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Cited by 279Stress Responses and CortisolHypothalamic control of reproductive hormonesNeuroendocrine regulation and behavior

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Puberty and adolescence as a time of vulnerability to stressors that alter neurobehavioral processes

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Holder, Mary K., Blaustein, Jeffrey D.·2014·Frontiers in Neuroendocrinology
DOI 10.1016/j.yfrne.2013.10.004PMC PMC3946873
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Abstract

Puberty and adolescence are major life transitions during which an individual's physiology and behavior changes from that of a juvenile to that of an adult. Here we review studies documenting the effects of stressors during pubertal and adolescent development on the adult brain and behavior. The experience of complex or compound stressors during puberty/adolescence generally increases stress reactivity, increases anxiety and depression, and decreases cognitive performance in adulthood. These behavioral changes correlate with decreased hippocampal volumes and alterations in neural plasticity. Moreover, stressful experiences during puberty disrupt behavioral responses to gonadal hormones both in sexual performance and on cognition and emotionality. These behavioral changes correlate with altered estrogen receptor densities in some estrogen-concentrating brain areas, suggesting a remodeling of the brain's response to hormones. A hypothesis is presented that activation of the immune system results in chronic neuroinflammation that may mediate the alterations of hormone-modulated behaviors in adulthood.

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Research works printed but not linked: 279

  1. Aloisi, 2001, Immune function of microglia, Glia, 36, 165, 10.1002/glia.1106 · DOI
  2. Altemus, 1997, Neonatal hippocampal damage in rats: long-term spatial memory deficits and associations with magnitude of hippocampal damage, Hippocampus, 7, 403, 10.1002/(SICI)1098-1063(1997)7:4<403::AID-HIPO6>3.0.CO;2-J · DOI
  3. Andersen, 2004, Delayed effects of early stress on hippocampal development, Neuropsychopharmacology, 29, 1988, 10.1038/sj.npp.1300528 · DOI
  4. Angold, 2006, Puberty and depression, Child Adolesc. Psychiatric Clin. North Am., 15, 919, 10.1016/j.chc.2006.05.013 · DOI · Paper page
  5. Anisman, 2009, Cascading effects of stressors and inflammatory immune system activation: implications for major depressive disorder, J. Psychiatry Neurosci., 34, 4
  6. Araki, 1975, Immunoreactive gonadotropin-releasing hormone (Gn-RH) during maturation in the rat: ontogeny of regional hypothalamic differences, Endocrinology, 97, 693, 10.1210/endo-97-3-693 · DOI
  7. Arnett, 1996, Sensation seeking, aggressiveness, and adolescent reckless behavior, Personality Individ. Differ., 20, 693, 10.1016/0191-8869(96)00027-X · DOI
  8. Astbury, J., 2001. Gender Disparities in Mental Health. Mental Health. Ministerial Round Tables 2001, 54th World Health Assemble. WHO, Geneva, Switzerland, 2001, pp. 73–92.
  9. Avital, 2005, Exposure to juvenile stress exacerbates the behavioural consequences of exposure to stress in the adult rat, Int. J. Neuropsychopharmacol., 8, 163, 10.1017/S1461145704004808 · DOI
  10. Avital, 2006, Effects of early-life stress on behavior and neurosteroid levels in the rat hypothalamus and entorhinal cortex, Brain Res. Bull., 68, 419, 10.1016/j.brainresbull.2005.09.015 · DOI
  11. Barnea-Goraly, 2005, White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study, Cereb. Cortex, 15, 1848, 10.1093/cercor/bhi062 · DOI · Paper page
  12. Bauer, 2007, The neuropoietic cytokine family in development, plasticity, disease and injury, Nat. Rev. Neurosci., 8, 221, 10.1038/nrn2054 · DOI
  13. Bazak, 2009, Pre-pubertal stress exposure affects adult behavioral response in association with changes in circulating corticosterone and brain-derived neurotrophic factor, Psychoneuroendocrinology, 34, 844, 10.1016/j.psyneuen.2008.12.018 · DOI
  14. Bekku, 2005, Animal model of menopausal depressive-like state in female mice: prolongation of immobility time in the forced swimming test following ovariectomy, Psychopharmacology, 183, 300, 10.1007/s00213-005-0179-0 · DOI
  15. Bekman, 2010, Affective and personality risk and cognitive mediators of initial adolescent alcohol use, J. Stud. Alcohol Drugs, 71, 570, 10.15288/jsad.2010.71.570 · DOI
  16. Beltran-Campos, 2011, Increase of mushroom spine density in CA1 apical dendrites produced by water maze training is prevented by ovariectomy, Brain Res., 1369, 119, 10.1016/j.brainres.2010.10.105 · DOI
  17. Benes, 1994, Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood, Arch. Gen. Psychiatry, 51, 477, 10.1001/archpsyc.1994.03950060041004 · DOI · Paper page
  18. Benes, 2000, Convergence and plasticity of monoaminergic systems in the medial prefrontal cortex during the postnatal period: implications for the development of psychopathology, Cereb. Cortex, 10, 1014, 10.1093/cercor/10.10.1014 · DOI · Paper page
  19. Bernardi, 1989, Influence of ovariectomy, estradiol and progesterone on the behavior of mice in an experimental model of depression, Physiol. Behav., 45, 1067, 10.1016/0031-9384(89)90238-2 · DOI
  20. Bilbo, 2011, A lifespan approach to neuroinflammatory and cognitive disorders: a critical role for glia, J. Neuroimmune Pharmacol.
  21. Blaustein, 2008, Neuroendocrine regulation of feminine sexual behavior: lessons from rodent models and thoughts about humans, Ann. Rev. Psychol., 59, 93, 10.1146/annurev.psych.59.103006.093556 · DOI
  22. Blaustein, 2013, Enduring influence of pubertal stressors on behavioral response to hormones in female mice, Horm. Behav., 64, 390, 10.1016/j.yhbeh.2013.01.015 · DOI
  23. Bloch, 2003, Endocrine factors in the etiology of postpartum depression, Compr. Psychiatry, 44, 234, 10.1016/S0010-440X(03)00034-8 · DOI · Paper page
  24. Boulanger, 2009, Immune proteins in brain development and synaptic plasticity, Neuron, 64, 93, 10.1016/j.neuron.2009.09.001 · DOI · Paper page
  25. Bourgeois, 1993, Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage, J. Neurosci., 13, 2801, 10.1523/JNEUROSCI.13-07-02801.1993 · DOI · Paper page
  26. Bourgeois, 1994, Synaptogenesis in the prefrontal cortex of rhesus monkeys, Cereb. Cortex, 4, 78, 10.1093/cercor/4.1.78 · DOI · Paper page
  27. Brandi, 1993, Insulin resistance of stress: sites and mechanisms, Clin. Sci. (Lond.), 85, 525, 10.1042/cs0850525 · DOI
  28. Capuron, 2011, Immune system to brain signaling: neuropsychopharmacological implications, Pharmacol. Ther., 130, 226, 10.1016/j.pharmthera.2011.01.014 · DOI · Paper page
  29. Carey, 1995, The influence of ovarian steroids on hypothalamic–pituitary–adrenal regulation in the female rat, J. Endocrinol., 144, 311, 10.1677/joe.0.1440311 · DOI · Paper page
  30. Carpentier, 2009, Immune influence on adult neural stem cell regulation and function, Neuron, 64, 79, 10.1016/j.neuron.2009.08.038 · DOI
  31. Cavaillon, 2001, Pro- versus anti-inflammatory cytokines: myth or reality, Cell Mol. Biol. (Noisy-le-grand), 47, 695
  32. Chester, 2008, Age- and sex-dependent effects of footshock stress on subsequent alcohol drinking and acoustic startle behavior in mice selectively bred for high-alcohol preference, Alcohol. Clin. Exp. Res., 32, 1782, 10.1111/j.1530-0277.2008.00763.x · DOI · Paper page
  33. Choleris, 2003, An estrogen-dependent four-gene micronet regulating social recognition: a study with oxytocin and estrogen receptor-alpha and -beta knockout mice, Proc. Natl. Acad. Sci. USA, 100, 6192, 10.1073/pnas.0631699100 · DOI · Paper page
  34. Choleris, 2006, Involvement of estrogen receptor alpha, beta and oxytocin in social discrimination: a detailed behavioral analysis with knockout female mice, Genes Brain Behav., 5, 528, 10.1111/j.1601-183X.2006.00203.x · DOI
  35. 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 · DOI
  36. Commins, 1985, Autoradiographic localization of estrogen and androgen receptors in the sexually dimorphic area and other regions of the gerbil brain, J. Comp. Neurol., 231, 473, 10.1002/cne.902310406 · DOI
  37. Conrad, 2011, Altered anxiety-like behavior and long-term potentiation in the bed nucleus of the stria terminalis in adult mice exposed to chronic social isolation, unpredictable stress, and ethanol beginning in adolescence, Alcohol, 45, 585, 10.1016/j.alcohol.2010.11.002 · DOI
  38. Coulter, 1996, Postnatal development of the dopamine transporter: a quantitative autoradiographic study, Brain Res. Dev. Brain Res., 92, 172, 10.1016/0165-3806(96)00004-1 · DOI
  39. Crawford, 2003, Parallel developmental trajectories of sensation seeking and regular substance use in adolescents, Psychol. Addict. Behav., 17, 179, 10.1037/0893-164X.17.3.179 · DOI
  40. Cunningham, 2002, Amygdalo-cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence, J. Comp. Neurol., 453, 116, 10.1002/cne.10376 · DOI · Paper page
  41. Dahl, 2009, Heightened stress responsiveness and emotional reactivity during pubertal maturation: implications for psychopathology, Dev. Psychopathol., 21, 1, 10.1017/S0954579409000017 · DOI · Paper page
  42. Dalla, 2004, Oestrogen-deficient female aromatase knockout (ArKO) mice exhibit depressive-like symptomatology, Eur. J. Neurosci., 20, 217, 10.1111/j.1460-9568.2004.03443.x · DOI
  43. Daniel, 1997, Estrogen enhances performance of female rats during acquisition of a radial arm maze, Horm. Behav., 32, 217, 10.1006/hbeh.1997.1433 · DOI
  44. Dantzer, 2001, Cytokine-induced sickness behavior: mechanisms and implications, Ann. N. Y. Acad. Sci., 933, 222, 10.1111/j.1749-6632.2001.tb05827.x · DOI
  45. Datson, 2008, Central corticosteroid actions: search for gene targets, Eur. J. Pharmacol., 583, 272, 10.1016/j.ejphar.2007.11.070 · DOI
  46. 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 · DOI
  47. Davis, 2005, Differential effects of estrogen on hippocampal- and striatal-dependent learning, Neurobiol. Learn. Mem., 84, 132, 10.1016/j.nlm.2005.06.004 · DOI
  48. De Kloet, 2008, Neuropharmacology of glucocorticoids: focus on emotion, cognition and cocaine, Eur. J. Pharmacol., 585, 473, 10.1016/j.ejphar.2008.03.011 · DOI
  49. Deverman, 2009, Cytokines and CNS development, Neuron, 64, 61, 10.1016/j.neuron.2009.09.002 · DOI · Paper page
  50. Diaz-Veliz, 1989, Influence of the estrous cycle, ovariectomy and estradiol replacement upon the acquisition of conditioned avoidance responses in rats, Physiol. Behav., 46, 397, 10.1016/0031-9384(89)90010-3 · DOI
  51. Diaz-Veliz, 1991, Effects of estradiol replacement in ovariectomized rats on conditioned avoidance responses and other behaviors, Physiol. Behav., 50, 61, 10.1016/0031-9384(91)90498-D · DOI
  52. Diaz-Veliz, 1997, Ketanserin and anxiety levels: influence of gender, estrous cycle, ovariectomy and ovarian hormones in female rats, Pharmacol. Biochem. Behav., 58, 637, 10.1016/S0091-3057(97)90004-6 · DOI
  53. Doremus-Fitzwater, 2009, Social and non-social anxiety in adolescent and adult rats after repeated restraint, Physiol. Behav., 97, 484, 10.1016/j.physbeh.2009.03.025 · DOI
  54. Eaton, 2012, An invariant dimensional liability model of gender differences in mental disorder prevalence: evidence from a national sample, J. Abnorm. Psychol., 121, 282, 10.1037/a0024780 · DOI · Paper page
  55. Ellison, 2012, Puberty as a life history transition, Ann. Hum. Biol., 39, 352, 10.3109/03014460.2012.693199 · DOI · Paper page
  56. Eugenin, 2001, Microglia at brain stab wounds express connexin 43 and in vitro form functional gap junctions after treatment with interferon-gamma and tumor necrosis factor-alpha, Proc. Natl. Acad. Sci. USA, 98, 4190, 10.1073/pnas.051634298 · DOI
  57. Farber, 1995, Age-specific neurotoxicity in the rat associated with NMDA receptor blockade: potential relevance to schizophrenia?, Biol. Psychiatry, 38, 788, 10.1016/0006-3223(95)00046-1 · DOI
  58. Farrell, 2013, Sex differences and chronic stress effects on the neural circuitry underlying fear conditioning and extinction, Physiol. Behav., 10.1016/j.physbeh.2013.04.002 · DOI
  59. Feder, 1974, Activation of lordosis in ovariectomized guinea pigs by free and esterified forms of estrone, estradiol-17 beta and estriol, Physiol. Behav., 13, 251, 10.1016/0031-9384(74)90042-0 · DOI
  60. File, 2003, A review of 25 years of the social interaction test, Eur. J. Pharmacol., 463, 35, 10.1016/S0014-2999(03)01273-1 · DOI
  61. Gadient, 1994, Expression of interleukin-6 (IL-6) and interleukin-6 receptor (IL-6R) mRNAs in rat brain during postnatal development, Brain Res., 637, 10, 10.1016/0006-8993(94)91211-4 · DOI
  62. Galeeva, 2001, Analysis of mouse plus-maze behavior modulated by ovarian steroids, Behav. Brain Res., 119, 41, 10.1016/S0166-4328(00)00341-7 · DOI
  63. Ge, 2001, Pubertal transition, stressful life events, and the emergence of gender differences in adolescent depressive symptoms, Dev. Psychol., 37, 404, 10.1037/0012-1649.37.3.404 · DOI · Paper page
  64. Gerocs, 1986, Quantitative analysis of dendritic protrusions in the medial preoptic area during postnatal development, Brain Res., 391, 49, 10.1016/0165-3806(86)90006-4 · DOI
  65. Giedd, 1997, Sexual dimorphism of the developing human brain, Prog. Neuropsychopharmacol. Biol. Psychiatry, 21, 1185, 10.1016/S0278-5846(97)00158-9 · DOI
  66. Giedd, 1999, Brain development during childhood and adolescence: a longitudinal MRI study, Nat. Neurosci., 2, 861, 10.1038/13158 · DOI · Paper page
  67. Girotti, 2006, Habituation to repeated restraint stress is associated with lack of stress-induced c-fos expression in primary sensory processing areas of the rat brain, Neuroscience, 138, 1067, 10.1016/j.neuroscience.2005.12.002 · DOI
  68. Goldstein, 1990, Androgen regulation of dendritic growth and retraction in the development of a sexually dimorphic spinal nucleus, J. Neurosci., 10, 935, 10.1523/JNEUROSCI.10-03-00935.1990 · DOI
  69. Gomez, 2004, Androgen-sensitive changes in regulation of restraint-induced adrenocorticotropin secretion between early and late puberty in male rats, Endocrinology, 145, 59, 10.1210/en.2003-0565 · DOI
  70. Gomez-Gonzalez, 2010, Prenatal stress alters microglial development and distribution in postnatal rat brain, Acta Neuropathol., 119, 303, 10.1007/s00401-009-0590-4 · DOI
  71. Gottsch, 2004, A role for kisspeptins in the regulation of gonadotropin secretion in the mouse, Endocrinology, 145, 4073, 10.1210/en.2004-0431 · DOI · Paper page
  72. Graeber, 2010, Changing face of microglia, Science, 330, 783, 10.1126/science.1190929 · DOI · Paper page
  73. Graeber, 2010, Microglia: biology and pathology, Acta Neuropathol., 119, 89, 10.1007/s00401-009-0622-0 · DOI
  74. Grant, 2003, Stressors and child and adolescent psychopathology: moving from markers to mechanisms of risk, Psychol. Bull., 129, 447, 10.1037/0033-2909.129.3.447 · DOI
  75. Grant, 2004, Stressors and child and adolescent psychopathology: measurement issues and prospective effects, J. Clin. Child Adolesc. Psychol., 33, 412, 10.1207/s15374424jccp3302_23 · DOI
  76. Green, 2012, Social instability stress in adolescence increases anxiety and reduces social interactions in adulthood in male Long-Evans rats, Dev. Psychobiol.
  77. Grippo, 2003, Behavioral and cardiovascular changes in the chronic mild stress model of depression, Physiol. Behav., 78, 703, 10.1016/S0031-9384(03)00050-7 · DOI
  78. Guillamon, 1988, Effects of sex steroids on the development of the locus coeruleus in the rat, Brain Res., 468, 306, 10.1016/0165-3806(88)90143-5 · DOI
  79. Hanisch, 2007, Microglia: active sensor and versatile effector cells in the normal and pathologic brain, Nat. Neurosci., 10, 1387, 10.1038/nn1997 · DOI · Paper page
  80. Harris, 2004, Increased glucocorticoid response to a novel stress in rats that have been restrained, Physiol. Behav., 81, 557, 10.1016/j.physbeh.2004.01.017 · DOI
  81. Helmreich, 1997, Correlation between changes in stress-induced corticosterone secretion and GR mRNA levels, Stress, 2, 101, 10.3109/10253899709014741 · DOI
  82. Herbison, 1995, Sexually dimorphic expression of androgen receptor immunoreactivity by somatostatin neurones in rat hypothalamic periventricular nucleus and bed nucleus of the stria terminalis, J. Neuroendocrinol., 7, 543, 10.1111/j.1365-2826.1995.tb00791.x · DOI
  83. Hinwood, M., Tynan, R.J., Charnley, J.L., Beynon, S.B., Day, T.A., Walker, F.R., 2012. Chronic stress induced remodeling of the prefrontal cortex: structural re-organization of microglia and the inhibitory effect of minocycline. Cereb. Cortex. · DOI
  84. Hou, 2012, A neuroimmunological perspective on anxiety disorders, Hum. Psychopharmacol., 27, 6, 10.1002/hup.1259 · DOI
  85. Huang, 2012, Estradiol acutely suppresses inhibition in the hippocampus through a sex-specific endocannabinoid and mGluR-dependent mechanism, Neuron, 74, 801, 10.1016/j.neuron.2012.03.035 · DOI
  86. Huttenlocher, 1979, Synaptic density in human frontal cortex – developmental changes and effects of aging, Brain Res., 163, 195, 10.1016/0006-8993(79)90349-4 · DOI · Paper page
  87. 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 · DOI
  88. Ilin, 2009, Enriched environment experience overcomes learning deficits and depressive-like behavior induced by juvenile stress, PLoS ONE, 4, e4329, 10.1371/journal.pone.0004329 · DOI
  89. Im-Bolter, 2013, I thought we were good: social cognition, figurative language, and adolescent psychopathology, J. Child Psychol. Psychiatry, 10.1111/jcpp.12067 · DOI
  90. Imwalle, 2005, Lack of functional estrogen receptor beta influences anxiety behavior and serotonin content in female mice, Physiol. Behav., 84, 157, 10.1016/j.physbeh.2004.11.002 · DOI
  91. Insel, 1990, The ontogeny of excitatory amino acid receptors in rat forebrain – I. N-methyl-d-aspartate and quisqualate receptors, Neuroscience, 35, 31, 10.1016/0306-4522(90)90117-M · DOI · Paper page
  92. Intlekofer, 2010, Distribution of mRNAs encoding classical progestin receptor, progesterone membrane components 1 and 2, serpine mRNA binding protein 1, and progestin and ADIPOQ receptor family members 7 and 8 in rat forebrain, Neuroscience, 172, 55, 10.1016/j.neuroscience.2010.10.051 · DOI
  93. Isgor, 2004, Delayed effects of chronic variable stress during peripubertal-juvenile period on hippocampal morphology and on cognitive and stress axis functions in rats, Hippocampus, 14, 636, 10.1002/hipo.10207 · DOI · Paper page
  94. Ismail, 2013, Pubertal immune challenge blocks the ability of estradiol to enhance performance on cognitive tasks in adult female mice, Psychoneuroendocrinology, 38, 1170, 10.1016/j.psyneuen.2012.11.003 · DOI
  95. Ismail, 2011, Long-term effects of pubertal stressors on female sexual receptivity and estrogen receptor-alpha expression in CD-1 female mice, Horm. Behav., 59, 565, 10.1016/j.yhbeh.2011.02.010 · DOI
  96. Ismail, 2012, A pubertal immune challenge alters the antidepressant-like effects of chronic estradiol treatment in inbred and outbred adult female mice, Neuroscience
  97. Jacobson-Pick, 2010, Differential impact of juvenile stress and corticosterone in juvenility and in adulthood, in male and female rats, Behav. Brain Res., 214, 268, 10.1016/j.bbr.2010.05.036 · DOI
  98. Jacobson-Pick, 2012, Short- and long-term effects of juvenile stressor exposure on the expression of GABAA receptor subunits in rats, Stress, 15, 416, 10.3109/10253890.2011.634036 · DOI
  99. Jakubowski, 1991, Postnatal development of gonadotropin-releasing hormone and cyclophilin gene expression in the female and male rat brain, Endocrinology, 128, 2702, 10.1210/endo-128-6-2702 · DOI
  100. Janeway, 2001, How the immune system works to protect the host from infection: a personal view, Proc. Natl. Acad. Sci. USA, 98, 7461, 10.1073/pnas.131202998 · DOI
  101. Jedlicka, 2008, A role for the spine apparatus in LTP and spatial learning, Behav. Brain Res., 192, 12, 10.1016/j.bbr.2008.02.033 · DOI
  102. Johansen, 2011, Molecular mechanisms of fear learning and memory, Cell, 147, 509, 10.1016/j.cell.2011.10.009 · DOI · Paper page
  103. John, 2003, Cytokines: powerful regulators of glial cell activation, Neuroscientist, 9, 10, 10.1177/1073858402239587 · DOI
  104. Johnston, 1991, Sex differences in animal tests of anxiety, Physiol. Behav., 49, 245, 10.1016/0031-9384(91)90039-Q · DOI · Paper page
  105. Jones, 2012, The role of the innate immune system in psychiatric disorders, Mol. Cell. Neurosci.
  106. Kalsbeek, 1988, Development of the dopaminergic innervation in the prefrontal cortex of the rat, J. Comp. Neurol., 269, 58, 10.1002/cne.902690105 · DOI · Paper page
  107. Kauffman, 2007, Emerging ideas about kisspeptin–GPR54 signaling in the neuroendocrine regulation of reproduction, Trends Neurosci., 30, 504, 10.1016/j.tins.2007.08.001 · DOI
  108. Kendig, 2011, Predatory threat induces huddling in adolescent rats and residual changes in early adulthood suggestive of increased resilience, Behav. Brain Res., 225, 405, 10.1016/j.bbr.2011.07.058 · DOI
  109. Konkle, 2003, Evaluation of the effects of chronic mild stressors on hedonic and physiological responses: sex and strain compared, Brain Res., 992, 227, 10.1016/j.brainres.2003.08.047 · DOI
  110. Korenbrot, 1977, Preputial separation as an external sign of pubertal development in the male rat, Biol. Reprod., 17, 298, 10.1095/biolreprod17.2.298 · DOI · Paper page
  111. Korol, 2004, Role of estrogen in balancing contributions from multiple memory systems, Neurobiol. Learn. Mem., 82, 309, 10.1016/j.nlm.2004.07.006 · DOI
  112. Koss, 2012, Estrogen effects on the forced swim test differ in two outbred rat strains, Physiol. Behav., 106, 81, 10.1016/j.physbeh.2012.01.004 · DOI
  113. Krezel, 2001, Increased anxiety and synaptic plasticity in estrogen receptor beta -deficient mice, Proc. Natl. Acad. Sci. USA, 98, 12278, 10.1073/pnas.221451898 · DOI
  114. Kuhnemann, 1994, Sex differences in the development of estrogen receptors in the rat brain, Horm. Behav., 28, 483, 10.1006/hbeh.1994.1046 · DOI
  115. Kvetnansky, 2009, Catecholaminergic systems in stress: structural and molecular genetic approaches, Physiol. Rev., 89, 535, 10.1152/physrev.00042.2006 · DOI · Paper page
  116. Laroche, 2009, Enduring influences of peripubertal/adolescent stressors on behavioral response to estradiol and progesterone in adult female mice, Endocrinology, 150, 3717, 10.1210/en.2009-0099 · DOI
  117. Laroche, 2009, Reduced behavioral response to gonadal hormones in mice shipped during the peripubertal/adolescent period, Endocrinology, 150, 2351, 10.1210/en.2008-1595 · DOI
  118. Laugero, 2000, Summation of behavioral and immunological stress: metabolic consequences to the growing mouse, Am. J. Physiol. Endocrinol. Metab., 279, E44, 10.1152/ajpendo.2000.279.1.E44 · DOI
  119. Lemieux, 2008, Symptom severity predicts degree of T cell activation in adult women following childhood maltreatment, Brain Behav. Immun., 22, 994, 10.1016/j.bbi.2008.02.005 · DOI · Paper page
  120. Lenz, 2012, Sexual differentiation of the rodent brain: dogma and beyond, Front. Neurosci., 6, 26, 10.3389/fnins.2012.00026 · DOI
  121. Leslie, 1991, Postnatal development of D1 dopamine receptors in the medial prefrontal cortex, striatum and nucleus accumbens of normal and neonatal 6-hydroxydopamine treated rats: a quantitative autoradiographic analysis, Brain Res. Dev. Brain Res., 62, 109, 10.1016/0165-3806(91)90195-O · DOI
  122. Leuner, 2003, Associative memory formation increases the observation of dendritic spines in the hippocampus, J. Neurosci., 23, 659, 10.1523/JNEUROSCI.23-02-00659.2003 · DOI
  123. Lewis, 2004, Postnatal development of prefrontal inhibitory circuits and the pathophysiology of cognitive dysfunction in schizophrenia, Ann. N. Y. Acad. Sci., 1021, 64, 10.1196/annals.1308.008 · DOI
  124. Li, 2004, Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice, Proc. Natl. Acad. Sci. USA, 101, 2185, 10.1073/pnas.0307313101 · DOI
  125. Li, 2006, Decreases in nestlet shredding of mice by serotonin uptake inhibitors: comparison with marble burying, Life Sci., 78, 1933, 10.1016/j.lfs.2005.08.002 · DOI
  126. Ling, 1993, The origin and nature of ramified and amoeboid microglia: a historical review and current concepts, Glia, 7, 9, 10.1002/glia.440070105 · DOI
  127. Lu, 1998, Androgen receptor in mouse brain: sex differences and similarities in autoregulation, Endocrinology, 139, 1594, 10.1210/endo.139.4.5863 · DOI
  128. Luine, 2008, Sex steroids and cognitive function, J. Neuroendocrinol., 20, 866, 10.1111/j.1365-2826.2008.01710.x · DOI
  129. Luine, 2012, Estrogens facilitate memory processing through membrane mediated mechanisms and alterations in spine density, Front. Neuroendocrinol., 33, 388, 10.1016/j.yfrne.2012.07.004 · DOI
  130. Luine, 1998, Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters, Horm. Behav., 34, 149, 10.1006/hbeh.1998.1473 · DOI
  131. Magarinos, 1995, Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors, Neuroscience, 69, 89, 10.1016/0306-4522(95)00259-L · DOI · Paper page
  132. Marcondes, 2001, Estrous cycle influences the response of female rats in the elevated plus-maze test, Physiol. Behav., 74, 435, 10.1016/S0031-9384(01)00593-5 · DOI
  133. Marshall, 1969, Variations in pattern of pubertal changes in girls, Arch. Dis. Child., 44, 291, 10.1136/adc.44.235.291 · DOI · Paper page
  134. Marti, 1997, Influence of regularity of exposure to chronic stress on the pattern of habituation of pituitary–adrenal hormones, prolactin and glucose, Stress, 1, 179, 10.3109/10253899709001107 · DOI
  135. Maslova, 2002, Chronic stress during prepubertal development: immediate and long-lasting effects on arterial blood pressure and anxiety-related behavior, Psychoneuroendocrinology, 27, 549, 10.1016/S0306-4530(01)00092-0 · DOI
  136. Mathews, 2008, Increased depressive behaviour in females and heightened corticosterone release in males to swim stress after adolescent social stress in rats, Behav. Brain Res., 190, 33, 10.1016/j.bbr.2008.02.004 · DOI
  137. McCormick, 2012, From the stressed adolescent to the anxious and depressed adult: investigations in rodent models, Neuroscience
  138. McCormick, 1998, Neonatal sex hormones have ‘organizational’ effects on the hypothalamic–pituitary–adrenal axis of male rats, Brain Res. Dev. Brain Res., 105, 295, 10.1016/S0165-3806(97)00155-7 · DOI · Paper page
  139. McCormick, 2002, Peripheral and central sex steroids have differential effects on the HPA axis of male and female rats, Stress, 5, 235, 10.1080/1025389021000061165 · DOI
  140. McCormick, 2005, Long-lasting, sex- and age-specific effects of social stressors on corticosterone responses to restraint and on locomotor responses to psychostimulants in rats, Horm. Behav., 48, 64, 10.1016/j.yhbeh.2005.01.008 · DOI
  141. McCormick, 2008, Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats, Behav. Brain Res., 187, 228, 10.1016/j.bbr.2007.09.005 · DOI
  142. McEwen, 2000, Allostasis, allostatic load, and the aging nervous system: role of excitatory amino acids and excitotoxicity, Neurochem. Res., 25, 1219, 10.1023/A:1007687911139 · DOI
  143. McEwen, 2012, Estrogen effects on the brain: actions beyond the hypothalamus via novel mechanisms, Behav. Neurosci., 126, 4, 10.1037/a0026708 · DOI
  144. Medzhitov, 2000, Innate immune recognition: mechanisms and pathways, Immunol. Rev., 173, 89, 10.1034/j.1600-065X.2000.917309.x · DOI
  145. Meyer, 1978, The effects of puberty and castration on hippocampal dendritic spines of mice. A Golgi study, Brain Res., 155, 108, 10.1016/0006-8993(78)90309-8 · DOI
  146. Miller, 2009, Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression, Biol. Psychiatry, 65, 732, 10.1016/j.biopsych.2008.11.029 · DOI · Paper page
  147. Mohr, 2013, Pubertally born neurons and glia are functionally integrated into limbic and hypothalamic circuits of the male Syrian hamster, Proc. Natl. Acad. Sci. USA, 110, 4792, 10.1073/pnas.1219443110 · DOI
  148. Mora, 1996, Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats, Psychoneuroendocrinology, 21, 609, 10.1016/S0306-4530(96)00015-7 · DOI
  149. Morgan, 2001, Effects of estrogen on activity and fear-related behaviors in mice, Horm. Behav., 40, 472, 10.1006/hbeh.2001.1716 · DOI
  150. Morgan, 2002, Estrogen’s effects on activity, anxiety, and fear in two mouse strains, Behav. Brain Res., 132, 85, 10.1016/S0166-4328(01)00398-9 · DOI · Paper page
  151. Navarro, 2011, Interactions between kisspeptin and neurokinin B in the control of GnRH secretion in the female rat, Am. J. Physiol. Endocrinol. Metab., 300, E202, 10.1152/ajpendo.00517.2010 · DOI
  152. Nilsson, 2001, Mechanisms of estrogen action, Physiol. Rev., 81, 1535, 10.1152/physrev.2001.81.4.1535 · DOI
  153. Novac, 2004, Nuclear receptors: overview and classification, Curr. Drug Targets Inflamm. Allergy, 3, 335, 10.2174/1568010042634541 · DOI
  154. Nunez, 2000, Androgens reduce cell death in the developing rat visual cortex, Brain Res. Dev. Brain Res., 125, 83, 10.1016/S0165-3806(00)00126-7 · DOI
  155. 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 · DOI
  156. Oakley, 2009, Kisspeptin signaling in the brain, Endocr. Rev., 30, 713, 10.1210/er.2009-0005 · DOI · Paper page
  157. Ogawa, 1998, Roles of estrogen receptor-alpha gene expression in reproduction-related behaviors in female mice, Endocrinology, 139, 5070, 10.1210/endo.139.12.6357 · DOI
  158. Ojeda, 1976, The onset of puberty in the female rat: changes in plasma prolactin, gonadotropins, luteinizing hormone-releasing hormone (LHRH), and hypothalamic LHRH content, Endocrinology, 98, 630, 10.1210/endo-98-3-630 · DOI
  159. Ojeda, 2006, Minireview: the neuroendocrine regulation of puberty: is the time ripe for a systems biology approach?, Endocrinology, 147, 1166, 10.1210/en.2005-1136 · DOI
  160. Okada, 1997, Influences of ovariectomy and continuous replacement of 17beta-estradiol on the tail skin temperature and behavior in the forced swimming test in rats, Jpn. J. Pharmacol., 73, 93, 10.1254/jjp.73.93 · DOI
  161. Olesen, 2011, Long-term alteration of anxiolytic effects of ovarian hormones in female mice by a peripubertal immune challenge, Horm. Behav., 60, 318, 10.1016/j.yhbeh.2011.06.005 · DOI
  162. Olivera-Lopez, 2008, Estradiol and neuropeptide Y (intra-lateral septal) reduce anxiety-like behavior in two animal models of anxiety, Peptides, 29, 1396, 10.1016/j.peptides.2008.04.002 · DOI
  163. O’Neil, 2003, Animal models of depression: are there any?, Hum. Psychopharmacol., 18, 239, 10.1002/hup.496 · DOI
  164. Osterlund, 2010, Underlying mechanisms mediating the antidepressant effects of estrogens, Biochim. Biophys. Acta, 1800, 1136, 10.1016/j.bbagen.2009.11.001 · DOI
  165. Palanza, 2001, Social stress in mice: gender differences and effects of estrous cycle and social dominance, Physiol. Behav., 73, 411, 10.1016/S0031-9384(01)00494-2 · DOI
  166. Pandaranandaka, 2006, Anxiolytic property of estrogen related to the changes of the monoamine levels in various brain regions of ovariectomized rats, Physiol. Behav., 87, 828, 10.1016/j.physbeh.2006.02.002 · DOI
  167. Pandaranandaka, 2009, Differential effects of exogenous and endogenous estrogen on anxiety as measured by elevated T-maze in relation to the serotonergic system, Behav. Brain Res., 198, 142, 10.1016/j.bbr.2008.10.043 · DOI
  168. Paolicelli, 2011, Microglia in development: linking brain wiring to brain environment, Neuron Glia Biol., 7, 77, 10.1017/S1740925X12000105 · DOI
  169. Parent, 2005, Control of puberty by excitatory amino acid neurotransmitters and its clinical implications, Endocrine, 28, 281, 10.1385/ENDO:28:3:281 · DOI
  170. Pariante, 2001, Glucocorticoid receptors in major depression: relevance to pathophysiology and treatment, Biol. Psychiatry, 49, 391, 10.1016/S0006-3223(00)01088-X · DOI · Paper page
  171. Parker, 1991, Adrenarche, Endocrinol. Metab. Clin. North Am., 20, 71, 10.1016/S0889-8529(18)30282-2 · DOI
  172. Parker, 1976, Hormonal events surrounding the natural onset of puberty in female rats, Biol. Reprod., 14, 347, 10.1095/biolreprod14.3.347 · DOI
  173. Parsons, 1982, Progestin receptor levels in rat hypothalamic and limbic nuclei, J. Neurosci., 2, 1446, 10.1523/JNEUROSCI.02-10-01446.1982 · DOI
  174. Patton, 2007, Pubertal transitions in health, Lancet, 369, 1130, 10.1016/S0140-6736(07)60366-3 · DOI
  175. Patton, 1996, Menarche and the onset of depression and anxiety in Victoria, Australia, J. Epidemiol. Community Health, 50, 661, 10.1136/jech.50.6.661 · DOI
  176. Peleg-Raibstein, 2011, Differential effects of post-weaning juvenile stress on the behaviour of C57BL/6 mice in adolescence and adulthood, Psychopharmacology, 214, 339, 10.1007/s00213-010-1991-8 · DOI
  177. Petanjek, 2011, Extraordinary neoteny of synaptic spines in the human prefrontal cortex, Proc. Natl. Acad. Sci. USA, 108, 13281, 10.1073/pnas.1105108108 · DOI · Paper page
  178. Picazo, 2006, Influence of the post-ovariectomy time frame on the experimental anxiety and the behavioural actions of some anxiolytic agents, Eur. J. Pharmacol., 530, 88, 10.1016/j.ejphar.2005.11.024 · DOI
  179. Pignatelli, 2006, Adrenarche in the rat, J. Endocrinol., 191, 301, 10.1677/joe.1.06972 · DOI
  180. 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 · DOI
  181. Plant, 2004, Neurobiological mechanisms of puberty in higher primates, Hum. Reprod. Update, 10, 67, 10.1093/humupd/dmh001 · DOI
  182. Pousset, 1994, Developmental expression of cytokine genes in the cortex and hippocampus of the rat central nervous system, Brain Res. Dev. Brain Res., 81, 143, 10.1016/0165-3806(94)90078-7 · DOI
  183. Rachman, 1998, Estrogen alters behavior and forebrain c-fos expression in ovariectomized rats subjected to the forced swim test, Proc. Natl. Acad. Sci. USA, 95, 13941, 10.1073/pnas.95.23.13941 · DOI
  184. Rainbow, 1982, Sex differences in rat brain oestrogen and progestin receptors, Nature, 300, 648, 10.1038/300648a0 · DOI
  185. Raivich, 2005, Like cops on the beat: the active role of resting microglia, Trends Neurosci., 28, 571, 10.1016/j.tins.2005.09.001 · DOI
  186. Ramaswamy, 2008, Structural interactions between kisspeptin and GnRH neurons in the mediobasal hypothalamus of the male rhesus monkey (Macaca mulatta) as revealed by double immunofluorescence and confocal microscopy, Endocrinology, 149, 4387, 10.1210/en.2008-0438 · DOI
  187. Redei, 1994, Fast glucocorticoid feedback inhibition of ACTH secretion in the ovariectomized rat: effect of chronic estrogen and progesterone, Neuroendocrinology, 60, 113, 10.1159/000126741 · DOI
  188. Reiss, 1996, Brain development, gender and IQ in children. A volumetric imaging study, Brain, 119, 1763, 10.1093/brain/119.5.1763 · DOI
  189. Roberti, 2004, A review of behavioral and biological correlates of sensation seeking, J. Res. Pers., 38, 256, 10.1016/S0092-6566(03)00067-9 · DOI · Paper page
  190. Rocha, 2005, 17 Beta-estradiol-induced antidepressant-like effect in the forced swim test is absent in estrogen receptor-beta knockout (BERKO) mice, Psychopharmacology, 179, 637, 10.1007/s00213-004-2078-1 · DOI
  191. Romeo, 2004, Testosterone cannot activate an adult-like stress response in prepubertal male rats, Neuroendocrinology, 79, 125, 10.1159/000077270 · DOI
  192. Romeo, 2004, Differential stress reactivity in intact and ovariectomized prepubertal and adult female rats, Neuroendocrinology, 80, 387, 10.1159/000084203 · DOI · Paper page
  193. Romeo, 2005, Stress-induced progesterone secretion and progesterone receptor immunoreactivity in the paraventricular nucleus are modulated by pubertal development in male rats, Stress, 8, 265, 10.1080/10253890500489320 · DOI
  194. Romeo, 2006, Stress history and pubertal development interact to shape hypothalamic–pituitary–adrenal axis plasticity, Endocrinology, 147, 1664, 10.1210/en.2005-1432 · DOI · Paper page
  195. Romeo, 2007, Age- and stress-induced changes in corticotropin-releasing hormone mRNA expression in the paraventricular nucleus of the hypothalamus, Neuroendocrinology, 85, 199, 10.1159/000102950 · DOI
  196. Roy, 2004, Further evidences that risk assessment and object exploration behaviours are useful to evaluate emotional reactivity in rodents, Behav. Brain Res., 154, 439, 10.1016/j.bbr.2004.03.010 · DOI
  197. Salim, 2012, Inflammation in anxiety, Adv. Protein Chem. Struct. Biol., 88, 1, 10.1016/B978-0-12-398314-5.00001-5 · DOI
  198. Sandstrom, 2004, Spatial memory retention is enhanced by acute and continuous estradiol replacement, Horm. Behav., 45, 128, 10.1016/j.yhbeh.2003.09.010 · DOI
  199. Santini, 2004, Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex, J. Neurosci., 24, 5704, 10.1523/JNEUROSCI.0786-04.2004 · DOI · Paper page
  200. Sapolsky, 1994, Rank-related differences in cardiovascular function among wild baboons – role of sensitivity to glucocorticoids, Am. J. Primatol., 32, 261, 10.1002/ajp.1350320404 · DOI

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Metadata

Authors
Holder, M. K., & Blaustein, J. D.
Affiliations
University of Massachusetts Amherst (US)
Corresponding author
Blaustein, Jeffrey D.
ORCID
Venue
Frontiers in Neuroendocrinology
Publisher
Elsevier BV
Published
2014-01
Volume
35
Issue
1
Pages
89-110
ISSN
0091-3022 (ISSN-L)
DOI
10.1016/j.yfrne.2013.10.004
PMC
PMC3946873
OpenAlex
W2030185037
Cited by
279
References
344
Citations by year
2026: 28 · 2025: 35 · 2024: 20 · 2023: 29 · 2022: 22 · 2021: 29 · 2020: 24 · 2019: 18 · 2018: 23 · 2017: 15 · 2016: 16 · 2015: 13 · 2014: 7
FWCI
0.98
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Neuroendocrinology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institute of Mental Health (MH093854, R21MH093854)
  • National Institute of Neurological Disorders and Stroke (R01NS019327, NS-19327)
Topics
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
Keywords
puberty, adolescence, developmental stress, stress reactivity, anxiety, depression, cognitive performance, hippocampal volume, neuroplasticity, gonadal hormones, sexual behavior, estrogen receptor, neuroinflammation, immune activation, neurobehavioral development
MeSH terms
Adolescent, Adolescent Behavior, Animals, Cognition, Humans, Puberty, Sexual Maturation, Stress, Psychological, Gonadal Hormones

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