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

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

Open access
Holder, Mary K., Blaustein, Jeffrey D.·2014·Frontiers in Neuroendocrinology
DOI 10.1016/j.yfrne.2013.10.004PMC PMC3946873
Open this paper in CoChat — free account

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.yfrne.2013.10.004

Cites

0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 285

  1. Aloisi F 2001 Immune function of microglia Glia 36 165 79 11596125
  2. Altemus KL Almli CR 1997 Neonatal hippocampal damage in rats: long-term spatial memory deficits and associations with magnitude of hippocampal damage Hippocampus 7 403 15 9287080
  3. Andersen SL Teicher MH 2004 Delayed effects of early stress on hippocampal development Neuropsychopharmacology 29 1988 93 15316569
  4. Angold A Costello EJ 2006 Puberty and depression Child Adolesc Psychiatr Clin N Am 15 919 37 ix 16952768
  5. Anisman H 2009 Cascading effects of stressors and inflammatory immune system activation: implications for major depressive disorder J Psychiatry Neurosci 34 4 20 19125209 PMC2612083
  6. Araki S Toran-Allerand CD Ferin M Vande Wiele RL 1975 Immunoreactive gonadotropin-releasing hormone (Gn-RH) during maturation in the rat: Ontogeny of regional hypothalamic differences Endocrinology 97 693 7 1100363
  7. Avital A Ram E Maayan R Weizman A Richter-Levin G 2006 Effects of early-life stress on behavior and neurosteroid levels in the rat hypothalamus and entorhinal cortex Brain Res Bull 68 419 24 16459196
  8. Avital A Richter-Levin G 2005 Exposure to juvenile stress exacerbates the behavioural consequences of exposure to stress in the adult rat Int J Neuropsychopharmacol 8 163 73 15546500
  9. Barnea-Goraly N Menon V Eckert M Tamm L Bammer R Karchemskiy A Dant CC Reiss AL 2005 White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study Cereb Cortex 15 1848 54 15758200
  10. Bauer S Kerr BJ Patterson PH 2007 The neuropoietic cytokine family in development, plasticity, disease and injury Nat Rev Neurosci 8 221 32 17311007
  11. Bazak N Kozlovsky N Kaplan Z Matar M Golan H Zohar J Richter-Levin G Cohen H 2009 Pre-pubertal stress exposure affects adult behavioral response in association with changes in circulating corticosterone and brain-derived neurotrophic factor Psychoneuroendocrinology 34 844 58 19181453
  12. Bekku N Yoshimura H 2005 Animal model of menopausal depressive-like state in female mice: prolongation of immobility time in the forced swimming test following ovariectomy Psychopharmacology (Berl) 183 300 7 16228195
  13. Bekman NM Cummins K Brown SA 2010 Affective and personality risk and cognitive mediators of initial adolescent alcohol use J Stud Alcohol Drugs 71 570 80 20553666 PMC2887926
  14. Beltran-Campos V Prado-Alcala RA Leon-Jacinto U Aguilar-Vazquez A Quirarte GL Ramirez-Amaya V Diaz-Cintra S 2011 Increase of mushroom spine density in CA1 apical dendrites produced by water maze training is prevented by ovariectomy Brain Res 1369 119 30 21070752
  15. Benes FM Taylor JB Cunningham MC 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 27 11007552
  16. Benes FM Turtle M Khan Y Farol P 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 84 8192550
  17. Bernardi M Vergoni AV Sandrini M Tagliavini S Bertolini A 1989 Influence of ovariectomy, estradiol and progesterone on the behavior of mice in an experimental model of depression Physiol Behav 45 1067 8 2780868
  18. Bilbo SD Smith SH Schwarz JM 2011 A Lifespan Approach to Neuroinflammatory and Cognitive Disorders: A Critical Role for Glia J Neuroimmune Pharmacol PMC3267003 21822589
  19. Blaustein JD 2008 Neuroendocrine regulation of feminine sexual behavior: lessons from rodent models and thoughts about humans Ann Rev Psych 59 93 118 17678443
  20. Blaustein JD Ismail N 2013 Enduring influence of pubertal stressors on behavioral response to hormones in female mice Horm Behav 64 390 8 23998680 PMC3761225
  21. Bloch M Daly RC Rubinow DR 2003 Endocrine factors in the etiology of postpartum depression Compr Psychiatry 44 234 46 12764712
  22. Boulanger LM 2009 Immune proteins in brain development and synaptic plasticity Neuron 64 93 109 19840552
  23. Bourgeois JP Goldman-Rakic PS Rakic P 1994 Synaptogenesis in the prefrontal cortex of rhesus monkeys Cereb Cortex 4 78 96 8180493
  24. Bourgeois JP Rakic P 1993 Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage J Neurosci 13 2801 20 8331373 PMC6576672
  25. Brandi LS Santoro D Natali A Altomonte F Baldi S Frascerra S Ferrannini E 1993 Insulin resistance of stress: sites and mechanisms Clin Sci (Lond) 85 525 35 8287639
  26. Capuron L Miller AH 2011 Immune system to brain signaling: neuropsychopharmacological implications Pharmacol Ther 130 226 38 21334376 PMC3072299
  27. Carey MP Deterd CH de Koning J Helmerhorst F de Kloet ER 1995 The influence of ovarian steroids on hypothalamic-pituitary-adrenal regulation in the female rat J Endocrinol 144 311 21 7706984
  28. Carpentier PA Palmer TD 2009 Immune influence on adult neural stem cell regulation and function Neuron 64 79 92 19840551 PMC2789107
  29. Cavaillon JM 2001 Pro- versus anti-inflammatory cytokines: myth or reality Cell Mol Biol (Noisy-le-grand) 47 695 702 11502077
  30. Chester JA Barrenha GD Hughes ML Keuneke KJ 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 94 18652593 PMC4426867
  31. Choleris E Gustafsson JA Korach KS Muglia LJ Pfaff DW Ogawa S 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 U S A 100 6192 7 12730370 PMC156348
  32. Choleris E Ogawa S Kavaliers M Gustafsson JA Korach KS Muglia LJ Pfaff DW 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 39 17010099
  33. Chung WC De Vries GJ Swaab DF 2002 Sexual differentiation of the bed nucleus of the stria terminalis in humans may extend into adulthood J Neurosci 22 1027 33 11826131 PMC6758506
  34. Commins D Yahr P 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 89 3968250
  35. Conrad KL Winder DG 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 93 21194878 PMC3085602
  36. Coulter CL Happe HK Murrin LC 1996 Postnatal development of the dopamine transporter: a quantitative autoradiographic study Brain Res Dev Brain Res 92 172 81 8738124
  37. Crawford AM Pentz MA Chou CP Li C Dwyer JH 2003 Parallel developmental trajectories of sensation seeking and regular substance use in adolescents Psychol Addict Behav 17 179 92 14498812
  38. Cunningham MG Bhattacharyya S Benes FM 2002 Amygdalo-cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence J Comp Neurol 453 116 30 12373778
  39. Dahl RE Gunnar MR 2009 Heightened stress responsiveness and emotional reactivity during pubertal maturation: implications for psychopathology Dev Psychopathol 21 1 6 19144219
  40. Dalla C Antoniou K Papadopoulou-Daifoti Z Balthazart J Bakker J 2004 Oestrogen-deficient female aromatase knockout (ArKO) mice exhibit depressive-like symptomatology Eur J Neurosci 20 217 28 15245494
  41. Daniel JM Fader AJ Spencer AL Dohanich GP 1997 Estrogen enhances performance of female rats during acquisition of a radial arm maze Horm Behav 32 217 25 9454673
  42. Dantzer R 2001 Cytokine-induced sickness behavior: mechanisms and implications Ann N Y Acad Sci 933 222 34 12000023
  43. Datson NA Morsink MC Meijer OC de Kloet ER 2008 Central corticosteroid actions: Search for gene targets Eur J Pharmacol 583 272 89 18295201
  44. Davis DM Jacobson TK Aliakbari S Mizumori SJ 2005 Differential effects of estrogen on hippocampal- and striatal-dependent learning Neurobiol Learn Mem 84 132 7 16054404
  45. Davis EC Shryne JE Gorski RA 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 8 9053778
  46. De Kloet ER de Jong IE Oitzi MS 2008 Neuropharmacology of glucocorticoids: focus on emotion, cognition and cocaine Eur J Pharmacol 585 473 82 18417120
  47. Deverman BE Patterson PH 2009 Cytokines and CNS development Neuron 64 61 78 19840550
  48. Diaz-Veliz G Alarcon T Espinoza C Dussaubat N Mora S 1997 Ketanserin and anxiety levels: influence of gender, estrous cycle, ovariectomy and ovarian hormones in female rats Pharmacol Biochem Behav 58 637 42 9329052
  49. Diaz-Veliz G Soto V Dussaubat N Mora S 1989 Influence of the estrous cycle, ovariectomy and estradiol replacement upon the acquisition of conditioned avoidance responses in rats Physiol Behav 46 397 401 2623060
  50. Diaz-Veliz G Urresta F Dussaubat N Mora S 1991 Effects of estradiol replacement in ovariectomized rats on conditioned avoidance responses and other behaviors Physiol Behav 50 61 5 1946732
  51. Doremus-Fitzwater TL Varlinskaya EI Spear LP 2009 Social and non-social anxiety in adolescent and adult rats after repeated restraint Physiol Behav 97 484 94 19345235 PMC2693722
  52. Eaton NR Keyes KM Krueger RF Balsis S Skodol AE Markon KE Grant BF Hasin DS 2012 An invariant dimensional liability model of gender differences in mental disorder prevalence: evidence from a national sample J Abnorm Psychol 121 282 8 21842958 PMC3402021
  53. Ellison PT Reiches MW Shattuck-Faegre H Breakey A Konecna M Urlacher S Wobber V 2012 Puberty as a life history transition Ann Hum Biol 39 352 60 22716225
  54. Eugenin EA Eckardt D Theis M Willecke K Bennett MV Saez JC 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 U S A 98 4190 5 11259646 PMC31201
  55. Farber NB Wozniak DF Price MT Labruyere J Huss J St Peter H Olney JW 1995 Age-specific neurotoxicity in the rat associated with NMDA receptor blockade: potential relevance to schizophrenia? Biol Psychiatry 38 788 96 8750036
  56. Farrell MR Sengelaub DR Wellman CL 2013 Sex differences and chronic stress effects on the neural circuitry underlying fear conditioning and extinction Physiol Behav PMC3812406 23624153
  57. Feder HH Silver R 1974 Activation of lordosis in ovariectomized guinea pigs by free and esterified forms of estrone, estradiol-17 beta and estriol Physiol Behav 13 251 5 4369747
  58. File SE Seth P 2003 A review of 25 years of the social interaction test Eur J Pharmacol 463 35 53 12600701
  59. Gadient RA Otten U 1994 Expression of interleukin-6 (IL-6) and interleukin-6 receptor (IL-6R) mRNAs in rat brain during postnatal development Brain Res 637 10 4 8180786
  60. Galeeva A Tuohimaa P 2001 Analysis of mouse plus-maze behavior modulated by ovarian steroids Behav Brain Res 119 41 7 11164524
  61. Ge X Conger RD Elder GH Jr 2001 Pubertal transition, stressful life events, and the emergence of gender differences in adolescent depressive symptoms Dev Psychol 37 404 17 11370915
  62. Gerocs K Rethelyi M Halasz B 1986 Quantitative analysis of dendritic protrusions in the medial preoptic area during postnatal development Brain Res 391 49 57 3955380
  63. Giedd JN Blumenthal J Jeffries NO Castellanos FX Liu H Zijdenbos A Paus T Evans AC Rapoport JL 1999 Brain development during childhood and adolescence: a longitudinal MRI study Nat Neurosci 2 861 3 10491603
  64. Giedd JN Castellanos FX Rajapakse JC Vaituzis AC Rapoport JL 1997 Sexual dimorphism of the developing human brain Prog Neuropsychopharmacol Biol Psychiatry 21 1185 201 9460086
  65. Girotti M Pace TW Gaylord RI Rubin BA Herman JP Spencer RL 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 81 16431027
  66. Goldstein LA Kurz EM Sengelaub DR 1990 Androgen regulation of dendritic growth and retraction in the development of a sexually dimorphic spinal nucleus J Neurosci 10 935 46 2319307 PMC6570122
  67. Gomez F Manalo S Dallman MF 2004 Androgen-sensitive changes in regulation of restraint-induced adrenocorticotropin secretion between early and late puberty in male rats Endocrinology 145 59 70 14563697
  68. Gomez-Gonzalez B Escobar A 2010 Prenatal stress alters microglial development and distribution in postnatal rat brain Acta Neuropathol 119 303 15 19756668
  69. Gottsch ML Cunningham MJ Smith JT Popa SM Acohido BV Crowley WF Seminara S Clifton DK Steiner RA 2004 A role for kisspeptins in the regulation of gonadotropin secretion in the mouse Endocrinology 145 4073 7 15217982
  70. Graeber MB 2010 Changing face of microglia Science 330 783 8 21051630
  71. Graeber MB Streit WJ 2010 Microglia: biology and pathology Acta Neuropathol 119 89 105 20012873
  72. Grant KE Compas BE Stuhlmacher AF Thurm AE McMahon SD Halpert JA 2003 Stressors and child and adolescent psychopathology: moving from markers to mechanisms of risk Psychol Bull 129 447 66 12784938
  73. Grant KE Compas BE Thurm AE McMahon SD Gipson PY 2004 Stressors and child and adolescent psychopathology: measurement issues and prospective effects J Clin Child Adolesc Psychol 33 412 25 15136206
  74. Green MR Barnes B McCormick CM 2012 Social instability stress in adolescence increases anxiety and reduces social interactions in adulthood in male Long-Evans rats Dev Psychobiol 23001904
  75. Grippo AJ Beltz TG Johnson AK 2003 Behavioral and cardiovascular changes in the chronic mild stress model of depression Physiol Behav 78 703 10 12782226
  76. Guillamon A de Blas MR Segovia S 1988 Effects of sex steroids on the development of the locus coeruleus in the rat Brain Res 468 306 10 3382961
  77. Hanisch UK Kettenmann H 2007 Microglia: active sensor and versatile effector cells in the normal and pathologic brain Nat Neurosci 10 1387 94 17965659
  78. Harris RB Gu H Mitchell TD Endale L Russo M Ryan DH 2004 Increased glucocorticoid response to a novel stress in rats that have been restrained Physiol Behav 81 557 68 15178148
  79. Helmreich DL Morano MI Akil H Watson SJ 1997 Correlation between Changes in Stress-Induced Corticosterone Secretion and GR mRNA Levels Stress 2 101 112 9787259
  80. Herbison AE 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 53 7496395
  81. Hinwood M Tynan RJ Charnley JL Beynon SB Day TA Walker FR 2012 Chronic Stress Induced Remodeling of the Prefrontal Cortex: Structural Re-Organization of Microglia and the Inhibitory Effect of Minocycline Cereb Cortex 22710611
  82. Hou R Baldwin DS 2012 A neuroimmunological perspective on anxiety disorders Hum Psychopharmacol 27 6 14 22213434
  83. Huang GZ Woolley CS 2012 Estradiol acutely suppresses inhibition in the hippocampus through a sex-specific endocannabinoid and mGluR-dependent mechanism Neuron 74 801 8 22681685 PMC3372866
  84. Huttenlocher PR 1979 Synaptic density in human frontal cortex - developmental changes and effects of aging Brain Res 163 195 205 427544
  85. Huttenlocher PR Dabholkar AS 1997 Regional differences in synaptogenesis in human cerebral cortex J Comp Neurol 387 167 78 9336221
  86. Ilin Y Richter-Levin G 2009 Enriched environment experience overcomes learning deficits and depressive-like behavior induced by juvenile stress PLoS One 4 e4329 19180243 PMC2631645
  87. Im-Bolter N Cohen NJ Farnia F 2013 I thought we were good: social cognition, figurative language, and adolescent psychopathology J Child Psychol Psychiatry 23550796
  88. Imwalle DB Gustafsson JA Rissman EF 2005 Lack of functional estrogen receptor beta influences anxiety behavior and serotonin content in female mice Physiol Behav 84 157 63 15642619
  89. Insel TR Miller LP Gelhard RE 1990 The ontogeny of excitatory amino acid receptors in rat forebrain--I. N-methyl-D-aspartate and quisqualate receptors Neuroscience 35 31 43 1972786
  90. Intlekofer KA Petersen SL 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 65 20977928 PMC3024713
  91. Isgor C Kabbaj M Akil H Watson SJ 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 48 15301440
  92. Ismail N Blaustein JD 2013 Pubertal immune challenge blocks the ability of estradiol to enhance performance on cognitive tasks in adult female mice Psychoneuroendocrinology 38 1170 1177 23218519 PMC3604046
  93. Ismail N Garas P Blaustein JD 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 71 21376052 PMC3085923
  94. Ismail N Kumlin AM Blaustein JD 2012 A pubertal immune challenge alters the antidepressant-like effects of chronic estradiol treatment in inbred and outbred adult female mice Neuroscience PMC3567249 23036617
  95. Jacobson-Pick S Richter-Levin G 2010 Differential impact of juvenile stress and corticosterone in juvenility and in adulthood, in male and female rats Behav Brain Res 214 268 76 20561965
  96. Jacobson-Pick S Richter-Levin G 2012 Short- and long-term effects of juvenile stressor exposure on the expression of GABAA receptor subunits in rats Stress 15 416 24 22044189
  97. Jakubowski M Blum M Roberts JL 1991 Postnatal development of gonadotropin-releasing hormone and cyclophilin gene expression in the female and male rat brain Endocrinology 128 2702 8 2036956
  98. Janeway CA Jr 2001 How the immune system works to protect the host from infection: a personal view Proc Natl Acad Sci U S A 98 7461 8 11390983 PMC34691
  99. Jedlicka P Vlachos A Schwarzacher SW Deller T 2008 A role for the spine apparatus in LTP and spatial learning Behav Brain Res 192 12 9 18395274
  100. Johansen JP Cain CK Ostroff LE LeDoux JE 2011 Molecular mechanisms of fear learning and memory Cell 147 509 24 22036561 PMC3215943
  101. John GR Lee SC Brosnan CF 2003 Cytokines: powerful regulators of glial cell activation Neuroscientist 9 10 22 12580336
  102. Johnston AL File SE 1991 Sex differences in animal tests of anxiety Physiol Behav 49 245 50 2062894
  103. Jones KA Thomsen C 2012 The role of the innate immune system in psychiatric disorders Mol Cell Neurosci 23064447
  104. Kalsbeek A Voorn P Buijs RM Pool CW Uylings HB 1988 Development of the dopaminergic innervation in the prefrontal cortex of the rat J Comp Neurol 269 58 72 3361004
  105. Kauffman AS Clifton DK Steiner RA 2007 Emerging ideas about kisspeptin-GPR54 signaling in the neuroendocrine regulation of reproduction Trends Neurosci 30 504 11 17904653
  106. Kendig MD Bowen MT Kemp AH McGregor IS 2011 Predatory threat induces huddling in adolescent rats and residual changes in early adulthood suggestive of increased resilience Behav Brain Res 225 405 14 21855579
  107. Kettenmann H Hanisch UK Noda M Verkhratsky A 2011 Physiology of microglia Physiol Rev 91 461 553 21527731
  108. Konkle AT Baker SL Kentner AC Barbagallo LS Merali Z Bielajew C 2003 Evaluation of the effects of chronic mild stressors on hedonic and physiological responses: sex and strain compared Brain Res 992 227 38 14625061
  109. Korenbrot CC Huhtaniemi IT Weiner RI 1977 Preputial separation as an external sign of pubertal development in the male rat Biol Reprod 17 298 303 889997
  110. Korol DL 2004 Role of estrogen in balancing contributions from multiple memory systems Neurobiol Learn Mem 82 309 23 15464412
  111. Koss WA Einat H Schloesser RJ Manji HK Rubinow DR 2012 Estrogen effects on the forced swim test differ in two outbred rat strains Physiol Behav 106 81 6 22266677 PMC3314120
  112. Krezel W Dupont S Krust A Chambon P Chapman PF 2001 Increased anxiety and synaptic plasticity in estrogen receptor beta -deficient mice Proc Natl Acad Sci U S A 98 12278 82 11593044 PMC59805
  113. Kuhnemann S Brown TJ Hochberg RB MacLusky NJ 1994 Sex differences in the development of estrogen receptors in the rat brain Horm Behav 28 483 91 7729817
  114. Kvetnansky R Sabban EL Palkovits M 2009 Catecholaminergic systems in stress: structural and molecular genetic approaches Physiol Rev 89 535 606 19342614
  115. Laroche J Gasbarro L Herman JP Blaustein JD 2009a Enduring influences of peripubertal/adolescent stressors on behavioral response to estradiol and progesterone in adult female mice Endocrinology 150 3717 25 19372198 PMC2717861
  116. Laroche J Gasbarro L Herman JP Blaustein JD 2009b Reduced behavioral response to gonadal hormones in mice shipped during the peripubertal/adolescent period Endocrinology 150 2351 8 19131570 PMC2671909
  117. Laugero KD Moberg GP 2000 Summation of behavioral and immunological stress: metabolic consequences to the growing mouse Am J Physiol Endocrinol Metab 279 E44 9 10893321
  118. Lemieux A Coe CL Carnes M 2008 Symptom severity predicts degree of T cell activation in adult women following childhood maltreatment Brain Behav Immun 22 994 1003 18396007 PMC2532919
  119. Lenz KM Nugent BM McCarthy MM 2012 Sexual differentiation of the rodent brain: dogma and beyond Front Neurosci 6 26 22363256 PMC3282918
  120. Leslie CA Robertson MW Cutler AJ Bennett JP Jr 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 14 1836980
  121. Leuner B Falduto J Shors TJ 2003 Associative memory formation increases the observation of dendritic spines in the hippocampus J Neurosci 23 659 65 12533625 PMC2740640
  122. Lewis DA Cruz D Eggan S Erickson S 2004 Postnatal development of prefrontal inhibitory circuits and the pathophysiology of cognitive dysfunction in schizophrenia Ann N Y Acad Sci 1021 64 76 15251876
  123. Li C Brake WG Romeo RD Dunlop JC Gordon M Buzescu R Magarinos AM Allen PB Greengard P Luine V McEwen BS 2004 Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice Proc Natl Acad Sci U S A 101 2185 90 14766964 PMC357073
  124. Li X Morrow D Witkin JM 2006 Decreases in nestlet shredding of mice by serotonin uptake inhibitors: comparison with marble burying Life Sci 78 1933 9 16182315
  125. Ling EA Wong WC 1993 The origin and nature of ramified and amoeboid microglia: a historical review and current concepts Glia 7 9 18 8423067
  126. Lohmiller J Sonya P 2006 Reproduction and Breeding Elsevier San Diego
  127. Lu SF McKenna SE Cologer-Clifford A Nau EA Simon NG 1998 Androgen receptor in mouse brain: sex differences and similarities in autoregulation Endocrinology 139 1594 601 9528939
  128. Luine VN 2008 Sex steroids and cognitive function J Neuroendocrinol 20 866 72 18513207
  129. Luine VN Frankfurt M 2012 Estrogens facilitate memory processing through membrane mediated mechanisms and alterations in spine density Front Neuroendocrinol 33 388 402 22981654 PMC3496031
  130. Luine VN Richards ST Wu VY Beck KD 1998 Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters Horm Behav 34 149 62 9799625
  131. Magarinos AM McEwen BS 1995 Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors Neuroscience 69 89 98 8637636
  132. Marcondes FK Miguel KJ Melo LL Spadari-Bratfisch RC 2001 Estrous cycle influences the response of female rats in the elevated plus-maze test Physiol Behav 74 435 40 11790402
  133. Marshall WA Tanner JM 1969 Variations in pattern of pubertal changes in girls Arch Dis Child 44 291 303 5785179 PMC2020314
  134. Marti O Armario A 1997 Influence of Regularity of Exposure to Chronic Stress on the Pattern of Habituation of Pituitary-Adrenal Hormones, Prolactin and Glucose Stress 1 179 189 9787243
  135. Maslova LN Bulygina VV Markel AL 2002 Chronic stress during prepubertal development: immediate and long-lasting effects on arterial blood pressure and anxiety-related behavior Psychoneuroendocrinology 27 549 61 11965354
  136. Mathews IZ Wilton A Styles A McCormick CM 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 40 18342957
  137. McCormick CM Furey BF Child M Sawyer MJ Donohue SM 1998 Neonatal sex hormones have ‘organizational’ effects on the hypothalamic-pituitary-adrenal axis of male rats Brain Res Dev Brain Res 105 295 307 9541747
  138. McCormick CM Green MR 2012 From the stressed adolescent to the anxious and depressed adult: Investigations in rodent models Neuroscience 22967838
  139. McCormick CM Linkroum W Sallinen BJ Miller NW 2002 Peripheral and central sex steroids have differential effects on the HPA axis of male and female rats Stress 5 235 47 12475728
  140. McCormick CM Robarts D Kopeikina K Kelsey JE 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 74 15919386
  141. McCormick CM Smith C Mathews IZ 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 38 17945360
  142. McEwen BS 2000 Allostasis, allostatic load, and the aging nervous system: role of excitatory amino acids and excitotoxicity Neurochem Res 25 1219 31 11059796
  143. McEwen BS Akama KT Spencer-Segal JL Milner TA Waters EM 2012 Estrogen effects on the brain: actions beyond the hypothalamus via novel mechanisms Behav Neurosci 126 4 16 22289042 PMC3480182
  144. Medzhitov R Janeway C Jr 2000 Innate immune recognition: mechanisms and pathways Immunol Rev 173 89 97 10719670
  145. Meyer G Ferres-Torres R Mas M 1978 The effects of puberty and castration on hippocampal dendritic spines of mice. A Golgi study Brain Res 155 108 12 688003
  146. Miller AH Maletic V Raison CL 2009 Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression Biol Psychiatry 65 732 41 19150053 PMC2680424
  147. Mohr MA Sisk CL 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 7 23460698 PMC3607016
  148. Mora S Dussaubat N Diaz-Veliz G 1996 Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats Psychoneuroendocrinology 21 609 20 9044444
  149. Morgan MA Pfaff DW 2001 Effects of estrogen on activity and fear-related behaviors in mice Horm Behav 40 472 82 11716576
  150. Morgan MA Pfaff DW 2002 Estrogen’s effects on activity, anxiety, and fear in two mouse strains Behav Brain Res 132 85 93 11853861
  151. Navarro VM Castellano JM McConkey SM Pineda R Ruiz-Pino F Pinilla L Clifton DK Tena-Sempere M Steiner RA 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 21045176 PMC3774070
  152. Nilsson S Makela S Treuter E Tujague M Thomsen J Andersson G Enmark E Pettersson K Warner M Gustafsson JA 2001 Mechanisms of estrogen action Physiol Rev 81 1535 65 11581496
  153. Novac N Heinzel T 2004 Nuclear receptors: overview and classification Curr Drug Targets Inflamm Allergy 3 335 46 15584884
  154. Nunez JL Jurgens HA Juraska JM 2000 Androgens reduce cell death in the developing rat visual cortex Brain Res Dev Brain Res 125 83 8 11154764
  155. Nunez JL Lauschke DM Juraska JM 2001 Cell death in the development of the posterior cortex in male and female rats J Comp Neurol 436 32 41 11413544
  156. O’Neil MF Moore NA 2003 Animal models of depression: are there any? Hum Psychopharmacol 18 239 54 12766928
  157. Oakley AE Clifton DK Steiner RA 2009 Kisspeptin signaling in the brain Endocr Rev 30 713 43 19770291 PMC2761114
  158. Ogawa S Eng V Taylor J Lubahn DB Korach KS Pfaff DW 1998 Roles of estrogen receptor-alpha gene expression in reproduction-related behaviors in female mice Endocrinology 139 5070 81 9832446
  159. Ojeda SR Lomniczi A Mastronardi C Heger S Roth C Parent AS Matagne V Mungenast AE 2006 Minireview: the neuroendocrine regulation of puberty: is the time ripe for a systems biology approach? Endocrinology 147 1166 74 16373420
  160. Ojeda SR Urbanski HF Puberty in the Rat Knobil E Neill J The Physiology of Reproduction Raven Press New York 1994 363 409
  161. Ojeda SR Wheaton JE Jameson HE McCann SM 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 8 770154
  162. Okada M Hayashi N Kometani M Nakao K Inukai T 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 6 9032138
  163. Olesen KM Ismail N Merchasin ED Blaustein JD 2011 Long-term alteration of anxiolytic effects of ovarian hormones in female mice by a peripubertal immune challenge Horm Behav 60 318 26 21722643 PMC3166431
  164. Olivera-Lopez JI Molina-Hernandez M Tellez-Alcantara NP Jaramillo MT 2008 Estradiol and neuropeptide Y (intra-lateral septal) reduce anxiety-like behavior in two animal models of anxiety Peptides 29 1396 403 18499302
  165. Osterlund MK 2010 Underlying mechanisms mediating the antidepressant effects of estrogens Biochim Biophys Acta 1800 1136 44 19900508
  166. Palanza P Gioiosa L Parmigiani S 2001 Social stress in mice: gender differences and effects of estrous cycle and social dominance Physiol Behav 73 411 20 11438369
  167. Pandaranandaka J Poonyachoti S Kalandakanond-Thongsong S 2006 Anxiolytic property of estrogen related to the changes of the monoamine levels in various brain regions of ovariectomized rats Physiol Behav 87 828 35 16545402
  168. Pandaranandaka J Poonyachoti S Kalandakanond-Thongsong S 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 8 19046994
  169. Paolicelli RC Gross CT 2011 Microglia in development: linking brain wiring to brain environment Neuron Glia Biol 7 77 83 22857738
  170. Parent AS Matagne V Bourguignon JP 2005 Control of puberty by excitatory amino acid neurotransmitters and its clinical implications Endocrine 28 281 6 16388117
  171. Pariante CM Miller AH 2001 Glucocorticoid receptors in major depression: relevance to pathophysiology and treatment Biol Psychiatry 49 391 404 11274650
  172. Parker CR Jr Mahesh VB 1976 Hormonal events surrounding the natural onset of puberty in female rats Biol Reprod 14 347 53 175861
  173. Parker LN 1991 Adrenarche Endocrinol Metab Clin North Am 20 71 83 2029889
  174. Parsons B Rainbow TC MacLusky NJ McEwen BS 1982 Progestin receptor levels in rat hypothalamic and limbic nuclei J Neurosci 2 1446 52 6889633 PMC6564403
  175. Patton GC Hibbert ME Carlin J Shao Q Rosier M Caust J Bowes G 1996 Menarche and the onset of depression and anxiety in Victoria, Australia J Epidemiol Community Health 50 661 6 9039386 PMC1060384
  176. Patton GC Viner R 2007 Pubertal transitions in health Lancet 369 1130 9 17398312
  177. Paus T Keshavan M Giedd JN 2008 Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9 947 57 19002191 PMC2762785
  178. Peleg-Raibstein D Feldon J 2011 Differential effects of post-weaning juvenile stress on the behaviour of C57BL/6 mice in adolescence and adulthood Psychopharmacology (Berl) 214 339 51 20803000
  179. Perry VH Newman TA Cunningham C 2003 The impact of systemic infection on the progression of neurodegenerative disease Nat Rev Neurosci 4 103 12 12563281
  180. Petanjek Z Judas M Simic G Rasin MR Uylings HB Rakic P Kostovic I 2011 Extraordinary neoteny of synaptic spines in the human prefrontal cortex Proc Natl Acad Sci U S A 108 13281 6 21788513 PMC3156171
  181. Picazo O Estrada-Camarena E Hernandez-Aragon A 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 94 16356491
  182. Pignatelli D Xiao F Gouveia AM Ferreira JG Vinson GP 2006 Adrenarche in the rat J Endocrinol 191 301 8 17065412
  183. Pinos H Collado P Rodriguez-Zafra M Rodriguez C Segovia S Guillamon A 2001 The development of sex differences in the locus coeruleus of the rat Brain Res Bull 56 73 8 11604252
  184. Plant TM Barker-Gibb ML 2004 Neurobiological mechanisms of puberty in higher primates Hum Reprod Update 10 67 77 15005465
  185. Pousset F 1994 Developmental expression of cytokine genes in the cortex and hippocampus of the rat central nervous system Brain Res Dev Brain Res 81 143 6 7805281
  186. Rachman IM Unnerstall JR Pfaff DW Cohen RS 1998 Estrogen alters behavior and forebrain c-fos expression in ovariectomized rats subjected to the forced swim test Proc Natl Acad Sci U S A 95 13941 6 9811905 PMC24977
  187. Rainbow TC Parsons B McEwen BS 1982 Sex differences in rat brain oestrogen and progestin receptors Nature 300 648 9 7144917
  188. Raivich G 2005 Like cops on the beat: the active role of resting microglia Trends Neurosci 28 571 3 16165228
  189. Ramaswamy S Guerriero KA Gibbs RB Plant TM 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 95 18511511 PMC2553371
  190. Redei E Li L Halasz I McGivern RF Aird F 1994 Fast glucocorticoid feedback inhibition of ACTH secretion in the ovariectomized rat: effect of chronic estrogen and progesterone Neuroendocrinology 60 113 23 7969768
  191. Reiss AL Abrams MT Singer HS Ross JL Denckla MB 1996 Brain development, gender and IQ in children. A volumetric imaging study Brain 119 Pt 5 1763 74 8931596
  192. Roberti JW 2004 A review of behavioral and biological correlates of sensation seeking Journal of Research in Personality 38 256 279
  193. Rocha BA Fleischer R Schaeffer JM Rohrer SP Hickey GJ 2005 17 Beta-estradiol-induced antidepressant-like effect in the forced swim test is absent in estrogen receptor-beta knockout (BERKO) mice Psychopharmacology (Berl) 179 637 43 15645223
  194. Romeo RD Bellani R Karatsoreos IN Chhua N Vernov M Conrad CD McEwen BS 2006 Stress history and pubertal development interact to shape hypothalamic-pituitary-adrenal axis plasticity Endocrinology 147 1664 74 16410296
  195. Romeo RD Bellani R McEwen BS 2005 Stress-induced progesterone secretion and progesterone receptor immunoreactivity in the paraventricular nucleus are modulated by pubertal development in male rats Stress 8 265 71 16423715
  196. Romeo RD Karatsoreos IN Jasnow AM McEwen BS 2007 Age- and stress-induced changes in corticotropin-releasing hormone mRNA expression in the paraventricular nucleus of the hypothalamus Neuroendocrinology 85 199 206 17505125
  197. Romeo RD Lee SJ Chhua N McPherson CR McEwen BS 2004a Testosterone cannot activate an adult-like stress response in prepubertal male rats Neuroendocrinology 79 125 32 15103225
  198. Romeo RD Lee SJ McEwen BS 2004b Differential stress reactivity in intact and ovariectomized prepubertal and adult female rats Neuroendocrinology 80 387 93 15741744
  199. Roy V Chapillon P 2004 Further evidences that risk assessment and object exploration behaviours are useful to evaluate emotional reactivity in rodents Behav Brain Res 154 439 48 15313032
  200. Salim S Chugh G Asghar M 2012 Inflammation in anxiety Adv Protein Chem Struct Biol 88 1 25 22814704

200 of 285 shown

Cited by

Sorted by citations

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
  • Social Sciences › Psychology › Social Psychology › 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

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