonhuman primates: the evidence for it and the need to redefine it
Conley, A. J., Bernstein, R. M., & Nguyen, A. D. (2012) · Journal of Endocrinology · doi:10.1530/joe-11-0467 · Cited by 53 · see citing works
Testicular Xenografts: A Novel Approach to Study Cytotoxic Damage in Juvenile Primate Testis
Jahnukainen, K., Ehmcke, J., & Schlatt, S. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3754 · Cited by 51 · see citing works
Majumdar, S. S., Sarda, K., Bhattacharya, I., & Plant, T. M. (2012) · Human Reproduction · doi:10.1093/humrep/des184 · Cited by 50 · see citing works
Self-citationKasuya, E., Nyberg, C. L., Mogi, K., & Terasawa, E. (1999) · Endocrinology · doi:10.1210/endo.140.2.6574 · Cited by 50 · see citing works
Spergel, D. J. (2007) · Endocrinology · doi:10.1210/en.2006-1693 · Cited by 48 · see citing works
Neuroendocrine mechanisms that delay and initiate puberty in higher primates
Plant, T. M., & Shahab, M. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00924-1 · Cited by 48 · see citing works
Self-citationGuerriero, K. A., Keen, K. L., & Terasawa, E. (2012) · Endocrinology · doi:10.1210/en.2011-1701 · Cited by 46 · see citing works
Circulating Concentrations of Dimeric Inhibin A and B in the Male Rhesus Monkey (Macaca mulatta)1
Plant, T. M., Padmanabhan, V., Ramaswamy, S., McConnell, D. S., Winters, S. J., Groome, N. P., MIDGLEY, A. R., & McNeilly, A. S. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.8.4164 · Cited by 46 · see citing works
Self-citationHendrickx, A. G., & Dukelow, W. R. (1995) · Elsevier eBooks · doi:10.1016/b978-012088661-6/50011-9 · Cited by 43 · see citing works
Neurokinin B signalling in the human reproductive axis
Topaloglu, A. K., & Semple, R. K. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.07.014 · Cited by 41 · see citing works
Matsumoto, A. M., Karpas, A. E., Southworth, M. B., Dorsa, D. M., & Bremner, W. J. (1986) · Endocrinology · doi:10.1210/endo-119-1-362 · Cited by 41 · see citing works
Majumdar, S. S., Winters, S. J., & Plant, T. M. (1997) · Endocrinology · doi:10.1210/en.138.4.1363 · Cited by 41 · see citing works
Self-citationTestis size, epididymis weight, and sperm competition in rhesus macaques
Bercovitch, F. B., & Rodriguez, J. F. (1993) · American Journal of Primatology · doi:10.1002/ajp.1350300208 · Cited by 40 · see citing works
Puberty in Non-human Primates and Man
Plant, T. M., Terasawa, E., & Witchel, S. F. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00032-6 · Cited by 38 · see citing works
Self-citationChandrashekar, V., & Bartke, A. (1988) · Steroids · doi:10.1016/0039-128x(88)90052-9 · Cited by 38 · see citing works
Hormonal Control of Spermatogenesis
Weinbauer, G. F., & Nieschlag, E. (1993) · Elsevier eBooks · doi:10.1016/b978-0-08-091764-1.50008-8 · Cited by 37 · see citing works
Medhamurthy, R., ABEYAWARDENE, S. A., Culler, M. D., Negro-Vilar, A. F., & Plant, T. M. (1990) · Endocrinology · doi:10.1210/endo-126-4-2116 · Cited by 37 · see citing works
Self-citationThe Changes They are A-Timed: Metabolism, Endogenous Clocks, and the Timing of Puberty
Tolson, K. P., & Chappell, P. E. (2012) · Frontiers in Endocrinology · doi:10.3389/fendo.2012.00045 · Cited by 36 · see citing works
Fraser, M. O., Pohl, C. R., & Plant, T. M. (1989) · Biology of Reproduction · doi:10.1095/biolreprod40.5.972 · Cited by 36 · see citing works
Self-citationHuhtaniemi, I. T., Dunkel, L., & Perheentupa, J. (1986) · Pediatric Research · doi:10.1203/00006450-198612000-00028 · Cited by 35 · see citing works
Hypothalamic mechanism of the onset of puberty
Terasawa, E. (1999) · Current Opinion in Endocrinology & Diabetes · doi:10.1097/00060793-199902000-00008 · Cited by 35 · see citing works
Simorangkir, D. R., Ramaswamy, S., Marshall, G. R., Roslund, R. M., & Plant, T. M. (2012) · Reproduction · doi:10.1530/rep-11-0411 · Cited by 34 · see citing works
Self-citationNeuroendocrine Control of Gonadotropin Secretion
Goodman, R. L. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00033-8 · Cited by 34 · see citing works
Vician, L. J., Adams, L. A., Clifton, D. K., & Steiner, R. A. (1991) · Molecular and Cellular Neuroscience · doi:10.1016/1044-7431(91)90037-o · Cited by 34 · see citing works
Shetty, G., Mitchell, J., Meyer, J. M., Wu, Z., Lam, T., Phan, T., Zhang, J., Hill, L., Tailor, R. C., Peters, K. A., et al. (2020) · Andrology · doi:10.1111/andr.12807 · Cited by 33 · see citing works
Barker-Gibb, M. L., Sahu, A., Pohl, C. R., & Plant, T. M. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020784 · Cited by 33 · see citing works
Self-citationMedhamurthy, R., GAY, V. L., & Plant, T. M. (1990) · Endocrinology · doi:10.1210/endo-126-2-1036 · Cited by 31 · see citing works
Self-citationRamaswamy, S., Dwarki, K., Ali, B. F., Gibbs, R. B., & Plant, T. M. (2013) · Endocrinology · doi:10.1210/en.2012-2154 · Cited by 30 · see citing works
Self-citationKNDy neuron as a gatekeeper of puberty onset
Uenoyama, Y., Tsukamura, H., & Maeda, K. (2014) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.12398 · Cited by 29 · see citing works
Gonadectomy negatively impacts social behavior of adolescent male primates
Richards, A. B., Morris, R. W., Ward, S. E., Schmitz, S., Rothmond, D. A., Noble, P. L., Woodward, R. A., Winslow, J., & Weickert, C. S. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.03.021 · Cited by 29 · see citing works
Conley, A. J., Moeller, B. C., Nguyen, A. D., Stanley, S. D., Plant, T. M., & Abbott, D. H. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2010.12.022 · Cited by 29 · see citing works
Self-citationStreet, M. E., Ponzi, D., Renati, R., Petraroli, M., D’Alvano, T., Lattanzi, C., Ferrari, V. D., Rollo, D., & Stagi, S. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1149417 · Cited by 32 · see citing works
Kalil, B., Ramaswamy, S., & Plant, T. M. (2015) · Neuroendocrinology · doi:10.1159/000442420 · Cited by 27 · see citing works
Self-citationRole of Kisspeptin and Neurokinin B Signaling in Male Rhesus Monkey Puberty
Garcia, J. P., Keen, K. L., Kenealy, B. P., Seminara, S. B., & Terasawa, E. (2018) · Endocrinology · doi:10.1210/en.2018-00443 · Cited by 28 · see citing works
Sexual Dimorphism in Kisspeptin Signaling
Lee, E. B., Dilower, I., Marsh, C. A., Wolfe, M. W., Masumi, S., Upadhyaya, S., & Rumi, M. A. K. (2022) · Cells · doi:10.3390/cells11071146 · Cited by 26 · see citing works
Neural mechanisms underlying the pubertal increase in LHRH release in the rhesus monkey
Richter, T. A., & Terasawa, E. (2001) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(01)00442-8 · Cited by 24 · see citing works
Plant, T. M., & Zorub, D. S. (1986) · Endocrinology · doi:10.1210/endo-118-1-227 · Cited by 24 · see citing works
Self-citationKenealy, B. P., Keen, K. L., Kapoor, A., & Terasawa, E. (2015) · Endocrinology · doi:10.1210/en.2015-1770 · Cited by 23 · see citing works
Mann, D. R., & Plant, T. M. (2010) · Brain Research · doi:10.1016/j.brainres.2010.09.082 · Cited by 23 · see citing works
Self-citationJahnukainen, K., Ehmcke, J., Nurmio, M., & Schlatt, S. (2007) · Endocrinology · doi:10.1210/en.2007-0809 · Cited by 23 · see citing works
Winters, S. J., & Plant, T. M. (1999) · Endocrinology · doi:10.1210/endo.140.12.7167 · Cited by 23 · see citing works
Self-citationMcCosh, R. B., Szeligo, B. M., Bedenbaugh, M. N., Lopez, J. A., Hardy, S. L., Hileman, S. M., Lehman, M. N., & Goodman, R. L. (2017) · Endocrinology · doi:10.1210/en.2017-00075 · Cited by 21 · see citing works
Ramaswamy, S., Razack, B. S., Roslund, R. M., Suzuki, H., Marshall, G. R., Rajkovic, A., & Plant, T. M. (2013) · Molecular Human Reproduction · doi:10.1093/molehr/gat093 · Cited by 20 · see citing works
Self-citationThe mechanism underlying the pubertal increase in pulsatile GnRH release in primates
Terasawa, E. (2022) · Journal of Neuroendocrinology · doi:10.1111/jne.13119 · Cited by 19 · see citing works
Sisk, C. L. (1987) · Biology of Reproduction · doi:10.1095/biolreprod37.1.73 · Cited by 19 · see citing works
Adrenal androgen concentrations increase during infancy in male rhesus macaques (Macaca mulatta)
Conley, A. J., Plant, T. M., Abbott, D. H., Moeller, B. C., & Stanley, S. D. (2011) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00200.2011 · Cited by 18 · see citing works
Self-citationVerhagen, I., Ramaswamy, S., Teerds, K. J., Keijer, J., & Plant, T. M. (2014) · Andrology · doi:10.1111/andr.275 · Cited by 16 · see citing works
Self-citationRole of Kisspeptin and NKB in Puberty in Nonhuman Primates: Sex Differences
Garcia, J. P., Keen, K. L., Seminara, S. B., & Terasawa, E. (2019) · Seminars in Reproductive Medicine · doi:10.1055/s-0039-3400253 · Cited by 16 · see citing works
Fraser, M. O., Arslan, M., & Plant, T. M. (2004) · Pediatric Research · doi:10.1203/01.pdr.0000148063.68338.a0 · Cited by 16 · see citing works
Self-citationWilson, M. E., Fisher, J., & Chikazawa, K. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0148 · Cited by 16 · see citing works
Suter, K. J., Pohl, C. R., & Plant, T. M. (1999) · Journal of Endocrinology · doi:10.1677/joe.0.1600035 · Cited by 16 · see citing works
Self-citationNeuroendocrine control processes
Reiter, E. O. (1987) · Journal of Adolescent Health Care · doi:10.1016/0197-0070(87)90049-0 · Cited by 16 · see citing works
The role of testosterone in spermatogenesis
Weinbauer, G. F., & Nieschlag, E. (1990) · Springer eBooks · doi:10.1007/978-3-662-00814-0_2 · Cited by 16 · see citing works
Neuroendocrine mechanisms of puberty in non–human primates
Terasawa, E., & Garcia, J. P. (2020) · Current Opinion in Endocrine and Metabolic Research · doi:10.1016/j.coemr.2020.07.008 · Cited by 14 · see citing works
- Authors
- PLANT, T. M.
- Affiliations
- University of Pittsburgh (US)
- Corresponding author
- PLANT, T. M.
- ORCID
- PLANT, T. M.
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 1985-04
- Volume
- 116
- Issue
- 4
- Pages
- 1341-1350
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- OpenAlex
- W2007967271
- Cited by
- 128
- References
- 38
- Citations by year
- 2025: 1 · 2023: 1 · 2022: 2 · 2021: 2 · 2020: 2 · 2019: 2 · 2018: 3 · 2017: 1 · 2016: 4 · 2015: 6 · 2014: 6 · 2013: 5 · 2012: 11
- FWCI
- 3.15
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Pittsburgh
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD 08610, HD 13254)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Keywords
- gonadotropin secretion, luteinizing hormone, follicle-stimulating hormone, androgens, pubertal development, hypothalamic-pituitary-testicular axis, orchiectomy, rhesus monkeys, ontogeny, plasma prolactin, testicular volume, nocturnal hormone secretion, infant development, prepubertal development
- MeSH terms
- Androgens, Animals, Animals, Newborn, Circadian Rhythm, Gonadotropins, Macaca, Macaca mulatta, Male, Prolactin, Sexual Maturation, Testis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review