The organizing actions of adolescent gonadal steroid hormones on brain and behavioral development

Adkins-Regan, 1989, Sexual differentiation of reproductive behavior in pigs: defeminizing effects of prepubertal estradiol, Horm. Behav., 23, 290, 10.1016/0018-506X(89)90068-8

Ahmed, 2008, Pubertal hormones modulate the addition of new cells to sexually dimorphic brain regions, Nat. Neurosci., 11, 995, 10.1038/nn.2178

Andersen, 1997, Sex differences in dopamine receptor overproduction and elimination, Neuroreport, 8, 1495, 10.1097/00001756-199704140-00034

Andersen, 2003, Trajectories of brain development: point of vulnerability or window of opportunity, Neurosci. Biobehav. Rev., 27, 3, 10.1016/S0149-7634(03)00005-8

Andrews, 1981, Development of estradiol-positive feedback on luteinizing hormone release in the female rat: a quantitative study, Endocrinology, 109, 1404, 10.1210/endo-109-5-1404

Arnold, 1985, Organizational and activational effects of sex steroids on brain and behavior: a reanalysis, Horm. Behav., 19, 469, 10.1016/0018-506X(85)90042-X

Bakker, 2008, Role for estradiol in female-typical brain and behavioral sexual differentiation, Front. Neuroendocrinol., 29, 1, 10.1016/j.yfrne.2007.06.001

Bakker, 2002, The aromatase knock-out mouse provides new evidence that estradiol is required during development in the female for the expression of sociosexual behaviors in adulthood, J. Neurosci., 22, 9104, 10.1523/JNEUROSCI.22-20-09104.2002

Baum, 1990, Steroidal control of behavioural, neuroendocrine and brain sexual differentiation: studies in a carnivore the ferret, J. Neuroendocrinol., 2, 401, 10.1111/j.1365-2826.1990.tb00425.x

Bell, 2009, The role of the medial prefrontal cortex in the play fighting of rats, Behav. Neurosci., 123, 1158, 10.1037/a0017617

Beltz, 2013, Cognitive effects of variations in pubertal timing: is puberty a period of brain organization for human sex-typed cognition?, Horm. Behav., 63, 823, 10.1016/j.yhbeh.2013.04.002

Berenbaum, 2011, Sexual differentiation of human behavior: effects of prenatal and pubertal organizational hormones, Front. Neuroendocrinol., 32, 183, 10.1016/j.yfrne.2011.03.001

Bloch, 1995, Prepubertal testosterone treatment of neonatally gonadectomized male rats: defeminization and masculinization of behavioral and endocrine function in adulthood, Neurosci. Biobehav. Rev., 19, 187, 10.1016/0149-7634(94)00064-8

Bloch, 1995, Prepubertal testosterone treatment of female rats: defeminization of behavioral and endocrine function in adulthood, Neurosci. Biobehav. Rev., 19, 177, 10.1016/0149-7634(95)00065-M

Brock, 2011, The development of female sexual behavior requires prepubertal estradiol, J. Neurosci., 31, 5574, 10.1523/JNEUROSCI.0209-11.2011

Brown, 2015, Peri-pubertal exposure to testicular hormones organizes response to novel environments and social behaviour in adult male rats, Horm. Behav., 73, 135, 10.1016/j.yhbeh.2015.07.003

Chung, 2002, Sexual differentiation of the bed nucleus of the stria terminalis in humans may extend into adulthood, J. Neurosci., 22, 1027, 10.1523/JNEUROSCI.22-03-01027.2002

Clemens, 1978, Feminine sexual behavior in rats enhanced by prenatal inhibition of androgen aromatization, Horm. Behav., 11, 190, 10.1016/0018-506X(78)90048-X

Coniglio, 1973, Hormonal specificity in the suppression of sexual receptivity of the female golden hamster, J. Endocrinol., 57, 55, 10.1677/joe.0.0570055

Cooke, 2007, Morphological sex differences and laterality in the prepubertal medial amygdala, J. Comp. Neurol., 501, 904, 10.1002/cne.21281

Corbier, 1985, Sexual differentiation of positive feedback: effect of hour of castration at birth on estradiol-induced luteinizing hormone secretion in immature male rats, Endocrinology, 116, 142, 10.1210/endo-116-1-142

D'Occhio, 1980, Effects of androgenic and oestrogenic hormones on mating behaviour in rams castrated before and after puberty, J. Endocrinol., 86, 403, 10.1677/joe.0.0860403

Davis, 1996, Structural sexual dimorphisms in the anteroventral periventricular nucleus of the rat hypothalamus are sensitive to gonadal steroids perinatally, but develop peripubertally, Neuroendocrinology, 63, 142, 10.1159/000126950

Davis, 2010, Lesions of the medial prefrontal cortex cause maladaptive sexual behavior in male rats, Biol. Psychiatry, 67, 1199, 10.1016/j.biopsych.2009.12.029

De Lorme, 2013, Pubertal testosterone programs context-appropriate agonistic behavior and associated neural activation patterns in male Syrian hamsters, Physiol. Behav., 112–113, 1, 10.1016/j.physbeh.2013.02.003

de Jonge, 1988, Sexual behavior and sexual orientation of the female rat after hormonal treatment during various stages of development, Horm. Behav., 22, 100, 10.1016/0018-506X(88)90034-7

Dixon, 1993, Sexual and aggressive behavior of adult male marmosets (Callithrix jacchus) castrated neonatally, prepubertally, or in adulthood, Physiol. Behav., 54, 301, 10.1016/0031-9384(93)90115-V

Eckenhoff, 1988, Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life-span of the rhesus monkey, J. Neurosci., 8, 2729, 10.1523/JNEUROSCI.08-08-02729.1988

Eichmann, 1999, Organization of territorial marking behavior by testosterone during puberty in male tree shrews, Physiol. Behav., 65, 785, 10.1016/S0031-9384(98)00230-3

Epple, 1990, Copulatory behavior of Adult Tamarins (Saguinus fuscicollis) castrated as neonates or juveniles: effect of testosterone treatment, Horm. Behav., 24, 470, 10.1016/0018-506X(90)90036-W

Ferris, 1987, Scent marking and the maintenance of dominant/subordinate status in male golden hamsters, Physiol. Behav., 40, 661, 10.1016/0031-9384(87)90114-4

Field, 2008, The brain as the engine of sex differences in the organization of movement in rats, Arch. Sex. Behav., 37, 30, 10.1007/s10508-007-9270-4

Field, 2004, Neonatal and pubertal, but not adult, ovarian steroids are necessary for the development of female-typical patterns of dodging to protect a food item, Behav. Neurosci., 118, 1293, 10.1037/0735-7044.118.6.1293

File, 1978, Can social interaction be used to measure anxiety?, Br. J. Pharmacol., 62, 19, 10.1111/j.1476-5381.1978.tb07001.x

File, 1985, Animal models for predicting clinical efficacy of anxiolytic drugs: social behaviour, Neuropsychobiology, 13, 55, 10.1159/000118163

Ford, 1990, Differentiation of sexual behaviour in pigs, J. Reprod. Fertil. Suppl., 40, 311

Gogan, 1980, Effect of neonatal administration of steroids or gonadectomy upon oestradiol-induced luteinizing hormone release in rats of both sexes, J. Endocrinol., 85, 69, 10.1677/joe.0.0850069

Gorski, 1985, The 13th J.A.F. Stevenson memorial lecture. Sexual differentiation of the brain: possible mechanisms and implications, Can. J. Physiol. Pharmacol., 63, 577, 10.1139/y85-098

Gotz, 1976, Sex hormone-dependent brain maturation and sexual behaviour in rats, Endokrinologie, 68, 275

Gurney, 1980, Hormone induced sexual differentiation of brain and behavior in zebra finches, Science, 208, 1380, 10.1126/science.208.4450.1380

He, 2007, Neurogenesis decreases during brain maturation from adolescence to adulthood, Pharmacol. Biochem. Behav., 86, 327, 10.1016/j.pbb.2006.11.003

Huck, 1988, Social-dominance and reproductive success in pregnant and lactating golden-hamsters (Mesocricetus-auratus) under seminatural conditions, Physiol. Behav., 44, 313, 10.1016/0031-9384(88)90031-5

Huttenlocher, 1997, Regional differences in synaptogenesis in human cerebral cortex, J. Comp. Neurol., 387, 167, 10.1002/(SICI)1096-9861(19971020)387:2<167::AID-CNE1>3.0.CO;2-Z

Johnson, 2012, Astrocytes in the rat medial amygdala are responsive to adult androgens, J. Comp. Neurol., 520, 2531, 10.1002/cne.23061

Johnson, 2013, Androgen receptors mediate masculinization of astrocytes in the rat posterodorsal medial amygdala during puberty, J. Comp. Neurol., 521, 2298, 10.1002/cne.23286

Johnston, 1970

Juraska, 2016, Pubertal onset as a critical transition for neural development and cognition, Brain Res.

Kellogg, 1999, Brain androgen-inducible aromatase is critical for adolescent organization of environment-specific social interaction in male rats, Horm. Behav., 35, 155, 10.1006/hbeh.1998.1508

Kercmar, 2014, Gonadectomy prior to puberty decreases normal parental behavior in adult mice, Horm. Behav., 66, 667, 10.1016/j.yhbeh.2014.09.007

Koss, 2014, Dendritic remodeling in the adolescent medial prefrontal cortex and the basolateral amygdala of male and female rats, Synapse, 68, 61, 10.1002/syn.21716

Koss, 2015, Gonadectomy before puberty increases the number of neurons and glia in the medial prefrontal cortex of female, but not male, rats, Dev. Psychobiol., 57, 305, 10.1002/dev.21290

Larsson, 1976, Effects of estrone, estradiol and estriol combined with dihydrotestosterone on mounting and lordosis behavior in castrated male rats, Horm. Behav., 7, 379, 10.1016/0018-506X(76)90009-X

Larsson, 1967, Testicular hormone and developmental changes in mating behavior of the male rat, J. Comp. Physiol. Psychol., 63, 223, 10.1037/h0024358

Lenroot, 2006, Brain development in children and adolescents: insights from anatomical magnetic resonance imaging, Neurosci. Biobehav. Rev., 30, 718, 10.1016/j.neubiorev.2006.06.001

Lumia, 1977, Effects of androgen on marking and aggressive behavior of neonatally and prepubertally bulbectomized and castrated male gerbils, J. Comp. Physiol. Psychol., 91, 1377, 10.1037/h0077410

Markham, 2007, Neuron number decreases in the rat ventral, but not dorsal, medial prefrontal cortex between adolescence and adulthood, Neuroscience, 144, 961, 10.1016/j.neuroscience.2006.10.015

Meek, 1997, Actions of testosterone in prepubertal and postpubertal male hamsters: dissociation of effects on reproductive behavior and brain androgen receptor immunoreactivity, Horm. Behav., 31, 75, 10.1006/hbeh.1997.1371

Miller, 1977, Physical and behavioral aspects of sexual maturation in male golden hamsters, J. Comp. Physiol. Psychol., 91, 245, 10.1037/h0077315

Mohr, 2013, Pubertally born neurons and glia are functionally integrated into limbic and hypothalamic circuits of the male Syrian hamster, Proc. Natl. Acad. Sci. U. S. A., 110, 4792, 10.1073/pnas.1219443110

Morris, 2008, Sexual dimorphism and steroid responsiveness of the posterodorsal medial amygdala in adult mice, Brain Res., 1190, 115, 10.1016/j.brainres.2007.11.005

Newman, 1999, The medial extended amygdala in male reproductive behavior: a node in the mammalian social behavior network, Ann. N. Y. Acad. Sci., 877, 242, 10.1111/j.1749-6632.1999.tb09271.x

Nunez, 2001, Cell death in the development of the posterior cortex in male and female rats, J. Comp. Neurol., 436, 32, 10.1002/cne.1051

Nunez, 2002, Ovarian hormones after postnatal day 20 reduce neuron number in the rat primary visual cortex, J. Neurobiol., 52, 312, 10.1002/neu.10092

Paup, 1972, Masculinization of the female golden hamster by neonatal treatment with androgen or estrogen, Horm. Behav., 3, 123, 10.1016/0018-506X(72)90014-1

Payne, 1970, Agonistic behaviour between pairs of hamsters of same and opposite sex in a neutral observation area, Behaviour, 36

Pellis, 2002, Sex differences in play fighting revisited: traditional and nontraditional mechanisms of sexual differentiation in rats, Arch. Sex. Behav., 31, 17, 10.1023/A:1014070916047

Perrin, 2008, Growth of white matter in the adolescent brain: role of testosterone and androgen receptor, J. Neurosci., 28, 9519, 10.1523/JNEUROSCI.1212-08.2008

Phoenix, 1959, Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig, Endocrinology, 65, 369, 10.1210/endo-65-3-369

Pinos, 2001, The development of sex differences in the locus coeruleus of the rat, Brain Res. Bull., 56, 73, 10.1016/S0361-9230(01)00540-8

Primus, 1989, Pubertal-related changes influence the development of environment-related social interaction in the male rat, Dev. Psychobiol., 22, 633, 10.1002/dev.420220608

Primus, 1990, Gonadal hormones during puberty organize environment-related social interaction in the male rat, Horm. Behav., 24, 311, 10.1016/0018-506X(90)90012-M

Rankin, 2003, Postnatal neurogenesis in the vasopressin and oxytocin-containing nucleus of the pig hypothalamus, Brain Res., 971, 189, 10.1016/S0006-8993(03)02350-3

Romeo, 2001, Dihydrotestosterone activates sexual behavior in adult male hamsters but not in juveniles, Physiol. Behav., 73, 579, 10.1016/S0031-9384(01)00499-1

Romeo, 2002, Estradiol induces hypothalamic progesterone receptors, but does not activate mating behavior in male hamsters (Mesocricetus auratus) before puberty, Behav. Neurosci., 116, 198, 10.1037/0735-7044.116.2.198

Schulz, 2006, Pubertal hormones, the adolescent brain, and the maturation of social behaviors: lessons from the Syrian hamster, Mol. Cell. Endocrinol., 254-255, 120, 10.1016/j.mce.2006.04.025

Schulz, 2006, Testicular hormone exposure during adolescence organizes flank-marking behavior and vasopressin receptor binding in the lateral septum, Horm. Behav., 50, 477, 10.1016/j.yhbeh.2006.06.006

Schulz, 2009, Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence, Horm. Behav., 55, 597, 10.1016/j.yhbeh.2009.03.010

Shrenker, 1985, The role of postnatal testosterone in the development of sexually dimorphic behaviors in DBA/1Bg mice, Physiol. Behav., 35, 757, 10.1016/0031-9384(85)90408-1

Simerly, 2002, Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain, Annu. Rev. Neurosci., 25, 507, 10.1146/annurev.neuro.25.112701.142745

Sisk, 1983, Developmental time course of pubertal and photoperiodic changes in testosterone negative feedback on gonadotropin secretion in the golden hamster, Endocrinology, 112, 1208, 10.1210/endo-112-4-1208

Sisk, 2005, Pubertal hormones organize the adolescent brain and behavior, Front. Neuroendocrinol., 26, 163, 10.1016/j.yfrne.2005.10.003

Sisk, 2003, Puberty: a finishing school for male social behavior, Ann. N. Y. Acad. Sci., 1007, 189, 10.1196/annals.1286.019

Smith, 1998, Mechanisms underlying the absence of the pubertal shift in the playful defense of female rats, Dev. Psychobiol., 33, 147, 10.1002/(SICI)1098-2302(199809)33:2<147::AID-DEV5>3.0.CO;2-J

Sodersten, 1973, Estrogen-activated sexual behavior in male rats, Horm. Behav., 4, 247, 10.1016/0018-506X(73)90009-3

Sowell, 2004, Mapping changes in the human cortex throughout the span of life, Neuroscientist, 10, 372, 10.1177/1073858404263960

Spear, 2000, The adolescent brain and age-related behavioral manifestations, Neurosci. Biobehav. Rev., 24, 417, 10.1016/S0149-7634(00)00014-2

Steinberg, 2005, Cognitive and affective development in adolescence, Trends Cogn. Sci., 9, 69, 10.1016/j.tics.2004.12.005

Swithers, 2008, Influence of ovarian hormones on development of ingestive responding to alterations in fatty acid oxidation in female rats, Horm. Behav., 54, 471, 10.1016/j.yhbeh.2008.05.009

Vomachka, 1979, The development of gonadotropin and steroid hormone patterns in male and female hamsters from birth to puberty, Endocrinology, 105, 960, 10.1210/endo-105-4-960

Wallen, 2002, Masculinization and defeminization in altricial and precocial mammals: comparative aspects of steroid hormone action, vol. 4, 385

Wang, 2011, Bidirectional control of social hierarchy by synaptic efficacy in medial prefrontal cortex, Science, 334, 693, 10.1126/science.1209951

Ward, 1985, Sexual behavior differentiation: effects of prenatal manipulations in rats, vol. 7, 77

Willing, 2015, The timing of neuronal loss across adolescence in the medial prefrontal cortex of male and female rats, Neuroscience, 301, 268, 10.1016/j.neuroscience.2015.05.073

Zehr, 2006, Dendritic pruning of the medial amygdala during pubertal development of the male Syrian hamster, J. Neurobiol., 66, 578, 10.1002/neu.20251