Chronic stress and neural function: Accounting for sex and age

Journal of Neuroendocrinology

Volumn 19, Issue 10, 2007, Pages 743-751

  Luine, V N ^a   Beck, K D ^b,c   Bowman, R E ^d   Frankfurt, M ^e   Maclusky, N J ^f  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^d SACRED HEART UNIVERSITY   (United States)

^e CITY UNIVERSITY OF NEW YORK MEDICAL SCHOOL   (United States)

^f UNIVERSITY OF GUELPH   (Canada)

Author keywords

Anxiety; Memory; Oestradiol; Sex differences; Stress

Indexed keywords

CORTICOSTEROID; CORTICOSTERONE; ESTRADIOL; ESTROGEN; GLUCOCORTICOID RECEPTOR;

ADAPTIVE BEHAVIOR; AGING; ANXIETY; CHRONIC STRESS; COGNITIVE DEFECT; CORTICOSTEROID BLOOD LEVEL; CORTICOSTERONE RELEASE; DOWN REGULATION; ESTROGEN BLOOD LEVEL; FRONTAL CORTEX; HIPPOCAMPUS; HORMONE SENSITIVITY; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MENTAL FUNCTION; NONHUMAN; PRIORITY JOURNAL; RECALL; REVIEW; SEX DIFFERENCE; SPATIAL MEMORY; TASK PERFORMANCE; TRANQUILIZING ACTIVITY; VISUAL MEMORY;

ADAPTATION, PHYSIOLOGICAL; AGE FACTORS; AGING; ANIMALS; CENTRAL NERVOUS SYSTEM; CHRONIC DISEASE; FEMALE; GONADAL STEROID HORMONES; HUMANS; MALE; NEURONS; SEX FACTORS; STRESS; STRESS, PSYCHOLOGICAL;

EID: 34548550475     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2007.01594.x     Document Type: Review

References (50)

1. Selye H. The Stress of Life. New York, NY: McGraw-Hill, 1976.
2. Wellman L. Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J Neurobiol 2001; 49: 245-253.
3. Radley JJ, Sisti HM, Hao J, Rocher AB, McCall T, Hof PR, McEwen BS, Morrison JH. Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 2004; 125: 1-6.
4. Radley JJ, Rjocher AB, Miller M, Janssen WG, Listen C, Hof PR, McEwen BS, Morrison JH. Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cereb Cortex 2006; 16: 313-320.
5. Watanabe Y, Gould E, McEwen BS. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 1992; 588: 341-345.
6. Magarinos AM, Verdugo JM, McEwen BS. Chronic stress alters synaptic terminal structure in hippocampus. Proc Natl Acad Sci USA 1997; 94: 14002-14008.
7. McLaughlin KF, Baran SE, Wright RL, Conrad CD. Chronic stress enhances spatial memory in ovariectomized female rats despite CA3 dendritic retraction. Possible involvement of CA1 neurons. Neuroscience 2005; 135: 1045-1054.
8. Donohue HS, Gabbott PL, Davies HA, Rodriques JJ, Cordero MI, Sandi C, Medvedev NI, Popov VI, Colyer FM, Peddie CJ, Stewart MG. Chronic restraint stress induces changes in synapse morphology in stratum lacuosum-moleculare CA1 rat hippocampus: A stereological and three-dimensional ultrastructural study. Neuroscience 2006; 140: 597-606.
9. Luine V, Spencer RL, McEwen BS. Effects of chronic corticosterone ingestion on spatial memory performance and hippocampal serotonergic function. Brain Res 1993; 616: 65-70.
10. Beck KD, Luine VN. Food deprivation modulates chronic stress effects on object recognition in male rats: Role of monoamines and amino acids. Brain Res 1999; 830: 56-71.
11. Beck KD, Luine VN. Sex differences in behavioral and neurochemical profiles after chronic stress: Role of housing conditions. Physiol Behav 2002; 75: 661-673.
12. Luine VN. Sex differences in chronic stress effects on memory in rats. Stress 2002; 5: 205-216.
13. Sunanda RBS, Raju TR. Restraint stress-induced alterations in the levels of biogenic amines, amino acids, and AchE activity in the hippocampus. Neurochem Res 2000; 25: 1547-1552.
14. Torres IL, Gamaro GD, Vasconcellos AP, Silveira R, Dalmaz C. Effects of chronic restraint stress on feeding behavior and on monoamine levels in different brain structures in rats. Neurochem Res 2002; 27: 519-525.
15. Ren-Patterson RF, Cochran LW, Holmes A, Lesch KP, Lu B, Murphy DL. Gender-dependent modulation of brain monoamines and anxiety-like behaviors in mice with genetic serotonin transporter and BDNF deficiencies. Cell Mol Neurobiol 2006; 26: 755-780.
16. Kitraki E, Kremmyda O, Youlatos D, Alexis MN, Kittas C. Gender-dependent alterations in corticosteroid receptor status and spatial performance following 21 days of restraint stress. Neuroscience 2004; 125: 47-55.
17. Luine V, Villegas M, Martinez C, McEwen BS. Repeated stress causes reversible impairments of spatial memory performance. Brain Res 1994; 639: 167-170.
18. Conrad CD, Galea LA, Kuroda Y, McEwen BS. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav Neurosci 1996; 110: 1321-1334.
19. Luine V, Martinez C, Villegas M, Magarinos AM, McEwen BS. Restraint stress reversibly enhances spatial memory performance. Physiol Behav 1996; 59: 27-32.
20. Bowman RE, Micik R, Luine VN. Sex-dependent effects of short-term restraint stress on anxiety and cognitive functioning are task specific. Soc Neurosci Abstract 2006; 5: 778. 1.
21. Bowman RE, Beck KD, Luine VN. Chronic stress effects on memory. Sex differences in performance and monoamines. Horm Behav 2003; 43: 48-59.
22. Bowman RE. Stress-induced changes in spatial memory are sexually differentiated and vary across the lifespan. J Neuroendocrinol 2005; 17: 526-535.
23. Bowman RE, Zrull MC, Luine VN. Chronic restraint stress enhances radial arm maze performance in female rats. Brain Res 2001; 904: 279-289.
24. Bowman RE, Ferguson D, Luine VN. Effects of chronic restraint stress and estradiol on open field activity, spatial memory, and monoaminergic neurotransmitters in ovariectomized rats. Neuroscience 2002; 113: 401-410.
25. Conrad CD, Grote KD, Hobbs RJ, Ferayorni A. Sex differences in spatial and non-spatial Y-maze performance after chronic stress. Neurobiol Learn Mem 2003; 79: 32-40.
26. Galea LA, McEwen BS, Tanapat P, Deak T, Spencer RL, Dhabha FS. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 1997; 81: 689-697.
27. Bowman R, MacLusky NJ, Sarmiento Y, Frankfurt M, Gordon M, Luine VN. Sexually dimorphic effects of prenatal stress on cognition, hormonal responses and central neurotransmitters. Endocrinology 2004; 145: 3778-3787.
28. Bisagno V, Grillo CA, Piroli GG, Giraldo P, McEwen BS, Luine VN. Chronic stress alters amphetamine effects on behavior and synaptophysin levels in female rats. Pharmac Biochem Behav 2004; 78: 541-550.
29. Diamond DM, Campbell AM, Park CR, Woodson JC, Conrad CD, Bachsteter AD, Mervis RF. Influence of predator stress on the consolidation versus retrieval of long-term spatial memory and hippocampal spinogenesis. Hippocampus 2006; 16: 571-576.
30. Mitra R, Vyas A, Chatterjee G, Chattarji S. Chronic-stress induced modulation of different states of anxiety-like behavior in female rats. Neurosci Lett 2005; 383: 278-283.
31. Gotz AA, Stefanski V. Psychosocial maternal stress during pregnancy affects serum corticosterone, blood immune parameters and anxiety behaviour in adult male rat offspring. Physiol Behav 2007; 90: 108-115.
32. Figueiredo HF, Dolgas CM, Herman JP. Stress activation of cortex and hippocampus is modulated by sex and stage of estrus. Endocrinology 2002; 143: 2534-2540.
33. Bowman R, Maclusky NJ, Zrull MJ, Diaz SE, Luine VN. Aged rats: Sex differences and responses to chronic stress. Brain Res 2006; 1126: 156-166.
34. Di Nicola AF, Saravia FE, Beauquis J, Pietranera L, Ferrini MG. Estrogens and neuroendocrine hypothalamic-pituitary-adrenal axis function. Front Horm Res 2006; 35: 157-168.
35. Viau V, Meany MJ. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 1991; 129: 2503-2511.
36. McEwen BS. The neurobiology of stress: From serendipity to clinical relevance. Brain Res 2000; 886: 172-189.
37. Ward IL, Ward OB. Sexual behavior differentiation: Effects of prenatal manipulations in rats. In: Adler N, Pfaff D, Goy RW, eds. Handbook of Behavioral Neurobiology. New York, NY: Plenum, 1985: 301-309.
38. Garcia-Segura LM, Azcortia I, DonCarlos LC. Neuroprotection by estrogen. Prog Neurobiol 2001; 63: 29-60.
39. Conrad CD, Jackson JL, Wieczorek L, Baran SE, Harman JS, Wright RL, Korol DL. Actue stress impairs spatial memory in male but not female rats: Influence of estrous cycle. Pharmacol Biochem Behav 2004; 78: 569-579.
40. Walf AA, Frye CA. Antianxiety and antidepressive behavior produced by physiological estradiol regimen may be modulated by hypothalamic-pituitary-adrenal axis activity. Neuropsychopharmacology 2005; 30: 1288-1201.
41. Torras-Garcia M, Costa-Miserachs D, Coli-Andreu M, Portell-Cortes I. Decreased anxiety levels related to aging. Exp Brain Res 2005; 164: 177-184.
42. Scharfman HE, Maclusky NJ. Similarities between actions of estrogen and BDNF in the hippocampus: Coincidence or clue? Trends Neurosci 2005; 28: 79-85.
43. Luo C, Xu H, Li XM. Post-stress changes in BDNF and Bcl-2 immunoreactivities in hippocampal neurons: Effect of chronic administration of olanzapine. Brain Res 2004; 1025: 194-202.
44. Radecki DT, Brown LM, Martinez J, Teyler TJ. BDNF protects against stress-induced impairments in spatial learning and memory and LTP. Hippocampus 2005; 15: 246-253.
45. Kuroda Y, McEwen BS. Effect of chronic restraint stress and tianeptine on growth factors, growth-associated protein-43 and microtubule-associated protein 2 mRNA expression in the rat hippocampus. Brain Res Mol Brain Res 1998; 59: 35-39.
46. Blurton-Jones M, Kuan PN, Tuszynski MH. Anatomical evidence for transsynaptic influences of estrogen on brain-derived neurotrophic factor expression. J Comp Neurol 2004; 468: 347-360.
47. Zhou J, Zhang H, Cohen RS, Pandey SC. Effects of estrogen treatment on expression of brain-derived neurotrophic factor and cAMP response element-binding protein expression and phosphorylation in rat amygdaloid and hippocampal structures. Neuroendocrinology 2005; 81: 294-310.
48. Kuipers SD, Trentani A, Den Boer JA, Ter Horst GJ. Molecular correlates of impaired prefrontal plasticity in response to chronic stress. J Neurochem 2003; 85: 1312-1323.
49. Belsky IF, Young LJ. Oxytocin, vasopressin and social recognition in mammals. Peptides 2004; 25: 1565-1574.
50. Tomizawa K, Iga N, Lu YG, Moriwaki A, Matsushita M, Li ST, Miyamoto O, Itano T, Matsui H. Oxytocin improves long-lasting spatial memory during motherhood through MAP kinase cascade. Nat Neurosci 2003; 6: 384-390.