Postpartum Corticosterone Administration Reduces Dendritic Complexity and Increases the Density of Mushroom Spines of Hippocampal CA3 Arbours in Dams

Journal of Neuroendocrinology

Volumn 25, Issue 2, 2013, Pages 119-130

  Workman, J L ^a   Brummelte, S ^a,c   Galea, L A M ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CORT; Dams; Depression; Forced swim test; Hippocampus; Housing; Maternal; Maternal behaviour; Postpartum depression; Stress

Indexed keywords

CORTICOSTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DENSITY; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; DRUG MEGADOSE; FEMALE; GOLGI COMPLEX; HIPPOCAMPAL CA3 REGION; IMMOBILIZATION; MALE; MARE; MATERNAL BEHAVIOR; MATERNAL CARE; NONHUMAN; PRIORITY JOURNAL; PUERPERAL DEPRESSION; PUERPERIUM; PYRAMIDAL NERVE CELL;

EID: 84873027564     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2012.02380.x     Document Type: Article

References (76)

1. Lovejoy MC, Graczyk PA, O'Hare E, Neuman G. Maternal depression and parenting behavior: a meta-analytic review. Clin Psychol Rev 2000; 20: 561-592.
2. Grace SL, Evindar A, Stewart DE. The effect of postpartum depression on child cognitive development and behavior: a review and critical analysis of the literature. Arch Womens Ment Health 2003; 6: 263-274.
3. Seyfried LS, Marcus SM. Postpartum mood disorders. Int Rev Psychiatry 2003; 15: 231-242.
4. Bloch M, Schmidt PJ, Danaceau M, Murphy J, Nieman L, Rubinow DR. Effects of gonadal steroids in women with a history of postpartum depression. Am J Psychiatry 2000; 157: 924-930.
5. Taylor A, Glover V, Marks M, Kammerer M. Diurnal pattern of cortisol output in postnatal depression. Psychoneuroendocrinology 2009; 34: 1184-1188.
6. Pittenger C, Duman RS. Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 2008; 33: 88-109.
7. Binder EB, Kunzel HE, Nickel T, Kern N, Pfennig A, Majer M, Uhr M, Ising M, Holsboer F. HPA-axis regulation at in-patient admission is associated with antidepressant therapy outcome in male but not in female depressed patients. Psychoneuroendocrinology 2009; 34: 99-109.
8. Jolley SN, Elmore S, Barnard KE, Carr DB. Dysregulation of the hypothalamic-pituitary-adrenal axis in postpartum depression. Biol Res Nurs 2007; 8: 210-222.
9. Ising M, Horstmann S, Kloiber S, Lucae S, Binder EB, Kern N, Kunzel HE, Pfennig A, Uhr M, Holsboer F. Combined dexamethasone/corticotropin releasing hormone test predicts treatment response in major depression - a potential biomarker? Biol Psychiatry 2007; 62: 47-54.
10. Schule C, Baghai TC, Eser D, Hafner S, Born C, Herrmann S, Rupprecht R. The combined dexamethasone/CRH Test (DEX/CRH test) and prediction of acute treatment response in major depression. PLoS ONE 2009; 4: e4324.
11. Parker KJ, Schatzberg AF, Lyons DM. Neuroendocrine aspects of hypercortisolism in major depression. Horm Behav 2003; 43: 60-66.
12. Antonijevic I. HPA axis and sleep: identifying subtypes of major depression. Stress 2008; 11: 15-27.
13. Bremmer MA, Deeg DJ, Beekman AT, Penninx BW, Lips P, Hoogendijk WJ. Major depression in late life is associated with both hypo- and hypercortisolemia. Biol Psychiatry 2007; 62: 479-486.
14. Magiakou MA, Mastorakos G, Rabin D, Dubbert B, Gold PW, Chrousos GP. Hypothalamic corticotropin-releasing hormone suppression during the postpartum period: implications for the increase in psychiatric manifestations at this time. J Clin Endocrinol Metab 1996; 81: 1912-1917.
15. Lightman SL, Windle RJ, Wood SA, Kershaw YM, Shanks N, Ingram CD. Peripartum plasticity within the hypothalamo-pituitary-adrenal axis. Prog Brain Res 2001; 133: 111-129.
16. Neumann ID. Brain mechanisms underlying emotional alterations in the peripartum period in rats. Depress Anxiety 2003; 17: 111-121.
17. Heinrichs M, Meinlschmidt G, Neumann I, Wagner S, Kirschbaum C, Ehlert U, Hellhammer DH. Effects of suckling on hypothalamic-pituitary-adrenal axis responses to psychosocial stress in postpartum lactating women. J Clin Endocrinol Metab 2001; 86: 4798-4804.
18. Field T. Breastfeeding and antidepressants. Infant Behav Dev 2008; 31: 481-487.
19. Watkins S, Meltzer-Brody S, Zolnoun D, Stuebe A. Early breastfeeding experiences and postpartum depression. Obstet Gynecol 2011; 118: 214-221.
20. Lommatzsch M, Hornych K, Zingler C, Schuff-Werner P, Hoppner J, Virchow JC. Maternal serum concentrations of BDNF and depression in the perinatal period. Psychoneuroendocrinology 2006; 31: 388-394.
21. Taylor A, Littlewood J, Adams D, Dore C, Glover V. Serum cortisol levels are related to moods of elation and dysphoria in new mothers. Psychiatry Res 1994; 54: 241-247.
22. Labad J, Vilella E, Reynolds RM, Sans T, Cavalle P, Valero J, Alonso P, Menchon JM, Labad A, Gutierrez-Zotes A. Increased morning adrenocorticotrophin hormone (ACTH) levels in women with postpartum thoughts of harming the infant. Psychoneuroendocrinology 2011; 36: 924-928.
23. Bloch M, Rubinow DR, Schmidt PJ, Lotsikas A, Chrousos GP, Cizza G. Cortisol response to ovine corticotropin-releasing hormone in a model of pregnancy and parturition in euthymic women with and without a history of postpartum depression. J Clin Endocrinol Metab 2005; 90: 695-699.
24. Brummelte S, Galea L. Chronic corticosterone during pregnancy and postpartum affects maternal care, cell proliferation and depressive-like behavior in the dam. Horm Behav 2010; 58: 769-779.
25. Brummelte S, Pawluski JL, Galea LA. High post-partum levels of corticosterone given to dams influence postnatal hippocampal cell proliferation and behavior of offspring: a model of post-partum stress and possible depression. Horm Behav 2006; 50: 370-382.
26. Bowman RE, Beck KD, Luine VN. Chronic stress effects on memory: sex differences in performance and monoaminergic activity. Horm Behav 2003; 43: 48-59.
27. Galea LA, McEwen BS, Tanapat P, Deak T, Spencer RL, Dhabhar FS. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 1997; 81: 689-697.
28. Pawluski JL, Galea LA. Hippocampal morphology is differentially affected by reproductive experience in the mother. J Neurobiol 2006; 66: 71-81.
29. Cryan JF, Valentino RJ, Lucki I. Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci Biobehav Rev 2005; 29: 547-569.
30. Sheline YI, Wang PW, Gado MH, Csernansky JG, Vannier MW. Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci USA 1996; 93: 3908-3913.
31. Sheline YI, Sanghavi M, Mintun MA, Gado MH. Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J Neurosci 1999; 19: 5034-5043.
32. McKinnon MC, Yucel K, Nazarov A, MacQueen GM. A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder. J Psychiatry Neurosci 2009; 34: 41-54.
33. Starkman MN, Gebarski SS, Berent S, Schteingart DE. Hippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing's syndrome. Biol Psychiatry 1992; 32: 756-765.
34. Starkman MN, Giordani B, Gebarski SS, Berent S, Schork MA, Schteingart DE. Decrease in cortisol reverses human hippocampal atrophy following treatment of Cushing's disease. Biol Psychiatry 1999; 46: 1595-1602.
35. Magarinos AM, Li CJ, Gal Toth J, Bath KG, Jing D, Lee FS, McEwen BS. Effect of brain-derived neurotrophic factor haploinsufficiency on stress-induced remodeling of hippocampal neurons. Hippocampus 2011; 21: 253-264.
36. Sunanda, Rao MS, Raju TR. Effect of chronic restraint stress on dendritic spines and excrescences of hippocampal CA3 pyramidal neurons - a quantitative study. Brain Res 1995; 694: 312-317.
37. Shors TJ, Chua C, Falduto J. Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J Neurosci 2001; 21: 6292-6297.
38. Brummelte S, Galea L. Chronic high corticosterone reduces neurogenesis in the dentate gyrus of adult male and female rats. Neuroscience 2010; 168: 680-690.
39. Craft RM, Kostick ML, Rogers JA, White CL, Tsutsui KT. Forced swim test behavior in postpartum rats. Pharmacol Biochem Behav 2010; 96: 402-412.
40. Fischer D, Patchev VK, Hellbach S, Hassan AH, Almeida OF. Lactation as a model for naturally reversible hypercorticalism plasticity in the mechanisms governing hypothalamo-pituitary- adrenocortical activity in rats. J Clin Invest 1995; 96: 1208-1215.
41. Landeros RV, Morisseau C, Yoo HJ, Fu SH, Hammock BD, Trainor BC. Corncob bedding alters the effects of estrogens on aggressive behavior and reduces estrogen receptor-alpha expression in the brain. Endocrinology 2012; 153: 949-953.
42. Laroche J, Gasbarro L, Herman JP, Blaustein JD. Enduring influences of peripubertal/adolescent stressors on behavioral response to estradiol and progesterone in adult female mice. Endocrinology 2009; 150: 3717-3725.
43. van Praag H, Kempermann G, Gage FH. Neural consequences of environmental enrichment. Nat Rev Neurosci 2000; 1: 191-198.
44. Johnson SA, Fournier NM, Kalynchuk LE. Effect of different doses of corticosterone on depression-like behavior and HPA axis responses to a novel stressor. Behav Brain Res 2006; 168: 280-288.
45. Kalynchuk LE, Gregus A, Boudreau D, Perrot-Sinal TS. Corticosterone increases depression-like behavior, with some effects on predator odor-induced defensive behavior, in male and female rats. Behav Neurosci 2004; 118: 1365-1377.
46. Wong EY, Herbert J. Raised circulating corticosterone inhibits neuronal differentiation of progenitor cells in the adult hippocampus. Neuroscience 2006; 137: 83-92.
47. Yeh KY. Corticosterone concentrations in the serum and milk of lactating rats: parallel changes after induced stress. Endocrinology 1984; 115: 1364-1370.
48. Porsolt RD, Le Pichon M, Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977; 266: 730-732.
49. Porsolt RD, Anton G, Blavet N, Jalfre M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 1978; 47: 379-391.
50. Galea LA, Wide JK, Barr AM. Estradiol alleviates depressive-like symptoms in a novel animal model of post-partum depression. Behav Brain Res 2001; 122: 1-9.
51. Dalla C, Antoniou K, Papadopoulou-Daifoti Z, Balthazart J, Bakker J. Male aromatase-knockout mice exhibit normal levels of activity, anxiety and 'depressive-like' symptomatology. Behav Brain Res 2005; 163: 186-193.
52. Hinojosa FR, Spricigo L Jr, Izidio GS, Bruske GR, Lopes DM, Ramos A. Evaluation of two genetic animal models in behavioral tests of anxiety and depression. Behav Brain Res 2006; 168: 127-136.
53. Smith JW, Seckl JR, Evans AT, Costall B, Smythe JW. Gestational stress induces post-partum depression-like behaviour and alters maternal care in rats. Psychoneuroendocrinology 2004; 29: 227-244.
54. Pollak DD, Rey CE, Monje FJ. Rodent models in depression research: classical strategies and new directions. Ann Med 2010; 42: 252-264.
55. Wilson RC, Vacek T, Lanier DL, Dewsbury DA. Open-field behavior in muroid rodents. Behav Biol 1976; 17: 495-506.
56. Crusio WE. Genetic dissection of mouse exploratory behaviour. Behav Brain Res 2001; 125: 127-132.
57. Son J, Song S, Lee S, Chang S, Kim M. Morphological change tracking of dendritic spines based on structural features. J Microsc 2011; 241: 261-272.
58. Magarinos AM, McEwen BS. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 1995; 69: 89-98.
59. Watanabe Y, Gould E, McEwen BS. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 1992; 588: 341-345.
60. Torner L, Karg S, Blume A, Kandasamy M, Kuhn HG, Winkler J, Aigner L, Neumann ID. Prolactin prevents chronic stress-induced decrease of adult hippocampal neurogenesis and promotes neuronal fate. J Neurosci 2009; 29: 1826-1833.
61. Leuner B, Caponiti JM, Gould E. Oxytocin stimulates adult neurogenesis even under conditions of stress and elevated glucocorticoids. Hippocampus 2011; 22: 861-868.
62. Bourne J, Harris KM. Do thin spines learn to be mushroom spines that remember? Curr Opin Neurobiol 2007; 17: 381-386.
63. Moghaddam B, Bolinao ML, Stein-Behrens B, Sapolsky R. Glucocorticoids mediate the stress-induced extracellular accumulation of glutamate. Brain Res 1994; 655: 251-254.
64. Yuste R, Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 2001; 24: 1071-1089.
65. Woolley CS. Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Horm Behav 1998; 34: 140-148.
66. Sparling JE, Mahoney M, Baker S, Bielajew C. The effects of gestational and postpartum environmental enrichment on the mother rat: a preliminary investigation. Behav Brain Res 2010; 208: 213-223.
67. Handa RJ, Burgess LH, Kerr JE, O'Keefe JA. Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm Behav 1994; 28: 464-476.
68. Goel N, Bale TL. Sex differences in the serotonergic influence on the hypothalamic-pituitary-adrenal stress axis. Endocrinology 2010; 151: 1784-1794.
69. Leuner B, Mirescu C, Noiman L, Gould E. Maternal experience inhibits the production of immature neurons in the hippocampus during the postpartum period through elevations in adrenal steroids. Hippocampus 2007; 17: 434-442.
70. Rees SL, Panesar S, Steiner M, Fleming AS. The effects of adrenalectomy and corticosterone replacement on maternal behavior in the postpartum rat. Horm Behav 2004; 46: 411-419.
71. Kimble DP, Rogers L, Hendrickson CW. Hippocampal lesions disrupt maternal, not sexual, behavior in the albino rat. J Comp Physiol Psychol 1967; 63: 401-407.
72. Brummelte S, Lieblich SE, Galea LA. Gestational and postpartum corticosterone exposure to the dam affects behavioral and endocrine outcome of the offspring in a sexually-dimorphic manner. Neuropharmacology 2012; 62: 406-418.
73. Baez M, Volosin M. Corticosterone influences forced swim-induced immobility. Pharmacol Biochem Behav 1994; 49: 729-736.
74. Korte SM, De Kloet ER, Buwalda B, Bouman SD, Bohus B. Antisense to the glucocorticoid receptor in hippocampal dentate gyrus reduces immobility in forced swim test. Eur J Pharmacol 1996; 301: 19-25.
75. Kokras N, Dalla C, Sideris AC, Dendi A, Mikail HG, Antoniou K, Papadopoulou-Daifoti Z. Behavioral sexual dimorphism in models of anxiety and depression due to changes in HPA axis activity. Neuropharmacology 2012; 62: 436-445.
76. Brummelte S, Galea LA. Depression during pregnancy and postpartum: contribution of stress and ovarian hormones. Prog Neuropsychopharmacol Biol Psychiatry 2010; 34: 766-776.