Chronic Stress- and Sex-Specific Neuromorphological and Functional Changes in Limbic Structures
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Hamann S, Canli T (2004) Individual differences in emotion processing. Curr Opin Neurobiol 14(2):233–238
Eichenbaum H, Yonelinas AP, Ranganath C (2007) The medial temporal lobe and recognition memory. Annu Rev Neurosci 30:123–152
Lipton PA, Eichenbaum H (2008) Complementary roles of hippocampus and medial entorhinal cortex in episodic memory. Neural Plast 2008:1–8
Bird CM, Burgess N (2008) The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 9(3):182–194
O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon, Oxford
Kesner RP, Hopkins RO (2006) Mnemonic functions of the hippocampus: a comparison between animals and humans. Biol Psychol 73(1):3–18
Aggleton JP, Hunt PR, Rawlins JN (1986) The effects of hippocampal lesions upon spatial and non-spatial tests of working memory. Behav Brain Res 19:133–146
Kessels RP, de Haan EH, Kappelle LJ, Postma A (2001) Varieties of human spatial memory: a meta-analysis on the effects of hippocampal lesions. Brain Res Brain Res Rev 35(3):295–303
Morris RGM, Garrud P, Rawlins JNP, O’Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681–683
McEwen BS, Milner TA (2007) Hippocampal formation: shedding light on the influence of sex and stress on the brain. Brain Res Rev 55(2):343–355
Luine VN, Beck KD, Bowman RE, Frankfurt M, Maclusky NJ (2007) Chronic stress and neural function: accounting for sex and age. J Neuroendocrinol 19(10):743–751
Ragozzino ME (2007) The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatum to behavioral flexibility. Ann N Y Acad Sci 1121:355–375
Dalley JW, Cardinal RN, Robbins TW (2004) Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 28(7):771–784
Cahill L, McGaugh JL (1998) Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci 21:294–299
LeDoux J (2000) The amygdala and emotion: a view through fear. In: Aggleton JP (ed) The amygdala: a functional analysis. Oxford University Press, New York, pp 289–310
Diamond DM, Campbell AM, Park CR, Halonen J, Zoladz PR (2007) The temporal dynamics model of emotional memory processing: a synthesis on the neurobiological basis of stress-induced amnesia, flashbulb and traumatic memories, and the Yerkes–Dodson law. Neural Past 2007:1–33
Quirk GJ, Russo GK, Barron JL, Lebron K (2000) The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J Neurosci 20(16):6225–6231
Gao YJ, Ren WH, Zhang YQ, Zhao ZQ (2004) Contributions of the anterior cingulate cortex and amygdala to pain- and fear-conditioned place avoidance in rats. Pain 110(1–2):343–353
Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106(2):274–285
Conrad CD, Magariños AM, LeDoux JE, McEwen BS (1999) Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci 113(5):902–913
Conrad CD, MacMillan DD II, Tsekhanov S, Wright RL, Baran SE, Fuchs RE (2004) Influence of chronic corticosterone and glucocorticoid receptor antagonism in the amygdala on fear conditioning. Neurobiol Learn Mem 81(3):185–199
Miracle AD, Brace MF, Huyck KD, Singler SA, Wellman CL (2006) Chronic stress impairs recall of extinction of conditioned fear. Neurobiol Learn Mem 85(3):213–218
Garcia R, Spennato G, Nilsson-Todd L, Moreau JL, Deschaux O (2008) Hippocampal low-frequency stimulation and chronic mild stress similarly disrupt fear extinction memory in rats. Neurobiol Learn Mem 89(4):560–566
Baran SE, Armstrong CE, Niren DC, Hanna JJ, Conrad CD (2009) Chronic stress and sex differences on the recall of fear conditioning and extinction. Neurobiol Learn Mem 91:323–332
Amaral DG, Lavenex P (2007) Hippocampal neuroanatomy. In: Andersen P, Morris RG, Amaral DG, Bliss T, O’Keefe J (eds) The hippocampus book. Oxford University Press, New York, pp 37–114
Smith TC, Wingard DL, Ryan MA, Kritz-Silverstein D, Slymen DJ, Sallis JF (2008) Prior assault and posttraumatic stress disorder after combat deployment. Epidemiology 19(3):505–512
Weber K, Rockstroh B, Borgelt J, Awiszus B, Popov T, Hoffmann K, Schonauer K, Watzl H, Propster K (2008) Stress load during childhood affects psychopathology in psychiatric patients. BMC Psychiatry 8:63
Kendler KS, Prescott CA (1999) A population-based twin study of lifetime major depression in men and women. Arch Gen Psychiatry 56(1):39–44
Patten SB, Stuart HL, Russell ML, Maxwell CJ, Arboleda-Florez J (2003) Epidemiology of major depression in a predominantly rural health region. Soc Psychiatry Psychiatr Epidemiol 38(7):360–365
Bale TL (2006) Stress sensitivity and the development of affective disorders. Horm Behav 50(4):529–533
Hammen C, Kim EY, Eberhart NK, Brennan PA (2009) Chronic and acute stress and the prediction of major depression in women. Depress Anxiety (in press). doi: 10.1002/da.20571
Gold PW, Chrousos GP (2002) Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states. Mol Psychiatry 7(3):254–275
Breslau N, Davis GC, Andreski P, Peterson EL, Schultz LR (1997) Sex differences in posttraumatic stress disorder. Arch Gen Psychiatry 54(11):1044–1048
Chida Y, Hamer M (2008) Chronic psychosocial factors and acute physiological responses to laboratory-induced stress in healthy populations: a quantitative review of 30 years of investigations. Psychol Bull 134(6):829–885
Weber K, Rockstroh B, Borgelt J, Awiszus B, Popov T, Hoffmann K, Schonauer K, Watzl H, Propster K (2008) Stress load during childhood affects psychopathology in psychiatric patients. BMC Psychiatry 8:63–72
Agid O, Kohn Y, Lerer B (2000) Environmental stress and psychiatric illness. Biomed Pharmacother 54(3):135–141
De Bellis MD, Baum AS, Birmaher B, Keshavan MS, Eccard CH, Boring AM, Jenkins FJ, Ryan ND (1999) A.E. Bennett Research Award. Developmental traumatology. Part I: biological stress systems. Biol Psychiatry 45(10):1259–1270
De Bellis MD, Thomas LA (2003) Biologic findings of post-traumatic stress disorder and child maltreatment. Curr Psychiatry Rep 5(2):108–117
Reus VI, Wolkowitz OM (2001) Antiglucocorticoid drugs in the treatment of depression. Expert Opin Investig Drugs 10:1789–1796
Brown ES, Varghese FP, McEwen BS (2004) Association of depression with medical illness: does cortisol play a role? Biol Psychiatry 55(1):1–9
Swaab DF, Bao AM, Lucassen PJ (2005) The stress system in the human brain in depression and neurodegeneration. Ageing Res Rev 4(2):141–194
Gomez RG, Fleming SH, Keller J, Flores B, Kenna H, Debattista C, Solvason B, Schatzberg AF (2006) The neuropsychological profile of psychotic major depression and its relation to cortisol. Biol Psychiatry 60:472–478
Reppermund S, Zihl J, Lucae S, Horstmann S, Kloiber S, Holsboer F, Ising M (2007) Persistent cognitive impairment in depression: the role of psychopathology and altered hypothalamic–pituitary–adrenocortical (HPA) system regulation. Biol Psychiatry 62(5):400–406
Beck AT (2008) The evolution of the cognitive model of depression and its neurobiological correlates. Am J Psychiatry 165(8):969–977
Pardon MC, Rattray I (2008) What do we know about the long-term consequences of stress on ageing and the progression of age-related neurodegenerative disorders? Neurosci Biobehav Rev 32(6):1103–1120
Sotiropoulos I, Cerqueira JJ, Catania C, Takashima A, Sousa N, Almeida OF (2008) Stress and glucocorticoid footprints in the brain—the path from depression to Alzheimer’s disease. Neurosci Biobehav Rev 32(6):1161–1173
Willner P (1997) Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology 134:319–329
McEwen BS, Weiss JM, Schwartz LS (1968) Selective retention of corticosterone by limbic structures in rat brain. Nature 220:911–912
McEwen BS, Weiss JM, Schwartz LS (1969) Uptake of corticosterone by rat brain and its concentration by certain limbic structures. Brain Res 16:227–241
Sapolsky RM (2000) Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 57:925–935
Bremner JD, Elzinga B, Schmahl C, Vermetten E (2008) Structural and functional plasticity of the human brain in posttraumatic stress disorder. Prog Brain Res 167:171–186
Bremner JD (2006) The relationship between cognitive and brain changes in posttraumatic stress disorder. Ann N Y Acad Sci 1071:80–86
Karl A, Schaefer M, Malta LS, Dörfel D, Rohleder N, Werner A (2006) A meta-analysis of structural brain abnormalities in PTSD. Neurosci Biobehav Rev 30:1004–1031
Gilbertson MW, Shenton ME, Ciazewski A, Kasai K, Lasko NB, Orr SP, Pitman RK (2002) Smaller hippocampal volume predicts pathological vulnerability to psychological trauma. Nat Neurosci 5:1242–1247
Lindauer RJ, Vlieger EJ, Jalink M, Olff M, Carlier IV, Majoie CB, den Heeten GJ, Gersons BP (2004) Smaller hippocampal volume in Dutch police officers with posttraumatic stress disorder. Biol Psychiatry 56(5):356–363
Wignall EL, Dickson JM, Vaughan P, Farrow TF, Wilkinson ID, Hunter MD, Woodruff PW (2004) Smaller hippocampal volume in patients with recent-onset posttraumatic stress disorder. Biol Psychiatry 56(11):832–836
Brown ES, Rush AJ, McEwen BS (1999) Hippocampal remodeling and damage by corticosteroids: implications for mood disorders. Neuropsychopharmacology 21:474–484
Bremner JD, Narayan M, Anderson ER, Staib LH, Miller HL, Charney DS (2000) Hippocampal volume reduction in major depression. Am J Psychiatry 157(1):115–117
Sheline YI, Gado MH, Kraemer HC (2003) Untreated depression and hippocampal volume loss. Am J Psychiatr 160(8):1516–1518
Campbell S, Marriott M, Nahmias C, MacQueen GM (2004) Lower hippocampal volume in patients suffering from depression: a meta-analysis. Am J Psychiatry 161(4):598–607
Lange C, Irle E (2004) Enlarged amygdala volume and reduced hippocampal volume in young women with major depression. Psychol Med 34(6):1059–1064
Vasic N, Walter H, Hose A, Wolf RC (2008) Gray matter reduction associated with psychopathology and cognitive dysfunction in unipolar depression: a voxel-based morphometry study. J Affect Disord 109(1–2):107–116
Sheline YI, Wang PW, Gado MH, Csernansky JC, Vannier MW (1996) Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci U S A 93:3908–3913
Vakili K, Pillay SS, Lafer B, Fava M, Renshaw PF, Bonello-Cintron CM, Yurgelun-Todd DA (2000) Hippocampal volume in primary unipolar major depression: a magnetic resonance imaging study. Biol Psychiatry 47(12):1087–1090
von Gunten A, Fox NC, Cipolotti L, Ron MA (2000) A volumetric study of hippocampus and amygdala in depressed patients with subjective memory problems. J Neuropsychiatry Clin Neurosci 12(4):493–498
Frodl T, Meisenzahl EM, Zetzsche T, Born C, Groll C, Jager M, Leinsinger G, Bottlender R, Hahn K, Moller HJ (2002) Hippocampal changes in patients with a first episode of major depression. Am J Psychiatry 159(7):1112–1118
Keller J, Shen L, Gomez RG, Garrett A, Solvason HB, Reiss A, Schatzberg AF (2008) Hippocampal and amygdalar volumes in psychotic and nonpsychotic unipolar depression. Am J Psychiatr 165(7):872–880
Sheline YI, Mittler BL, Mintun MA (2002) The hippocampus and depression. Eur Psychiatry 17(Suppl 3):300–305
Frodl TS, Koutsouleris N, Bottlender R, Born C, Jager M, Scupin I, Reiser M, Moller HJ, Meisenzahl EM (2008) Depression-related variation in brain morphology over 3 years: effects of stress? Arch Gen Psychiatry 65(10):1156–1165
Ahima RS, Harlan RE (1990) Charting of type II glucocorticoid receptor-like immunoreactivity in the rat central nervous system. Neuroscience 39(3):579–604
Ahima RS, Harlan RE (1991) Differential corticosteroid regulation of type II glucocorticoid receptor-like immunoreactivity in the rat central nervous system: topography and implications. Endocrinology 129(1):226–236
Ahima R, Krozowski Z, Harlan R (1991) Type I corticosteroid receptor-like immunoreactivity in the rat CNS: distribution and regulation by corticosteroids. J Comp Neurol 313(3):522–538
Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, Cullinan WE (2003) Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24(3):151–180
Bremner JD, Vythilingam M, Vermetten E, Nazeer A, Adil J, Khan S, Staib LH, Charney DS (2002) Reduced volume of orbitofrontal cortex in major depression. Biol Psychiatry 51(4):273–279
Coryell W, Nopoulos P, Drevets W, Wilson T, Andreasen NC (2005) Subgenual prefrontal cortex volumes in major depressive disorder and schizophrenia: diagnostic specificity and prognostic implications. Am J Psychiatry 162(9):1706–1712
Konarski JZ, McIntyre RS, Kennedy SH, Rafi-Tari S, Soczynska JK, Ketter TA (2008) Volumetric neuroimaging investigations in mood disorders: bipolar disorder versus major depressive disorder. Bipolar Disord 10(1):1–37
Brown ES, Woolston DJ, Frol AB (2008) Amygdala volume in patients receiving chronic corticosteroid therapy. Biol Psychiatry 63(7):705–709
Sheline YI, Gado MH, Price JL (1998) Amygdala core nuclei volumes are decreased in recurrent major depression. NeuroReport 9(9):2023–2028
Yoshikawa E, Matsuoka Y, Yamasue H, Inagaki M, Nakano T, Akechi T, Kobayakawa M, Fujimori M, Nakaya N, Akizuki N, Imoto S, Murakami K, Kasai K, Uchitomi Y (2006) Prefrontal cortex and amygdala volume in first minor or major depressive episode after cancer diagnosis. Biol Psychiatry 59(8):707–712
Frodl T, Meisenzahl E, Zetzsche T, Bottlender R, Born C, Groll C, Jager M, Leinsinger G, Hahn K, Moller HJ (2002) Enlargement of the amygdala in patients with a first episode of major depression. Biol Psychiatry 51(9):708–714
Ramel W, Goldin PR, Eyler LT, Brown GG, Gotlib IH, McQuaid JR (2007) Amygdala reactivity and mood-congruent memory in individuals at risk for depressive relapse. Biol Psychiatry 61(2):231–239
Kemp AH, Felmingham K, Das P, Hughes G, Peduto AS, Bryant RA, Williams LM (2007) Influence of comorbid depression on fear in posttraumatic stress disorder: an fMRI study. Psychiatry Res 155(3):265–259
Shin LM, Rauch SL, Pitman RK (2006) Amygdala, medial prefrontal cortex, and hippocampal function in PTSD. Ann N Y Acad Sci 1071:67–79
Shin LM, Wright CI, Cannistraro PA, Wedig MM, McMullin K, Martis B, Macklin ML, Lasko NB, Cavanagh SR, Krangel TS, Orr SP, Pitman RK, Whalen PJ, Rauch SL (2005) A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Arch Gen Psychiatry 62(3):273–281
Woon FL, Hedges DW (2008) Hippocampal and amygdala volumes in children and adults with childhood maltreatment-related posttraumatic stress disorder: a meta-analysis. Hippocampus 18(8):729–736
Becker JB, Arnold AP, Berkley KJ, Blaustein JD, Eckel LA, Hampson E, Herman JP, Marts S, Sadee W, Steiner M, Taylor J, Young E (2005) Strategies and methods for research on sex differences in brain and behavior. Endocrinology 146:1650–1673
Olff M, Langeland W, Draijer N, Gersons BP (2007) Gender differences in posttraumatic stress disorder. Psychol Bull 133(2):183–204
Richter R, Flowers T (2008) Gendered dimensions of disaster care: critical distinctions in female psychosocial needs, triage, pain assessment, and care. Am J Disaster Med 3(1):31–37
Heller W (1993) Gender differences in depression: perspectives from neuropsychology. J Affect Disord 29(2–3):129–143
Kessler RC, McGonagle KA, Swartz M, Blazer DG, Nelson CB (1993) Sex and depression in the National Comorbidity Survey. I: Lifetime prevalence, chronicity and recurrence. J Affect Disord 29(2-3):85–96
Weissman MM, Bland R, Joyce PR, Newman S, Wells JE, Wittchen HU (1993) Sex differences in rates of depression: cross-national perspectives. J Affect Disord 29(2–3):77–84
Gao S, Hendrie HC, Hall KS, Hui S (1998) The relationships between age, sex, and the incidence of dementia and Alzheimer disease: a meta-analysis. Arch Gen Psychiatry 55(9):809–815
Azad NA, Al Bugami M, Loy-English I (2007) Gender differences in dementia risk factors. Gend Med 4(2):120–129
Altemus KL, Almi CR (1997) Neonatal hippocampal damage in rats: long-term spatial memory deficits and associations with magnitude of hippocampal damage. Hippocampus 7:403–414
Parry BL, Javeed S, Laughlin GA, Hauger R, Clopton P (2000) Cortisol circadian rhythms during the menstrual cycle and with sleep deprivation in premenstrual dysphoric disorder and normal control subjects. Biol Psychiatry 48(9):920–931
Kajantie E, Phillips DI (2006) The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology 31(2):151–178
Goldstein JM, Jerram M, Poldrack R, Ahern T, Kennedy DN, Seidman LJ, Makris N (2005) Hormonal cycle modulates arousal circuitry in women using functional magnetic resonance imaging. J Neurosci 25(40):9309–9316
Protopopescu X, Pan H, Altemus M, Tuescher O, Polanecsky M, McEwen B, Silbersweig D, Stern E (2005) Orbitofrontal cortex activity related to emotional processing changes across the menstrual cycle. Proc Natl Acad Sci U S A 102(44):16060–16065
Genazzani AR, Pluchino N, Luisi S, Luisi M (2007) Estrogen, cognition and female ageing. Hum Reprod Update 13(2):175–187
Garcia-Bueno B, Caso JR, Leza JC (2008) Stress as a neuroinflammatory condition in brain: damaging and protective mechanisms. Neurosci Biobehav Rev 32(6):1136–1151
Buynitsky T, Mostofsky DI (2009) Restraint stress in biobehavioral research: recent developments. Neurosci Biobehav Rev 33:1089–1098
Conrad CD, Galea LAM, Kuroda Y, McEwen BS (1996) Chronic stress impairs rat spatial memory on the Y-maze, and this effect is blocked by tianeptine pretreatment. Behav Neurosci 110(6):1321–1334
Wright RL, Conrad CD (2005) Chronic stress leaves novelty-seeking intact while impairing spatial recognition memory in the Y-maze. Stress 8(2):151–154
Wright RL, Lightner EN, Harman JS, Meijer OC, Conrad CD (2006) Attenuating corticosterone levels on the day of memory assessment prevents chronic stress-induced impairments in spatial memory. Eur J NeuroSci 24:595–605
Kleen JK, Sitomer MT, Killeen PR, Conrad CD (2006) Chronic stress impairs spatial memory and motivation for reward without disrupting motor ability and motivation to explore. Behav Neurosci 120(4):842–851
Bellani R, Luecken L, Conrad CD (2006) Peripubertal anxiety profile can predict spatial memory impairments following chronic stress. Behav Brain Res 166(2):263–270
Dranovsky A, Hen R (2006) Hippocampal neurogenesis: regulation by stress and antidepressants. Biol Psychiatry 59(12):1136–1143
Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22:6810–6818
McLaughlin KJ, Gomez JL, Baran SE, Conrad CD (2007) The effects of chronic stress on hippocampal morphology and function: an evaluation of chronic restraint paradigms. Brain Res 1161:56–64
Magariños AM, McEwen BS, Flügge G, Fuchs E (1996) Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 16:3534–3540
Cook SC, Wellman CL (2004) Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 60(2):236–248
Brown SM, Henning S, Wellman CL (2005) Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cereb Cortex 15(11):1714–1722
Radley JJ, Sisti HM, Hao J, Rocher AB, McCall T, Hof PR, McEwen BS, Morrison JH (2004) Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 125:1–6
Vyas A, Jadhav S, Chattarji S (2006) Prolonged behavioral stress enhances synaptic connectivity in the basolateral amygdala. Neuroscience 143(2):387–393
Cui H, Sakamoto H, Higashi S, Kawata M (2008) Effects of single-prolonged stress on neurons and their afferent inputs in the amygdala. Neuroscience 152(3):703–712
Colla M, Kronenberg G, Deuschle M, Meichel K, Hagen T, Bohrer M, Heuser I (2007) Hippocampal volume reduction and HPA-system activity in major depression. J Psychiatry Res 41(7):553–560
Watanabe Y, Gould E, Daniels DC, Cameron H, McEwen BS (1992) Tianeptine attenuates stress-induced morphological changes in the hippocampus. Eur J Pharmacol 222:157–162
Luo L, Tan RX (2001) Fluoxetine inhibits dendrite atrophy of hippocampal neurons by decreasing nitric oxide synthase expression in rat depression model. Acta Pharmacol Sin 22(10):865–870
Bao AM, Meynen G, Swaab DF (2008) The stress system in depression and neurodegeneration: focus on the human hypothalamus. Brain Res Rev 57:531–553
Purves D, Lichtman JW (1985) Geometrical differences among homologous neurons in mammals. Science 228(4697):298–302
Schaefer AT, Larkum ME, Sakmann B, Roth A (2003) Coincidence detection in pyramidal neurons is tuned by their dendritic branching pattern. J Neurophysiol 89(6):3143–3154
Spruston N (2008) Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 9(3):206–221
Cove J, Blinder P, Baranes D (2009) Contacts among non-sister dendritic branches at bifurcations shape neighboring dendrites and pattern their synaptic inputs. Brain Res 1251:30–41
Martinez JL Jr, Barea-Rodriguez EJ (1997) How the brain stores information: Hebbian mechanisms. In: Lueer G, Lass U (eds) Erinnern und Behalten Wege zur Erforschung des menschlichen gedaechtnisses. Vandenhoeck & Ruprecht, Goettingen, pp 39–59
Conrad CD (2006) What is the functional significance of chronic stress-induced CA3 dendritic retraction within the hippocampus? Behav Cogn Neurosci Rev 5(1):41–60
Pittenger C, Duman RS (2008) Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 33(1):88–109
Calabrese F, Molteni R, Racagni G, Riva MA (2009) Neuronal plasticity: a link between stress and mood disorders. Psychoneuroendocrinology (in press). doi: 10.1016/j.psyneuen.2009.05.014
Grossman AW, Churchill JD, McKinney BC, Kodish IM, Otte SL, Greenough WT (2003) Experience effects on brain development: possible contributions to psychopathology. J Child Psychol Psychiatry 44(1):33–63
Fiala JC, Spacek J, Harris KM (2002) Dendritic spine pathology: cause or consequence of neurological disorders? Brain Res Rev 39(1):29–54
Sjostrom PJ, Rancz EA, Roth A, Hausser M (2008) Dendritic excitability and synaptic plasticity. Physiol Rev 88(2):769–840
Viau V (2002) Functional cross-talk between the hypothalamic–pituitary–gonadal and –adrenal axes. J Neuroendocrinol 14(6):506–513
Altemus M, Redwine L, Leong Y, Yoshikawa T, Yehuda R, Detera-Wadleigh S, Murphy DL (1997) Reduced sensitivity to glucocorticoid feedback and reduced glucocorticoid receptor mRNA expression in the luteal phase of the menstrual cycle. Neuropsychopharmacology 17:100–109
Viau V, Meaney MJ (1991) Variations in the hypothalamic–pituitary–adrenal response to stress during the estrous cycle in the rat. Endocrinology 129(5):2503–2511
Atkinson HC, Waddell BJ (1997) Circadian variation in basal plasma corticosterone and adrenocorticotropin in the rat: sexual dimorphism and changes across the estrous cycle. Endocrinology 138(9):3842–3848
Haim S, Shakhar G, Rossene E, Taylor AN, Ben-Eliyahu S (2003) Serum levels of sex hormones and corticosterone throughout 4- and 5-day estrous cycles in Fischer 344 rats and their simulation in ovariectomized females. J Endocrinol Invest 26(10):1013–1022
Conrad CD, Jackson JL, Wieczorek L, Baran SE, Harman JS, Wright RL, Korol DL (2004) Acute restraint stress impairs spatial memory in male but not female rats: influence of estrous cycle. Pharmacol Biochem Behav 78(3):569–579
Dalla C, Antoniou K, Drossopoulou G, Xagoraris M, Kokras N, Sfikakis A, Papadopoulou-Daifoti Z (2005) Chronic mild stress impact: are females more vulnerable? Neuroscience 135(3):703–714
McEwen BS, Conrad CD, Kuroda Y, Frankfurt M, Magariños AM, McKittrick C (1997) Prevention of stress-induced morphological and cognitive consequences. Eur Neuropsychopharm 7:S323–S328
McEwen BS, Magariños AM (1997) Stress effects on morphology and function of the hippocampus. Ann N Y Acad Sci 821:271–284
McEwen BS (2005) Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 54(5 Suppl 1):20–23
Lambert KG, Buckelew SK, Staffiso-Sandoz G, Gaffga S, Carpenter W, Fisher J, Kinsely CH (1998) Activity-stress induces atrophy of apical dendrites of hippocampal pyramidal neurons in male rats. Physiol Behav 65:43–49
Sousa N, Lukoyanov NV, Madeira MD, Almeida OFX, Paula-Barbosa MM (2000) Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97:253–266
Woolley CS, Gould E, McEwen BS (1990) Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 531:225–231
Magariños AM, McEwen BS (1995) Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience 69(1):83–88
Sandi C, Davies HA, Cordero MI, Rodriquez JJ, Popov VI, Stewart MG (2003) Rapid reversal of stress induced loss of synapses in CA3 of rat hippocampus following water maze training. Eur J NeuroSci 17:2447–2456
Fuchs E, Uno H, Flügge G (1995) Chronic psychosocial stress induces morphological alterations in hippocampal pyramidal neurons of the tree shrew. Brain Res 673(2):275–282
Conrad CD, McLaughlin KJ, Harman JS, Foltz C, Wieczorek L, Lightner E, Wright RL (2007) Chronic glucocorticoids increase hippocampal vulnerability to neurotoxicity under conditions that produce CA3 dendritic retraction but fail to impair spatial recognition memory. J Neurosci 27(31):8278–8285
Luine VN, Spencer RL, McEwen BS (1993) Effects of chronic corticosterone ingestion on spatial memory performance and hippocampal serotonergic function. Brain Res 616:65–70
Luine V, Villegas M, Martinez C, McEwen BS (1994) Repeated stress causes reversible impairments of spatial memory performance. Brain Res 639:167–170
Park CR, Campbell AM, Diamond DM (2001) Chronic psychosocial stress impairs learning and memory and increases sensitivity to yohimbine in rats. Biol Psychiatry 50:994–1004
Gerges NZ, Alzoubi KH, Park CR, Diamond DM, Alkadhi KA (2004) Adverse effect of the combination of hypothyroidism and chronic psychosocial stress on hippocampus-dependent memory in rats. Behav Brain Res 155(1):77–84
Srivareerat M, Tran TT, Alzoubi KH, Alkadhi KA (2009) Chronic psychosocial stress exacerbates impairment of cognition and long-term potentiation in beta-amyloid rat model of Alzheimer’s disease. Biol Psychiatry 65(11):918–926
Sunanda, Shankaranarayana Rao BS, Raju TR (2000) Chronic restraint stress impairs acquisition and retention of spatial memory task in rats. Curr Sci 79:14581–1584
Ohl F, Fuchs E (1999) Differential effects of chronic stress on memory processes in the tree shrew. Cogn Brain Res 7:379–387
Venero C, Tilling T, Hermans-Borgmeyer I, Schmidt R, Schachner M, Sandi C (2002) Chronic stress induces opposite changes in the mRNA expression of the cell adhesion molecules NCAM and L1. Neuroscience 115(4):1211–1219
Wright RL, Conrad CD (2008) Enriched environment prevents chronic stress-induced spatial learning and memory deficits. Behav Brain Res 187(1):41–47
Ma WP, Cao J, Tian M, Cui MH, Han HL, Yang YX, Xu L (2007) Exposure to chronic constant light impairs spatial memory and influences long-term depression in rats. Neurosci Res 59(2):224–230
Song L, Che W, Min-Wei W, Murakami Y, Matsumoto K (2006) Impairment of the spatial learning and memory induced by learned helplessness and chronic mild stress. Pharmacol Biochem Behav 83(2):186–193
Walesiuk A, Trofimiuk E, Braszko JJ (2005) Gingko biloba extract diminishes stress-induced memory deficits in rats. Pharmacol Rep 57(2):176–187
Watanabe Y, Gould E, Cameron HA, Daniels DC, McEwen BS (1992) Phenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus 2(4):431–436
Galea LAM, McEwen BS, Tanapat P, Deak T, Spencer RL, Dhabhar FS (1997) Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 81(3):689–697
McLaughlin KJ, Wilson JO, Harman J, Wright RL, Wieczorek L, Gomez J, Korol DL, Conrad CD (2009) Chronic 17β-estradiol or cholesterol prevents stress-induced hippocampal CA3 dendritic retraction in ovariectomized females: possible correspondence between CA1 spine properties and spatial acquisition. Hippocampus (in press)
McLaughlin KJ, Baran SE, Wright RL, Conrad CD (2005) Chronic stress enhances spatial memory in ovariectomized female rats despite CA3 dendritic retraction: possible involvement of CA1 neurons. Neuroscience 135(4):1045–1054
Bowman RE, Zrull MC, Luine VN (2001) Chronic restraint stress enhances radial arm maze performance in female rats. Brain Res 904:279–289
Kitraki E, Kremmyda O, Youlatos D, Alexis MN, Kittas C (2004) Gender-dependent alterations in corticosteroid receptor status and spatial performance following 21 days of restraint stress. Neuroscience 125:47–55
Kitraki E, Kremmyda O, Youlatos D, Alexis M, Kittas C (2004) Spatial performance and corticosteroid receptor status in the 21-day restraint stress paradigm. Ann N Y Acad Sci 1018:323–327
Conrad CD, Grote KA, Hobbs RJ, Ferayorni A (2003) Sex differences in spatial and non-spatial Y-maze performance after chronic stress. Neurobiol Learn Mem 79:32–40
Bowman RE, Ferguson D, Luine VN (2002) Effects of chronic restraint stress and estradiol on open field activity, spatial memory, and monoaminergic neurotransmitters in ovariectomized rats. Neuroscience 113:401–410
McEwen BS, Alves SE (1999) Estrogen actions in the central nervous system. Endocr Rev 20(3):279–307
Lee SJ, McEwen BS (2001) Neurotrophic and neuroprotective actions of estrogens and their therapeutic implications. Annu Rev Pharmacol Toxicol 41:569–591
Loy R, Gerlach JL, McEwen BS (1988) Autoradiographic localization of estradiol-binding neurons in the rat hippocampal formation and entorhinal cortex. Brain Res 467(2):245–251
Blurton-Jones M, Tuszynski MH (2002) Estrogen receptor-beta colocalizes extensively with parvalbumin-labeled inhibitory neurons in the cortex, amygdala, basal forebrain, and hippocampal formation of intact and ovariectomized adult rats. J Comp Neurol 452(3):276–287
Kretz O, Fester L, Wehrenberg U, Zhou L, Brauckmann S, Zhao S, Prange-Kiel J, Naumann T, Jarry H, Frotscher M, Rune GM (2004) Hippocampal synapses depend on hippocampal estrogen synthesis. J Neurosci 24(26):5913–5921
Cornil CA, Ball GF, Balthazart J (2006) Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from? Brain Res 1126(1):2–26
Conrad CD, Jackson JL, Wise L (2004) Chronic stress enhances ibotenic acid-induced damage selectively within the hippocampal CA3 region of male, but not female rats. Neuroscience 125(3):759–767
Takuma K, Matsuo A, Himeno Y, Hoshina Y, Ohno Y, Funatsu Y, Arai S, Kamei H, Mizoguchi H, Nagai T, Koike K, Inoue M, Yamada K (2007) 17β-Estradiol attenuates hippocampal neuronal loss and cognitive dysfunction induced by chronic restraint stress in ovariectomized rats. Neuroscience 146(1):60–68
Bowman RE, Beck KD, Luine VN (2003) Chronic stress effects on memory: sex differences in performance and monoaminergic activity. Horm Behav 43:48–59
Brun VH, Otnass MK, Molden S, Steffenach HA, Witter MP, Moser MB, Moser EI (2002) Place cells and place recognition maintained by direct entorhinal–hippocampal circuitry. Science 296(5576):2243–2246
Vago DR, Bevan A, Kesner RP (2007) The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval. Hippocampus 17(10):977–987
Brun VH, Leutgeb S, Wu HQ, Schwarcz R, Witter MP, Moser EI, Moser MB (2008) Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. Neuron 57(2):290–302
Kajiwara R, Wouterlood FG, Sah A, Boekel AJ, Baks-te Bulte LT, Witter MP (2008) Convergence of entorhinal and CA3 inputs onto pyramidal neurons and interneurons in hippocampal area CA1—an anatomical study in the rat. Hippocampus 18(3):266–280
Poirier GL, Amin E, Aggleton JP (2008) Qualitatively different hippocampal subfield engagement emerges with mastery of a spatial memory task by rats. J Neurosci 28:1034–1045
Vago DR, Kesner RP (2008) Disruption of the direct perforant path input to the CA1 subregion of the dorsal hippocampus interferes with spatial working memory and novelty detection. Behav Brain Res 189(2):273–283
Goodrich-Hunsaker NJ, Hunsaker MR, Kesner RP (2008) The interactions and dissociations of the dorsal hippocampus subregions: how the dentate gyrus, CA3, and CA1 process spatial information. Behav Neurosci 122(1):16–26
Hoang LT, Kesner RP (2008) Dorsal hippocampus, CA3, and CA1 lesions disrupt temporal sequence completion. Behav Neurosci 122(1):9–15
Hunsaker MR, Lee B, Kesner RP (2008) Evaluating the temporal context of episodic memory: the role of CA3 and CA1. Behav Brain Res 188(2):310–315
Okada K, Okaichi H (2009) Functional differentiation and cooperation among the hippocampal subregions in rats to effect spatial memory processes. Behav Brain Res 200(1):181–191
Nakazawa K, Sun LD, Quirk MC, Rondi-Reig L, Wilson MA, Tonegawa S (2003) Hippocampal CA3 NMDA receptors are crucial for memory acquisition of one-time experience. Neuron 38(2):305–315
Gold AE, Kesner RP (2005) The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat. Hippocampus 15(6):808–814
Lee I, Jerman TS, Kesner RP (2005) Disruption of delayed memory for a sequence of spatial locations following CA1- or CA3-lesions of the dorsal hippocampus. Neurobiol Learn Mem 84(2):138–147
Maclusky NJ, Hajszan T, Prange-Kiel J, Leranth C (2006) Androgen modulation of hippocampal synaptic plasticity. Neuroscience 138:957–965
Cunningham RL, Claiborne BJ, McGinnis MY (2007) Pubertal exposure to anabolic androgenic steroids increases spine densities on neurons in the limbic system of male rats. Neuroscience 150(3):609–615
Hajszan T, MacLusky NJ, Leranth C (2008) Role of androgens and the androgen receptor in remodeling of spine synapses in limbic brain areas. Horm Behav 53(5):638–646
Prange-Kiel J, Rune GM (2006) Direct and indirect effects of estrogen on the rat hippocampus. Neuroscience 138:765–772
Woolley CS (2007) Acute effects of estrogen on neuronal physiology. Annu Rev Pharmacol Toxicol 47:657–680
McLaughlin KJ, Bimonte-Nelson HA, Neisewander JL, Conrad CD (2008) Assessment of estradiol influence on spatial tasks and hippocampal CA1 spines: evidence that the duration of hormone deprivation after ovariectomy compromises 17β-estradiol effectiveness in altering CA1 spines. Horm Behav 54(3):386–395
Woolley CS, Gould E, Frankfurt M, McEwen BS (1990) Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10:4035–4039
Woolley CS, McEwen BS (1992) Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12(7):2549–2554
Woolley CS (1998) Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Horm Behav 34:140–148
Garza-Meilandt A, Cantu RE, Claiborne BJ (2006) Estradiol’s effects on learning and neuronal morphology vary with route of administration. Behav Neurosci 120(4):905–916
Wallace M, Luine V, Arellanos A, Frankfurt M (2006) Ovariectomized rats show decreased recognition memory and spine density in the hippocampus and prefrontal cortex. Brain Res 1126(1):176–182
Sandstrom NJ, Williams CL (2001) Memory retention is modulated by acute estradiol and progesterone replacement. Behav Neurosci 115:384–393
Sandstrom NJ, Williams CL (2004) Spatial memory retention is enhanced by acute and continuous estradiol replacement. Horm Behav 45(2):128–135
Donohue HS, Gabbott PLA, Davies HA, Rodriguez JJ, Cordero MI, Sandi C, Medvedev NI, Popov VI, Colyer FM, Peddie CJ, Stewart MG (2006) Chronic restraint stress induces changes in synapse morphology in stratum lacunosum-moleculare CA1 rat hippocampus: a stereological and three-dimensional ultrastructural study. Neuroscience 140(2):597–606
Shors TJ (2006) Significant life events and the shape of memories to come: a hypothesis. Neurobiol Learn Mem 85:103–115
Dalla C, Whetstone AS, Hodes GE, Shors TJ (2009) Stressful experience has opposite effects on dendritic spines in the hippocampus of cycling versus masculinized females. Neurosci Lett 449(1):52–56
Diamond DM, Campbell AM, Park CR, Woodson JC, Conrad CD, Bachstetter AD, Mervis R (2006) Influence of predator stress on the consolidation versus retrieval of long-term spatial memory and hippocampal spinogenesis. Hippocampus 16:571–576
Cerqueira JJ, Almeida OF, Sousa N (2008) The stressed prefrontal cortex. Left? Right!. Brain Behav Immun 22(5):630–638
Holmes A, Wellman CL (2009) Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neurosci Biobehav Rev 33(6):773–783
Singewald N (2007) Altered brain activity processing in high-anxiety rodents revealed by challenge paradigms and functional mapping. Neurosci Biobehav Rev 31(1):18–40
Del Arco A, Segovia G, Garrido P, de Blas M, Mora F (2007) Stress, prefrontal cortex and environmental enrichment: studies on dopamine and acetylcholine release and working memory performance in rats. Behav Brain Res 176(2):267–273
Mizoguchi K, Yuzurihara M, Ishige A, Sasaki H, Chui DH, Tabira T (2000) Chronic stress induces impairment of spatial working memory because of prefrontal dopaminergic dysfunction. J Neurosci 20(4):1568–1574
Moghaddam B (1993) Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J Neurochem 60:1650–1557
Miner LH, Jedema HP, Moore FW, Blakely RD, Grace AA, Sesack SR (2006) Chronic stress increases the plasmalemmal distribution of the norepinephrine transporter and the coexpression of tyrosine hydroxylase in norepinephrine axons in the prefrontal cortex. J Neurosci 26(5):1571–1578
Herman JP, Ostrander MM, Mueller NK, Figueiredo H (2005) Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29(8):1201–1213
Liston C, Miller MM, Goldwater DS, Radley JJ, Rocher AB, Hof PR, Morrison JH, McEwen BS (2006) Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 26(30):7870–7874
Garrett JE, Wellman CL (2009) Chronic stress effects on dendritic morphology in medial prefrontal cortex: sex differences and estrogen dependence. Neuroscience 162(1):195–207
Izquierdo A, Wellman CL, Holmes A (2006) Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice. J Neurosci 26(21):5733–5738
Seib LM, Wellman CL (2003) Daily injections alter spine density in rat medial prefrontal cortex. Neurosci Lett 337(1):29–32
Czéh B, Perez-Cruz C, Fuchs E, Flügge G (2008) Chronic stress-induced cellular changes in the medial prefrontal cortex and their potential clinical implications: does hemisphere location matter? Behav Brain Res 190(1):1–13
Cerqueira JJ, Pego JM, Taipa R, Bessa JM, Almeida OF, Sousa N (2005) Morphological correlates of corticosteroid-induced changes in prefrontal cortex-dependent behaviors. J Neurosci 25(34):7792–7800
Cerqueira JJ, Mailliet F, Almeida OF, Jay TM, Sousa N (2007) The prefrontal cortex as a key target of the maladaptive response to stress. J Neurosci 27(11):2781–2787
Grootendorst J, de Kloet ER, Vossen C, Dalm S, Oitzl MS (2001) Repeated exposure to rats has persistent genotype-dependent effects on learning and locomotor activity of apolipoprotein E knockout and C57Bl/6 mice. Behav Brain Res 125(1–2):249–259
Grootendorst J, de Kloet ER, Dalm S, Oitzl MS (2001) Reversal of cognitive deficit of apolipoprotein E knockout mice after repeated exposure to a common environmental experience. Neuroscience 108(2):237–247
Schwabe L, Dalm S, Schachinger H, Oitzl MS (2008) Chronic stress modulates the use of spatial and stimulus-response learning strategies in mice and man. Neurobiol Learn Mem 90(3):495–503
Wellman CL (2001) Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. Brain Res 828:127–134
Cerqueira JJ, Taipa R, Uylings HB, Almeida OF, Sousa N (2007) Specific configuration of dendritic degeneration in pyramidal neurons of the medial prefrontal cortex induced by differing corticosteroid regimens. Cereb Cortex 17(9):1998–2006
Wang VC, Sable HJ, Ju YH, Allred CD, Helferich WG, Korol DL, Schantz SL (2008) Effects of chronic estradiol treatment on delayed spatial alternation and differential reinforcement of low rates of responding. Behav Neurosci 122(4):794–804
Cahill L, Babinsky R, Markowitsch HJ, McGaugh JL (1995) The amygdala and emotional memory. Nature 377:295–296
Sarter M, Markowitsch HJ (1985) Involvement of the amygdala in learning and memory: a critical review, with emphasis on anatomical relations. Behav Neurosci 99(2):342–380
McGaugh JL, Roozendaal B (2002) Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12:205–210
Roozendaal B (2002) Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiol Learn Mem 78:578–595
Roozendaal B, Portillo-Marquez G, McGaugh JL (1996) Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning. Behav Neurosci 110(5):1074–1083
Roozendaal B, McGaugh JL (1997) Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. Eur J NeuroSci 9:76–83
Rodriguez Manzanares PA, Isoardi NA, Carrer HF, Molina VA (2005) Previous stress facilitates fear memory, attenuates GABAergic inhibition, and increases synaptic plasticity in the rat basolateral amygdala. J Neurosci 25(38):8725–8734
Roozendaal B, McReynolds JR, McGaugh JL (2004) The basolateral amygdala interacts with the medial prefrontal cortex in regulating glucocorticoid effects on working memory impairment. J Neurosci 24(6):1385–1392
Anglada-Figueroa D, Quirk GJ (2005) Lesions of the basal amygdala block expression of conditioned fear but not extinction. J Neurosci 25(42):9680–9685
Conrad CD, Mauldin-Jourdain ML, Hobbs RJ (2001) Metyrapone reveals that previous chronic stress differentially impairs hippocampal-dependent memory. Stress 4(4):305–318
Vyas A, Pillai AG, Chattarji S (2004) Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 128(4):667–673
Jackson ED, Payne JD, Nadel L, Jacobs WJ (2006) Stress differentially modulates fear conditioning in healthy men and women. Biol Psychiatry 59(6):516–522
Zorawski M, Blanding NQ, Kuhn CM, LaBar KS (2006) Effects of stress and sex on acquisition and consolidation of human fear conditioning. Learn Mem 13(4):441–450
Shors TJ, Weiss C, Thompson RF (1992) Stress-induced facilitation of classical conditioning. Science 257:537–539
Bangasser DA, Shors TJ (2004) Acute stress impairs trace eyeblink conditioning in females without altering the unconditional response. Neurobiol Learn Mem 82:57–60
Wood GE, Shors TJ (1998) Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones. Proc Natl Acad Sci U S A 95(7):4066–4071
Shors TJ (2001) Acute stress rapidly and persistently enhances memory formation in the male rat. Neurobiol Learn Mem 75:10–29
Waddell J, Bangasser DA, Shors TJ (2008) The basolateral nucleus of the amygdala is necessary to induce the opposing effects of stressful experience on learning in males and females. J Neurosci 28(20):5290–5294
Turner BB (1997) Influence of gonadal steroids on brain corticosteroid receptors: a minireview. Neurochem Res 22(11):1375–1385
Karandrea D, Kittas C, Kitraki E (2000) Contribution of sex and cellular context in the regulation of brain corticosteroid receptors following restraint stress. Neuroendocrinology 71:343–353
Alves SE, Hoskin E, Lee SJ, Brake WG, Ferguson D, Luine V, Allen PB, Greengard P, McEwen BS (2002) Serotonin mediates CA1 spine density but is not crucial for ovarian steroid regulation of synaptic plasticity in the adult rat dorsal hippocampus. Synapse 45(2):143–151
Beck KD, Luine VN (2002) Sex differences in behavioral and neurochemical profiles after chronic stress: role of housing conditions. Physiol Behav 75:661–673
Inoue T, Li XB, Abekawa T, Kitaichi Y, Izumi T, Nakagawa S, Koyama T (2004) Selective serotonin reuptake inhibitor reduces conditioned fear through its effect in the amygdala. Eur J Pharmacol 497(3):311–316
Mitsushima D, Yamada K, Takase K, Funabashi T, Kimura F (2006) Sex differences in the basolateral amygdala: the extracellular levels of serotonin and dopamine, and their responses to restraint stress in rats. Eur J NeuroSci 24(11):3245–3254
Conrad CD (2008) Chronic stress-induced hippocampal vulnerability: the glucocorticoid vulnerability hypothesis. Rev Neurosci 19(6):395–412
Conrad CD, Wright RL, McLaughlin KJ (2009) Stress and vulnerability to brain damage. In: Squire LR (ed) Encyclopedia of neuroscience. Academic, Oxford, pp 481–488
Foy MR, Baudry M, Briton RD, Thompson RF (2008) Estrogen and hippocampal plasticity in rodent models. J Alzheim Dis 15:589–603