Lactation-induced reduction in hippocampal neurogenesis is reversed by repeated stress exposure

Hippocampus

Volumn 24, Issue 6, 2014, Pages 673-683

  Hillerer, Katharina M ^a,b   Neumann, Inga D ^a   Couillard Despres, Sebastien ^b   Aigner, Ludwig ^b   Slattery, David A ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b PARACELSUS MEDICAL UNIVERSITY   (Austria)

Author keywords

Corticosterone; Differentiation; Hippocampal volume; Lactation; Neurons

Indexed keywords

CORTICOSTERONE; DOUBLECORTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; BRAIN SIZE; BRAIN WEIGHT; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DNA DENATURATION; FEMALE; HIPPOCAMPUS; HISTOPATHOLOGY; IMMOBILIZATION STRESS; LACTATION; NERVE CELL DIFFERENTIATION; NONHUMAN; NULLIPARA; PRIORITY JOURNAL; RAT; RIGHT HEMISPHERE; STRESS; ANIMAL; BLOOD; DENTATE GYRUS; EXERCISE; MENTAL STRESS; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; ORGAN SIZE; PARITY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; WISTAR RAT;

ANIMALS; ASTROCYTES; CELL COUNT; CELL PROLIFERATION; CELL SURVIVAL; CORTICOSTERONE; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; LACTATION; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; ORGAN SIZE; PARITY; RATS, WISTAR; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL;

EID: 84900541691     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22258     Document Type: Article

References (69)

1. Abrous DN, Koehl M, Le Moal M. 2005. Adult neurogenesis: From precursors to network and physiology. Physiol Rev 85:523-569.
2. Aimone JB, Deng W, Gage FH. 2010. Adult neurogenesis: Integrating theories and separating functions. Trends Cogn Sci 14:325-337.
3. Altemus M, Deuster PA, Galliven E, Carter CS, Gold PW. 1995. Suppression of hypothalmic-pituitary-adrenal axis responses to stress in lactating women. J Clin Endocrinol Metab 80:2954-2959.
4. Barha CK, Brummelte S, Lieblich SE, Galea LA. 2011. Chronic restraint stress in adolescence differentially influences hypothalamic-pituitary-adrenal axis function and adult hippocampal neurogenesis in male and female rats. Hippocampus 21:1216-1227.
5. Beck CT. 2006. Postpartum depression: It isn't just the blues. Am J Nurs 106:40-50; quiz 50-51.
6. Bridges RS. 2008. Neurobiology of the parental brain, Academic Press; Edition 1:1-550. ISBN:9780123742858.
7. Brunton PJ, Russell JA, Douglas AJ. 2008. Adaptive responses of the maternal hypothalamic-pituitary-adrenal axis during pregnancy and lactation. J Neuroendocrinol 20:764-776.
8. Cameron HA, Gould E. 1994. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61:203-209.
9. Cameron HA, Woolley CS, Gould E. 1993a. Adrenal steroid receptor immunoreactivity in cells born in the adult rat dentate gyrus. Brain Res 611:342-346.
10. Cameron HA, Woolley CS, McEwen BS, Gould E. 1993b. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56:337-344.
11. Carter CS, Altemus M, Chrousos GP. 2001. Neuroendocrine and emotional changes in the post-partum period. Prog Brain Res 133:241-249.
12. Czeh B, Welt T, Fischer AK, Erhardt A, Schmitt W, Muller MB, Toschi N, Fuchs E, Keck ME. 2002. Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: Effects on stress hormone levels and adult hippocampal neurogenesis. Biol Psychiatry 52:1057-1065.
13. Darnaudery M, Dutriez I, Viltart O, Morley-Fletcher S, Maccari S. 2004. Stress during gestation induces lasting effects on emotional reactivity of the dam rat. Behav Brain Res 153:211-216.
14. Darnaudery M, Perez-Martin M, Del Favero F, Gomez-Roldan C, Garcia-Segura LM, Maccari S. 2007. Early motherhood in rats is associated with a modification of hippocampal function. Psychoneuroendocrinology 32:803-812.
15. Falconer EM, Galea LA. 2003. Sex differences in cell proliferation, cell death and defensive behavior following acute predator odor stress in adult rats. Brain Res 975:22-36.
16. Fuchs E. 2007. Neurogenesis in the adult brain: Is there an association with mental disorders? Eur Arch Psychiatry Clin Neurosci 257:247-249.
17. Furuta M, Bridges RS. 2009. Effects of maternal behavior induction and pup exposure on neurogenesis in adult, virgin female rats. Brain Res Bull 80:408-413.
18. Galea LA, Ormerod BK, Sampath S, Kostaras X, Wilkie DM, Phelps MT. 2000. Spatial working memory and hippocampal size across pregnancy in rats. Horm Behav 37:86-95.
19. Galea LA, Uban KA, Epp JR, Brummelte S, Barha CK, Wilson WL, Lieblich SE, Pawluski JL. 2008. Endocrine regulation of cognition and neuroplasticity: Our pursuit to unveil the complex interaction between hormones, the brain, and behaviour. Can J Exp Psychol 62:247-260.
20. Gandelmann R, Zarrow MX, Denenberg VH, Myers M. 1971. Olfactory bulb removal eliminates behavior in the mouse. Science 171:210-211.
21. Geum D, Sun W, Paik SK, Lee CC, Kim K. 1997. Estrogen-induced cyclin D1 and D3 gene expressions during mouse uterine cell proliferation in vivo: Differential induction mechanism of cyclin D1 and D3. Mol Reprod Dev 46:450-458.
22. Gould E, Woolley CS, Cameron HA, Daniels DC, McEwen BS. 1991. Adrenal steroids regulate postnatal development of the rat dentate gyrus: II. Effects of glucocorticoids and mineralocorticoids on cell birth. J Comp Neurol 313:486-493.
23. Gould E, Cameron HA, Daniels DC, Woolley CS, McEwen BS. 1992. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 12:3642-3650.
24. Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E. 1997. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17:2492-2498.
25. Gould E, Tanapat P, McEwen BS, Flugge G, Fuchs E. 1998. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci U S A 95:3168-3171.
26. Hanson ND, Owens MJ, Nemeroff CB. 2011. Depression, antidepressants, and neurogenesis: A critical reappraisal. Neuropsychopharmacology 36:2589-2602.
27. Heine VM, Zareno J, Maslam S, Joels M, Lucassen PJ. 2005. Chronic stress in the adult dentate gyrus reduces cell proliferation near the vasculature and VEGF and Flk-1 protein expression. Eur J Neurosci 21:1304-1314.
28. Heinrichs M, Meinlschmidt G, Neumann I, Wagner S, Kirschbaum C, Ehlert U, Hellhammer DH. 2001. Effects of suckling on hypothalamic-pituitary-adrenal axis responses to psychosocial stress in postpartum lactating women. J Clin Endocrinol Metab 86:4798-4804.
29. Hillerer KM, Neumann ID, Slattery DA. 2012. From stress to postpartum mood and anxiety disorders: How chronic peripartum stress can impair maternal adaptations. Neuroendocrinology 95(1):22-38
30. Hillerer KM, Reber SO, Neumann ID, Slattery DA. 2011b. Exposure to chronic pregnancy stress reverses peripartum-associated adaptations: implications for postpartum anxiety and mood disorders. Endocrinology 152:3930-3940.
31. Hillerer KM, Neumann ID, Couillard-Despres S, Aigner L, Slattery DA. 2013. Sex-dependent regulation of hippocampal neurogenesis under basal and chronic stress conditions in rats. Hippocampus 23:476-487.
32. Hong J, Shah NN, Thomas TJ, Gallo MA, Yurkow EJ, Thomas T. 1998. Differential effects of estradiol and its analogs on cyclin D1 and CDK4 expression in estrogen receptor positive MCF-7 and estrogen receptor-transfected MCF-10AEwt5 cells. Oncol Rep 5:1025-1033.
33. Kandasamy M, Couillard-Despres S, Raber KA, Stephan M, Lehner B, Winner B, Kohl Z, Rivera FJ, Nguyen HP, Riess O, 2010. Stem cell quiescence in the hippocampal neurogenic niche is associated with elevated transforming growth factor-beta signaling in an animal model of Huntington disease. J Neuropathol Exp Neurol 69:717-728.
34. Kinsley CH, Trainer R, Stafisso-Sandoz G, Quadros P, Marcus LK, Hearon C, Meyer EA, Hester N, Morgan M, Kozub FJ, 2006. Motherhood and the hormones of pregnancy modify concentrations of hippocampal neuronal dendritic spines. Horm Behav 49:131-142.
35. Kuipers SD, Trentani A, Westenbroek C, Bramham CR, Korf J, Kema IP, Ter Horst GJ, Den Boer JA. 2006. Unique patterns of FOS, phospho-CREB and BrdU immunoreactivity in the female rat brain following chronic stress and citalopram treatment. Neuropharmacology 50:428-440.
36. Leuner B, Gould E. 2010. Dendritic growth in medial prefrontal cortex and cognitive flexibility are enhanced during the postpartum period. J Neurosci 30:13499-13503.
37. Leuner B, Shors TJ. 2006. Learning during motherhood: A resistance to stress. Horm Behav 50:38-51.
38. Leuner B, Mirescu C, Noiman L, Gould E. 2007. Maternal experience inhibits the production of immature neurons in the hippocampus during the postpartum period through elevations in adrenal steroids. Hippocampus 17:434-442.
39. Lledo PM, Alonso M, Grubb MS. 2006. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:179-193.
40. Lonstein JS. 2007. Regulation of anxiety during the postpartum period. Front Neuroendocrinol 28:115-141.
41. Lucassen PJ, Vollmann-Honsdorf GK, Gleisberg M, Czeh B, De Kloet ER, Fuchs E. 2001. Chronic psychosocial stress differentially affects apoptosis in hippocampal subregions and cortex of the adult tree shrew. Eur J Neurosci 14:161-166.
42. Luo C, Xu H, Li XM. 2005. Quetiapine reverses the suppression of hippocampal neurogenesis caused by repeated restraint stress. Brain Res 1063:32-39.
43. Maestripieri D, D'Amato FR. 1991. Anxiety and maternal aggression in house mice (Mus musculus): A look at interindividual variability. J Comp Psychol 105:295-301.
44. 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.
45. Meaney MJ, Viau V, Aitken DH, Bhatnagar S. 1989. Glucocoticoid receptors in brain and pituitary of the lactating dam. Physiol Behav 45:209-212.
46. Neumann ID. 2001. Alterations in behavioral and neuroendocrine stress coping strategies in pregnant, parturient and lactating rats. Prog Brain Res 133:143-152.
47. Neumann ID. 2003. Brain mechanisms underlying emotional alterations in the peripartum period in rats. Depress Anxiety 17:111-121.
48. Neumann ID, Johnstone HA, Hatzinger M, Liebsch G, Shipston M, Russell JA, Landgraf R, Douglas AJ. 1998. Attenuated neuroendocrine responses to emotional and physical stressors in pregnant rats involve adenohypophysial changes. J Physiol 508 (Pt 1):289-300.
49. Oatridge A, Holdcroft A, Saeed N, Hajnal JV, Puri BK, Fusi L, Bydder GM. 2002. Change in brain size during and after pregnancy: study in healthy women and women with preeclampsia. AJNR Am J Neuroradiol 23:19-26.
50. Pawluski JL, Galea LA. 2006. Hippocampal morphology is differentially affected by reproductive experience in the mother. J Neurobiol 66:71-81.
51. Pawluski JL, Galea LA. 2007. Reproductive experience alters hippocampal neurogenesis during the postpartum period in the dam. Neuroscience 149:53-67.
52. Pawluski JL, Charlier TD, Lieblich SE, Hammond GL, Galea LA. 2009. Reproductive experience alters corticosterone and CBG levelsin the rat dam. Physiol Behav 96:108-114.
53. Pawluski JL, van den Hove DL, Rayen I, Prickaerts J, Steinbusch HW. 2011. Stress and the pregnant female: Impact on hippocampal cell proliferation, but not affective-like behaviors. Horm Behav 59:572-580.
54. Pham K, Nacher J, Hof PR, McEwen BS. 2003. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 17:879-886.
55. Purcell RH, Sun B, Pass LL, Power ML, Moran TH, Tamashiro KL. 2011. Maternal stress and high-fat diet effect on maternal behavior, milk composition, and pup ingestive behavior. Physiol Behav 104:474-479.
56. Robertson E, Grace S, Wallington T, Stewart DE. 2004. Antenatal risk factors for postpartum depression: A synthesis of recent literature. Gen Hosp Psychiatry 26:289-295.
57. Rosenbrock H, Koros E, Bloching A, Podhorna J, Borsini F. 2005. Effect of chronic intermittent restraint stress on hippocampal expression of marker proteins for synaptic plasticity and progenitor cell proliferation in rats. Brain Res 1040:55-63.
58. Russell JA, Douglas AJ, Ingram CD. 2001. Brain preparations for maternity-Adaptive changes in behavioral and neuroendocrine systems during pregnancy and lactation. An overview. Prog Brain Res 133:1-38.
59. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, et al. 2003. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805-809.
60. Slattery DA, Neumann ID. 2008. No stress please! Mechanisms of stress hyporesponsiveness of the maternal brain. J Physiol 586:377-385.
61. Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA. 2011. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 476:458-461.
62. Stern JM, Goldman L, Levine S. 1973. Pituitary-adrenal responsiveness during lactation in rats. Neuroendocrinology 12:179-191.
63. Takahashi T, Nowakowski RS, Caviness VS Jr. 1992. BUdR as an S-phase marker for quantitative studies of cytokinetic behaviour in the murine cerebral ventricular zone. J Neurocytol 21:185-197.
64. Tanapat P, Hastings NB, Reeves AJ, Gould E. 1999. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrusof the adult female rat. J Neurosci 19: 5792-5801.
65. Tanapat P, Hastings NB, Rydel TA, Galea LA, Gould E. 2001. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J Comp Neurol 437:496-504.
66. Torner L, Karg S, Blume A, Kandasamy M, Kuhn HG, Winkler J, Aigner L, Neumann ID. 2009. Prolactin prevents chronic stress-induced decrease of adult hippocampal neurogenesis and promotes neuronal fate. J Neurosci 29:1826-1833.
67. Varodayan FP, Zhu XJ, Cui XN, Porter BE. 2009. Seizures increase cell proliferation in the dentate gyrus by shortening progenitor cell-cycle length. Epilepsia 50:2638-2647.
68. Walker CD, Trottier G, Rochford J, Lavallee D. 1995. Dissociation between behavioral and hormonal responses to the forced swim stress in lactating rats. J Neuroendocrinol 7:615-622.
69. Westenbroek C, Den Boer JA, Veenhuis M, Ter Horst GJ. 2004. Chronic stress and social housing differentially affect neurogenesis in male and female rats. Brain Res Bull 64:303-308.