Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat

Journal of Neuroscience

Volumn 19, Issue 14, 1999, Pages 5792-5801

  Tanapat, Patima ^a   Hastings, Nicholas B ^a   Reeves, Alison J ^a   Gould, Elizabeth ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

Dentate gyrus; Estrogen; Estrous cycle; Granule neuron; Neurogenesis; Sex differences

Indexed keywords

ESTROGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; DIESTRUS; ESTROGEN ACTIVITY; ESTRUS; ESTRUS CYCLE; FEMALE; HIPPOCAMPUS; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROESTRUS; RAT; SEX DIFFERENCE;

ANIMALS; BROMODEOXYURIDINE; CELL DIVISION; DENTATE GYRUS; ESTRADIOL; ESTRUS; FEMALE; HIPPOCAMPUS; MALE; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS;

EID: 0033565292     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335.
2. Arnold AP, Breedlove SM (1985) Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm Behav 19:469-498.
3. Barnea A, Nottebohm F (1994) Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci USA 91:11217-11221.
4. Bayer SA (1982) Changes in the total number of dentate granule cells in juvenile and adult rats: a correlated volumetric and 3H-thymidine autoradiographic study. Exp Brain Res 46:315-323.
5. Bucci DJ, Chiba AA, Gallagher M (1995) Spatial learning in male and female Long-Evans rats. Behav Neurosci 109:180-183.
6. Burek MJ, Nordeen KW, Nordeen EJ (1995) Estrogen promotes neuron addition to an avian song-control nucleus by regulating post-mitotic events. Brain Res Dev Brain Res 85:220-224.
7. Cameron HA, Gould E (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61:203-209.
8. Cameron HA, Woolley CS, McEwen BS, Gould E (1993) Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56:337-344.
9. Chisari A, Carino M, Perone M, Gaillard RC, Spinedi E (1995) Sex and strain variability in the rat hypothalamo-pituitary-adrenal (HPA) axis function. J Endocrinol Invest 18:25-33.
10. Cordoba Montoya DA, Carrer HF (1997) Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats. Brain Res 778:430-438.
11. Daniel JM, Fader AJ, Spencer AL, Dohanich GP (1997) Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm Behav 32:217-225.
12. Desmond NL, Levy WB (1997) Ovarian steroidal control of connectivity in the female hippocampus: an overview of recent experimental findings and speculations on its functional consequences. Hippocampus 7:239-245.
13. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
14. Gaarskjaer FB (1985) The development of the dentate area and the hippocampal mossy fiber projection of the rat. J Comp Neurol 241:154-170.
15. Galea LA, Kavaliers M, Ossenkopp KP (1996) Sexually dimorphic spatial learning in meadow voles Microtus pennsylvanicus and deer mice Peromyscus maniculatus. J Exp Biol 199:195-200.
16. 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.
17. Gould E, Woolley CS, McEwen BS (1991) Naturally occurring cell death in the developing dentate gyrus of the rat. J Comp Neurol 304:408-418.
18. 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.
19. Gould E, McEwen BS, Tanapat P, Galea LAM, 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.
20. 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 USA 95:3168-3171.
21. Gould E, Beylin A, Tanapat P, Reeves AJ, Shors TJ (1999a) Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265.
22. Gould E, Reeves AJ, Fallah M, Tanapat P, Gross CG, Fuchs E (1999b) Hippocampal neurogenesis in adult old world primates. Proc Natl Acad Sci USA 96:5263-5267.
23. Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B (1988) The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96:857-881.
24. Handa RJ, Burgess LH, Kerr JE, O'Keefe JA (1994) Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitaryadrenal axis. Horm Behav 28:464-476.
25. Hastings NB, Gould E (1999) Adult-generated granule cells rapidly extend axons into the CA3 region: a combined BrdU-labeling and retrograde tracer study. J Comp Neurol, in press.
26. Hidalgo A, Barami K, Iversen K, Goldman SA (1995) Estrogens and non-estrogenic ovarian influences combine to promote the recruitment and decrease the turnover of new neurons in the adult female canary brain. J Neurobiol 27:470-487.
27. 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.
28. Isgor C, Sengelaub DR (1998) Prenatal gonadal steroids affect adult spatial behavior, CA1 and CA3 pyramidal cell morphology in rats. Horm Behav 34:183-198.
29. Kamel F, Kubajak CL (1987) Modulation of gonadotropin secretion by corticosterone: interaction with gonadal steroids and mechanism of action. Endocrinology 121:561-568.
30. Kavaliers M, Galea LA (1995) Sex differences in the expression and antagonism of swim stress-induced analgesia in deer mice vary with the breeding season. Pain 63:327-334.
31. Kavaliers M, Ossenkopp KP, Prato FS, Innes DG, Galea LA, Kinsella DM, Perrot-Sinal TS (1996) Spatial learning in deer mice: sex differences and the effects of endogenous opioids and 60 Hz magnetic fields. J Comp Physiol 179:715-724.
32. Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495.
33. Laatikainen TJ (1991) Corticotropin-releasing hormone and opioid peptides in reproduction and stress. Ann Med 23:489-496.
34. Lee HW, Eghbali-Webb M (1998) Estrogen enhances proliferative capacity of cardiac flbroblasts by estrogen receptor- and mitogen-activated protein kinase-dependent pathways. J Mol Cell Cardiol 30:1359-1368.
35. Long JA, Evans HM (1922) The oestrus cycle in the rat and its associated phenomena. Mem Univ California 6:1.
36. Lopez F, Belloc F, Lacombe F, Dumain P, Reiffers J, Bernard P, Boisseau MR (1991) Modalities of synthesis of Ki67 antigen during the stimulation of lymphocytes. Cytometry 12:42-49.
37. 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 34:149-162.
38. Madeira MD, Paula-Barbosa MM (1993) Reorganization of mossy fiber synapses in male and female hypothyroid rats: a stereological study. J Comp Neurol 337:334-352.
39. Madeira MD, Sousa N, Paula-Barbosa MM (1991) Sexual dimorphism in the mossy fiber synapses of the rat hippocampus. Exp Brain Res 87:537-545.
40. Maren S, De Oca B, Fanselow MS (1994) Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: positive correlation between LTP and contextual learning. Brain Res 661:25-34.
41. McEwen BS, Gould E, Orchinik M, Weiland NG, Woolley CS (1995) Oestrogens and the structural and functional plasticity of neurons: implications for memory, ageing and neurodegenerative processes. Ciba Found Symp 191:52-66.
42. Minturn JE, Geschwind DH, Fryer HJ, Hockfield S (1995) Early post-mitotic neurons transiently express TOAD-64, a neural specific protein. J Comp Neurol 355:369-379.
43. Nottebohm F (1989) Hormonal regulation of synapses and cell number in the adult canary brain and its relevance to theories of long-term memory storage. In: Neural control of reproductive function (Lakoski J, Perez-Polo JR, Rossin D, eds), pp 583-601. Alan R. Liss.
44. Nowakowski RS, Lewin SB, Miller MW (1989) Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 18:311-318.
45. Packard MG (1998) Posttraining estrogen and memory modulation. Horm Behav 34:126-139.
46. Packard MG, Teather LA (1997a) Posttraining estradiol injections enhance memory in ovariectomized rats: cholinergic blockade and synergism. Neurobiol Learn Mem 68:172-188.
47. Packard MG, Teather LA (1997b) Intra-hippocampal estradiol infusion enhances memory in ovariectomized rats. NeuroReport 8:3009-3013.
48. Parducz A, Garcia-Segura LM (1993) Sexual differences in the synaptic connectivity in the rat dentate gyrus. Neurosci Lett 161:53-56.
49. Perrot-Sinal TS, Kostenuik MA, Ossenkopp KP, Kavaliers M (1996) Sex differences in performance in the Morris water maze and the effects of initial nonstationary hidden platform training. Behav Neurosci 110:1309-1320.
50. Rabin D, Gold PW, Margioris AN, Chrousos GP (1988) Stress and reproduction: physiologic and pathophysiologic interactions between the stress and reproductive axes. Adv Exp Med Biol 245:377-387.
51. Roof RL, Havens MD (1992) Testosterone improves maze performance and induces development of a male hippocampus in females. Brain Res 572:310-313.
52. Roof RL, Zhang Q, Glasier MM, Stein DG (1993) Gender-specific impairment on Morris water maze task after entorhinal cortex lesion. Behav Brain Res 57:47-51.
53. Shors TJ, Lewczyk C, Pacynski M, Mathew PR, Pickett J (1998) Stages of estrous mediate the stress-induced impairment of associative learning in the female rat. NeuroReport 9:419-423.
54. Sohrabji F, Miranda RC, Toran-Allerand CD (1994) Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J Neurosci 14:459-471.
55. Squire LR, Zola SM (1998) Episodic memory, semantic memory, and amnesia. Hippocampus 8:205-211.
56. Stackman RW, Blasberg ME, Langan CJ, Clark AS (1997) Stability of spatial working memory across the estrous cycle of Long-Evans rats. Neurobiol Learn Mem 67:167-171.
57. Stockard CR, Papanicolaou GN (1917) The existence of a typical oestrous cycle in the guinea-pig with a study of its histological and physiological changes. Am J Anat 22:225.
58. Viau V, Meaney MJ (1991) Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 129:2503-2511.
59. Warren SG, Juraska JM (1997) Spatial and nonspatial learning across the rat estrous cycle. Behav Neurosci 111:259-266.
60. Warren SG, Humphreys AG, Juraska JM, Greenough WT (1995) LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats. Brain Res 703:26-30.
61. Watters JJ, Campbell JS, Cunningham MJ, Krebs EG, Dorsa DM (1997) Rapid membrane effects of steroids in neuroblastoma cells: effects of estrogen on mitogen activated protein kinase signalling cascade and c-fos immediate early gene transcription. Endocrinology 138:4030-4033.
62. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
63. Wood GE, Beylin AV, Shors TJ (1998) Hippocampal-dependent trace conditioning is enhanced by stress in males, but impaired by stress in females. Soc Neurosci Abstr 24:267.1.
64. Woolley CS, McEwen BS (1992) Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12:2549-2554.
65. 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.