Hippocampal learning, memory, and neurogenesis: Effects of sex and estrogens across the lifespan in adults

Hormones and Behavior

Volumn 74, Issue , 2015, Pages 37-52

  Duarte Guterman, Paula ^a   Yagi, Shunya ^a   Chow, Carmen ^a   Galea, Liisa A M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Adult neurogenesis; Aging; Cognition; Dentate gyrus; Estrogen receptor; Hippocampus; Reproductive experience; Sex differences

Indexed keywords

ESTRADIOL; ESTROGEN; PROGESTERONE;

AGING; ARTICLE; CELL SURVIVAL; ESTRUS CYCLE; HIPPOCAMPUS; HORMONAL REGULATION; HORMONE ACTION; HUMAN; LEARNING; LIFESPAN; LONG TERM MEMORY; MEMORY; MENSTRUAL CYCLE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; SEX DIFFERENCE; SPATIAL MEMORY; SPATIAL ORIENTATION; ANIMAL; COGNITION; DRUG EFFECTS; FEMALE; GROWTH, DEVELOPMENT AND AGING; MALE; PHYSIOLOGY; RODENT; SEXUAL DEVELOPMENT;

AGING; ANIMALS; COGNITION; ESTRADIOL; ESTROGENS; FEMALE; HIPPOCAMPUS; MALE; MEMORY; NEUROGENESIS; PREGNANCY; RODENTIA; SEX CHARACTERISTICS;

EID: 84941879906     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2015.05.024     Document Type: Article

References (259)

1. Abou-Samra A.B., Pugeat M., Dechaud H., Nachury L., Bouchareb B., Fevre-Montange M., Tourniaire J. Increased plasma concentration of N-terminal beta-lipotrophin and unbound cortisol during pregnancy. Clin. Endocrinol. (Oxf) 1984, 20:221-228.
2. Acosta J.I., Mayer L., Talboom J.S., Zay C., Scheldrup M., Castillo J., Demers L.M., Enders C.K., Bimonte-Nelson H.A. Premarin improves memory, prevents scopolamine-induced amnesia and increases number of basal forebrain choline acetyltransferase positive cells in middle-aged surgically menopausal rats. Horm. Behav. 2009, 55:454-464.
3. Aimone J.B., Wiles J., Gage F.H. Computational influence of adult neurogenesis on memory encoding. Neuron 2009, 61:187-202.
4. Aimone J.B., Li Y., Lee S.W., Clemenson G.D., Deng W., Gage F.H. Regulation and function of adult neurogenesis: from genes to cognition. Physiol. Rev. 2014, 94:991-1026.
5. Akers K.G., Martinez-Canabal A., Restivo L., Yiu A.P., De Cristofaro A., Hsiang H.L., Wheeler A.L., Guskjolen A., Niibori Y., Shoji H., Ohira K., Richards B.A., Miyakawa T., Josselyn S.A., Frankland P.W. Hippocampal neurogenesis regulates forgetting during adulthood and infancy. Science 2014, 344:598-602.
6. Andersen N.E., Dahmani L., Konishi K., Bohbot V.D. Eye tracking, strategies, and sex differences in virtual navigation. Neurobiol. Learn. Mem. 2012, 97:81-89.
7. Baddeley A. Working memory: looking back and looking forward. Nat. Rev. Neurosci. 2003, 4:829-839.
8. Banasr M., Hery M., Brezun J.M., Daszuta A. Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus. Eur. J. Neurosci. 2001, 14:1417-1424.
9. Bannerman D.M., Rawlins J.N., McHugh S.B., Deacon R.M., Yee B.K., Bast T., Zhang W.N., Pothuizen H.H., Feldon J. Regional dissociations within the hippocampus-memory and anxiety. Neurosci. Biobehav. Rev. 2004, 28:273-283.
10. Barha C.K., Galea L.A.M. Influence of different estrogens on neuroplasticity and cognition in the hippocampus. Biochim. Biophys. Acta 2010, 1800:1056-1067.
11. Barha C.K., Galea L.A. Motherhood alters the cellular response to estrogens in the hippocampus later in life. Neurobiol. Aging 2011, 32:2091-2095.
12. Barha C.K., Galea L.A. The hormone therapy, Premarin, impairs hippocampus-dependent spatial learning and memory and reduces activation of new granule neurons in response to memory in female rats. Neurobiol. Aging 2013, 34:986-1004.
13. Barha C.K., Lieblich S.E., Galea L.A. Different forms of oestrogen rapidly upregulate cell proliferation in the dentate gyrus of adult female rats. J. Neuroendocrinol. 2009, 21:155-166.
14. Barha C.K., Dalton G.L., Galea L.A. Low doses of 17alpha-estradiol and 17beta-estradiol facilitate, whereas higher doses of estrone and 17alpha- and 17beta-estradiol impair, contextual fear conditioning in adult female rats. Neuropsychopharmacology 2010, 35:547-559.
15. Barha C.K., Lieblich S.E., Chow C., Galea L.A. Multiparity-induced enhancement of hippocampal neurogenesis and spatial memory depends on ovarian hormone status in middle age. Neurobiol. Aging 2015, 36:2391-2405.
16. Barker J.M., Galea L.A.M. Repeated estradiol administration increases cell proliferation and decreases cell death in female, but not male, rats. Neuroscience 2008, 152:888-902.
17. Barker J.M., Galea L.A. Sex and regional differences in estradiol content in the prefrontal cortex, amygdala and hippocampus of adult male and female rats. Gen. Comp. Endocrinol. 2009, 164:77-84.
18. Barker J.M., Galea L.A. Males show stronger contextual fear conditioning than females after context pre-exposure. Physiol. Behav. 2010, 99:82-90.
19. Baum L.W. Sex, hormones, and Alzheimer's disease. J. Gerontol. A Biol. Sci. Med. Sci. 2005, 60:736-743.
20. Bayer J., Schultz H., Gamer M., Sommer T. Menstrual-cycle dependent fluctuations in ovarian hormones affect emotional memory. Neurobiol. Learn. Mem. 2014, 110:55-63.
21. Beiko J., Lander R., Hampson E., Boon F., Cain D.P. Contribution of sex differences in the acute stress response to sex differences in water maze performance in the rat. Behav. Brain Res. 2004, 151:239-253.
22. Ben Abdallah N.M., Slomianka L., Vyssotski A.L., Lipp H.P. Early age-related changes in adult hippocampal neurogenesis in C57 mice. Neurobiol. Aging 2010, 31:151-161.
23. Bernstein L., Pike M.C., Ross R.K., Judd H.L., Brown J.B., Henderson B.E. Estrogen and sex hormone-binding globulin levels in nulliparous and parous women. J. Natl. Cancer Inst. 1985, 74:741-745.
24. Berry B., McMahan R., Gallagher M. Spatial learning and memory at defined points of the estrous cycle: effects on performance of a hippocampal-dependent task. Behav. Neurosci. 1997, 111:267-274.
25. Bimonte H.A., Denenberg V.H. Estradiol facilitates performance as working memory load increases. Psychoneuroendocrinology 1999, 24:161-173.
26. Bimonte-Nelson H.A., Singleton R.S., Hunter C.L., Price K.L., Moore A.B., Granholm A.C. Ovarian hormones and cognition in the aged female rat: I. Long-term, but not short-term, ovariectomy enhances spatial performance. Behav. Neurosci. 2003, 117:1395-1406.
27. Bimonte-Nelson H.A., Singleton R.S., Williams B.J., Granholm A.C. Ovarian hormones and cognition in the aged female rat: II. progesterone supplementation reverses the cognitive enhancing effects of ovariectomy. Behav. Neurosci. 2004, 118:707-714.
28. Bohacek J., Daniel J.M. The ability of oestradiol administration to regulate protein levels of oestrogen receptor alpha in the hippocampus and prefrontal cortex of middle-aged rats is altered following long-term ovarian hormone deprivation. J. Neuroendocrinol. 2009, 21:640-647.
29. Boulware M.I., Heisler J.D., Frick K.M. The memory-enhancing effects of hippocampal estrogen receptor activation involve metabotropic glutamate receptor signaling. J. Neurosci. 2013, 33:15184-15194.
30. Brailoiu E., Dun S.L., Brailoiu G.C., Mizuo K., Sklar L.A., Oprea T.I., Prossnitz E.R., Dun N.J. Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J. Endocrinol. 2007, 193:311-321.
31. Bridges R.S., Byrnes E.M. Reproductive experience reduces circulating 17beta-estradiol and prolactin levels during proestrus and alters estrogen sensitivity in female rats. Endocrinology 2006, 147:2575-2582.
32. Brinton R.D. The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications. Trends Neurosci. 2008, 31:529-537.
33. Brown J.P., Couillard-Despres S., Cooper-Kuhn C.M., Winkler J., Aigner L., Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 2003, 467:1-10.
34. Butz M., Lehmann K., Dammasch I.E., Teuchert-Noodt G. A theoretical network model to analyse neurogenesis and synaptogenesis in the dentate gyrus. Neural Netw. 2006, 19:1490-1505.
35. Cameron H.A., Glover L.R. Adult neurogenesis: beyond learning and memory. Annu. Rev. Psychol. 2015, 66:53-81.
36. Chakraborty T.R., Gore A.C. Aging-related changes in ovarian hormones, their receptors, and neuroendocrine function. Exp. Biol. Med. 2004, 229:977-987.
37. Chamizo V.D., Artigas A.A., Sansa J., Banterla F. Gender differences in landmark learning for virtual navigation: the role of distance to a goal. Behav. Process. 2011, 88:20-26.
38. Chan M., Chow C., Hamson D.K., Galea L.A.M. Effects of chronic oestradiol, progesterone and medroxyprogesterone acetate on hippocampal neurogenesis and adrenal mass in adult female rats. J. Neuroendocrinol. 2014, 26:386-399.
39. Chang Y.J., Yang C.H., Liang Y.C., Yeh C.M., Huang C.C., Hsu K.S. Estrogen modulates sexually dimorphic contextual fear extinction in rats through estrogen receptor beta. Hippocampus 2009, 19:1142-1150.
40. Cherney I.D., Brabec C.M., Runco D.V. Mapping out spatial ability: sex differences in way-finding navigation. Percept. Mot. Skills 2008, 107:747-760.
41. Chesler E.J., Juraska J.M. Acute administration of estrogen and progesterone impairs the acquisition of the spatial morris water maze in ovariectomized rats. Horm. Behav. 2000, 38:234-242.
42. Chiba S., Suzuki M., Yamanouchi K., Nishihara M. Involvement of granulin in estrogen-induced neurogenesis in the adult rat hippocampus. J. Reprod. Dev. 2007, 53:297-307.
43. Chow C., Epp J.R., Lieblich S.E., Barha C.K., Galea L.A. Sex differences in neurogenesis and activation of new neurons in response to spatial learning and memory. Psychoneuroendocrinology 2013, 38:1236-1250.
44. Christian K.M., Song H., Ming G.L. Functions and dysfunctions of adult hippocampal neurogenesis. Annu. Rev. Neurosci. 2014, 37:243-262.
45. Christie B.R., Cameron H.A. Neurogenesis in the adult hippocampus. Hippocampus 2006, 16:199-207.
46. Clelland C.D., Choi M., Romberg C., Clemenson G.D., Fragniere A., Tyers P., Jessberger S., Saksida L.M., Barker R.A., Gage F.H., Bussey T.J. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 2009, 325:210-213.
47. Conrad C.D., Jackson J.L., Wieczorek L., Baran S.E., Harman J.S., Wright R.L., Korol D.L. Acute stress impairs spatial memory in male but not female rats: influence of estrous cycle. Pharmacol. Biochem. Behav. 2004, 78:569-579.
48. Cuttler C., Graf P., Pawluski J.L., Galea L.A.M. Everyday life memory deficits in pregnant women. Can. J. Exp. Psychol. 2011, 65:27-37.
49. Dabbs J.M., Chang E.-L., Strong R.A., Milun R. Spatial ability, navigation strategy, and geographic knowledge among men and women. Evol. Hum. Behav. 1998, 19:89-98.
50. Daniel J.M. Estrogens, estrogen receptors, and female cognitive aging: the impact of timing. Horm. Behav. 2013, 63:231-237.
51. Daniel J.M., Bohacek J. The critical period hypothesis of estrogen effects on cognition: insights from basic research. Biochim. Biophys. Acta 2010, 1800:1068-1076.
52. Daniel J.M., Fader A.J., Spencer A.L., Dohanich G.P. Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm. Behav. 1997, 32:217-225.
53. Daniel J.M., Hulst J.L., Berbling J.L. Estradiol replacement enhances working memory in middle-aged rats when initiated immediately after ovariectomy but not after a long-term period of ovarian hormone deprivation. Endocrinology 2006, 147:607-614.
54. Darnaudéry M., Perez-Martin M., Del Favero F., Gomez-Roldan C., Garcia-Segura L.M., Maccari S. Early motherhood in rats is associated with a modification of hippocampal function. Psychoneuroendocrinology 2007, 32:803-812.
55. Davis D.M., Jacobson T.K., Aliakbari S., Mizumori S.J. Differential effects of estrogen on hippocampal- and striatal-dependent learning. Neurobiol. Learn. Mem. 2005, 84:132-137.
56. de Groot R.H., Vuurman E.F., Hornstra G., Jolles J. Differences in cognitive performance during pregnancy and early motherhood. Psychol. Med. 2006, 36:1023-1032.
57. Dietrich T., Krings T., Neulen J., Willmes K., Erberich S., Thron A., Sturm W. Effects of blood estrogen level on cortical activation patterns during cognitive activation as measured by functional MRI. NeuroImage 2001, 13:425-432.
58. Dorgan J.F., Reichman M.E., Judd J.T., Brown C., Longcope C., Schatzkin A., Campbell W.S., Franz C., Kahle L., Taylor P.R. Relationships of age and reproductive characteristics with plasma estrogens and androgens in premenopausal women. Cancer Epidemiol. Biomarkers Prev. 1995, 4:381-386.
59. Duarte-Guterman P., Lieblich S.E., Chow C., Galea L.A. Stage-specific changes in neurogenic and glial markers in Alzheimer's disease. Biol. Psychiatry 2015, 10. e0129880.
60. Ekonomou A., Savva G.M., Brayne C., Forster G., Francis P.T., Johnson M., Perry E.K., Attems J., Somani A., Minger S.L., Ballard C.G. Stage-specific changes in neurogenic and glial markers in Alzheimer's disease. Biol. Psychiatry 2015, 77:711-719.
61. Engler-Chiurazzi E., Tsang C., Nonnenmacher S., Liang W.S., Corneveaux J.J., Prokai L., Huentelman M.J., Bimonte-Nelson H.A. Tonic Premarin dose-dependently enhances memory, affects neurotrophin protein levels and alters gene expression in middle-aged rats. Neurobiol. Aging 2011, 32:680-697.
62. Engler-Chiurazzi E.B., Talboom J.S., Braden B.B., Tsang C.W., Mennenga S., Andrews M., Demers L.M., Bimonte-Nelson H.A. Continuous estrone treatment impairs spatial memory and does not impact number of basal forebrain cholinergic neurons in the surgically menopausal middle-aged rat. Horm. Behav. 2012, 62:1-9.
63. Ennaceur A., Neave N., Aggleton J.P. Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp. Brain Res. 1997, 113:509-519.
64. Epp J.R., Haack A.K., Galea L.A.M. Activation and survival of immature neurons in the dentate gyrus with spatial memory is dependent on time of exposure to spatial learning and age of cells at examination. Neurobiol. Learn. Mem. 2011, 95:316-325.
65. Epp J.R., Beasley C.L., Galea L.A. Increased hippocampal neurogenesis and p21 expression in depression: dependent on antidepressants, sex, age, and antipsychotic exposure. Neuropsychopharmacology 2013, 38:2297-2306.
66. Epp J.R., Chow C., Galea L.A. Hippocampus-dependent learning influences hippocampal neurogenesis. Front. Neurosci. 2013, 7:57.
67. Eriksson P.S., Perfilieva E., Björk-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med. 1998, 4:1313-1317.
68. Fantie B.D., Kolb B. An examination of prefrontal lesion size and the effects of cortical grafts on performance of the Morris water task by rats. Psychobiology 1990, 18:74-80.
69. Fester L., Ribeiro-Gouveia V., Prange-Kiel J., von Schassen C., Bottner M., Jarry H., Rune G.M. Proliferation and apoptosis of hippocampal granule cells require local oestrogen synthesis. J. Neurochem. 2006, 97:1136-1144.
70. Fester L., Prange-Kiel J., Jarry H., Rune G.M. Estrogen synthesis in the hippocampus. Cell Tissue Res. 2011, 345:285-294.
71. Fink G., Sumner B.E., McQueen J.K., Wilson H., Rosie R. Sex steroid control of mood, mental state and memory. Clin. Exp. Pharmacol. Physiol. 1998, 25:764-775.
72. Fowler C.D., Johnson F., Wang Z. Estrogen regulation of cell proliferation and distribution of estrogen receptor-alpha in the brains of adult female prairie and meadow voles. J. Comp. Neurol. 2005, 489:166-179.
73. Frick K.M., Fernandez S.M., Bulinski S.C. Estrogen replacement improves spatial reference memory and increases hippocampal synaptophysin in aged female mice. Neuroscience 2002, 115:547-558.
74. Frick K.M., Fernandez S.M., Bennett J.C., Prange-Kiel J., MacLusky N.J., Leranth C. Behavioral training interferes with the ability of gonadal hormones to increase CA1 spine synapse density in ovariectomized female rats. Eur. J. Neurosci. 2004, 19:3026-3032.
75. Frye C.A. Estrus-associated decrements in a water maze task are limited to acquisition. Physiol. Behav. 1995, 57:5-14.
76. Frye C.A., Duffy C.K., Walf A.A. Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task. Neurobiol. Learn. Mem. 2007, 88:208-216.
77. Furuta M., Bridges R.S. Gestation-induced cell proliferation in the rat brain. Brain Res. Dev. Brain Res. 2005, 156:61-66.
78. Galea L.A.M., Kimura D. Sex differences in route-learning. Personal. Individ. Differ. 1993, 14:53-65.
79. Galea L.A.M., McEwen B.S. Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neuroscience 1999, 89:955-964.
80. Galea L.A.M., Kavaliers M., Ossenkopp K.P., Hampson E. Gonadal hormone levels and spatial learning performance in the Morris water maze in male and female meadow voles, Microtus pennsylvanicus. Horm. Behav. 1995, 29:106-125.
81. Galea L.A.M., Ormerod B.K., Sampath S., Kostaras X., Wilkie D.M., Phelps M.T. Spatial working memory and hippocampal size across pregnancy in rats. Horm. Behav. 2000, 37:86-95.
82. Galea L.A., Wide J.K., Paine T.A., Holmes M.M., Ormerod B.K., Floresco S.B. High levels of estradiol disrupt conditioned place preference learning, stimulus response learning and reference memory but have limited effects on working memory. Behav. Brain Res. 2001, 126:115-126.
83. Galea L.A., Lee T.T., Kostaras X., Sidhu J.A., Barr A.M. High levels of estradiol impair spatial performance in the Morris water maze and increase 'depressive-like' behaviors in the female meadow vole. Physiol. Behav. 2002, 77:217-225.
84. Galea L.A., Wainwright S.R., Roes M.M., Duarte-Guterman P., Chow C., Hamson D.K. Sex, hormones and neurogenesis in the hippocampus: hormonal modulation of neurogenesis and potential functional implications. J. Neuroendocrinol. 2013, 25:1039-1061.
85. Gatewood J.D., Morgan M.D., Eaton M., McNamara I.M., Stevens L.F., Macbeth A.H., Meyer E.A., Lomas L.M., Kozub F.J., Lambert K.G., Kinsley C.H. Motherhood mitigates aging-related decrements in learning and memory and positively affects brain aging in the rat. Brain Res. Bull. 2005, 66:91-98.
86. Gibbs R.B. Estrogen replacement enhances acquisition of a spatial memory task and reduces deficits associated with hippocampal muscarinic receptor inhibition. Horm. Behav. 1999, 36:222-233.
87. Gibbs R.B. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiol. Aging 2000, 21:107-116.
88. Gibbs R.B. Estrogen therapy and cognition: a review of the cholinergic hypothesis. Endocr. Rev. 2010, 31:224-253.
89. Gibbs R.B., Johnson D.A. Sex-specific effects of gonadectomy and hormone treatment on acquisition of a 12-arm radial maze task by Sprague Dawley rats. Endocrinology 2008, 149:3176-3183.
90. Glasper E.R., Schoenfeld T.J., Gould E. Adult neurogenesis: optimizing hippocampal function to suit the environment. Behav. Brain Res. 2012, 227:380-383.
91. Glynn L.M. Giving birth to a new brain: hormone exposure of pregnancy influence human memory. Psychoneuroendocrinology 2010, 35:1148-1155.
92. Glynn L.M. Increasing parity is associated with cumulative effects on memory. J. Women's Health 2012, 21:1038-1045.
93. Gould E., Beylin A., Tanapat P., Reeves A., Shors T.J. Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 1999, 2:260-265.
94. Green A.D., Galea L.A. Adult hippocampal cell proliferation is suppressed with estrogen withdrawal after a hormone-simulated pregnancy. Horm. Behav. 2008, 54:203-211.
95. Gresack J.E., Frick K.M. Post-training estrogen enhances spatial and object memory consolidation in female mice. Pharmacol. Biochem. Behav. 2006, 84:112-119.
96. Grissom E.M., Hawley W.R., Hodges K.S., Fawcett-Patel J.M., Dohanich G.P. Biological sex influences learning strategy preference and muscarinic receptor binding in specific brain regions of prepubertal rats. Hippocampus 2013, 23:313-322.
97. Gupta R.R., Sen S., Diepenhorst L.L., Rudick C.N., Maren S. Estrogen modulates sexually dimorphic contextual fear conditioning and hippocampal long-term potentiation (LTP) in rats. Brain Res. 2001, 888:356-365.
98. Gutierrez-Lobos K., Scherer M., Anderer P., Katschnig H. The influence of age on the female/male ratio of treated incidence rates in depression. BMC Psychiatry 2002, 2:3.
99. Guzowski J.F., Setlow B., Wagner E.K., Mcgaugh J.L. Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J. Neurosci. 2001, 21:5089-5098.
100. Hammond R., Mauk R., Ninaci D., Nelson D., Gibbs R.B. Chronic treatment with estrogen receptor agonists restores acquisition of a spatial learning task in young ovariectomized rats. Horm. Behav. 2009, 56:309-314.
101. Hammond R., Nelson D., Kline E., Gibbs R.B. Chronic treatment with a GPR30 antagonist impairs acquisition of a spatial learning task in young female rats. Horm. Behav. 2012, 62:367-374.
102. Hampson E. Variations in sex-related cognitive abilities across the menstrual cycle. Brain Cogn. 1990, 14:26-43.
103. Hamson D.K., Wainwright S.R., Taylor J.R., Jones B.A., Watson N.V., Galea L.A.M. Androgens increase survival of adult-born neurons in the dentate gyrus by an androgen receptor-dependent mechanism in male rats. Endocrinology 2013, 154:3294-3304.
104. Hapon M.B., Simoncini M., Via G., Jahn G.A. Effect of hypothyroidism on hormone profiles in virgin, pregnant and lactating rats, and on lactation. Reproduction 2003, 126:371-382.
105. Harburger L.L., Bennett J.C., Frick K.M. Effects of estrogen and progesterone on spatial memory consolidation in aged females. Neurobiol. Aging 2007, 28:602-610.
106. Hastings N.B., Gould E. Rapid extension of axons into the CA3 region by adult-generated granule cells. J. Comp. Neurol. 1999, 413:146-154.
107. Hausmann M., Slabbekoom D., Van Goozen S.H.M., Cohen-Kettenis P.T., Güntürkün O. Sex hormones affect spatial abilities during the menstrual cycle. Behav. Neurosci. 2000, 114:1245-1250.
108. Hawley W.R., Grissom E.M., Barratt H.E., Conrad T.S., Dohanich G.P. The effects of biological sex and gonadal hormones on learning strategy in adult rats. Physiol. Behav. 2012, 105:1014-1020.
109. Hawley W.R., Grissom E.M., Moody N.M., Dohanich G.P., Vasudevan N. Activation of G-protein-coupled receptor 30 is sufficient to enhance spatial recognition memory in ovariectomized rats. Behav. Brain Res. 2014, 262:68-73.
110. Hazell G.G., Yao S.T., Roper J.A., Prossnitz E.R., O'Carroll A.M., Lolait S.J. Localisation of GPR30, a novel G protein-coupled oestrogen receptor, suggests multiple functions in rodent brain and peripheral tissues. J. Endocrinol. 2009, 202:223-236.
111. Henry J.D., Rendell P.G. A review of the impact of pregnancy on memory function. J. Clin. Exp. Neuropsychol. 2007, 29:793-803.
112. Henry J.F., Sherwin B.B. Hormones and cognitive functioning during late pregnancy and postpartum: a longitudinal study. Behav. Neurosci. 2012, 126:73-85.
113. Hillerer K.M., Neumann I.D., Couillard-Despres S., Aigner L., Slattery D.A. Sex-dependent regulation of hippocampal neurogenesis under basal and chronic stress conditions in rats. Hippocampus 2013, 23:476-487.
114. Hillerer K.M., Neumann I.D., Couillard-Despres S., Aigner L., Slattery D.A. Lactation-induced reduction in hippocampal neurogenesis is reversed by repeated stress exposure. Hippocampus 2014, 24:673-683.
115. Hogervorst E., Williams J., Budge M., Riedel W., Jolles J. The nature of the effect of female gonadal hormone replacement therapy on cognitive function in post-menopausal women: a meta-analysis. Neuroscience 2000, 101:485-512.
116. Holding C.S., Holding D.H. Acquisition of route network knowledge by males and females. J. Gen. Psychol. 1989, 116:29-41.
117. Holmes M.M., Wide J.K., Galea L.A. Low levels of estradiol facilitate, whereas high levels of estradiol impair, working memory performance on the radial arm maze. Behav. Neurosci. 2002, 116:928-934.
118. Ingberg E., Theodorsson A., Theodorsson E., Strom J.O. Methods for long-term 17β-estradiol administration to mice. Gen. Comp. Endocrinol. 2012, 175:188-193.
119. Jacobs E., D'Esposito M. Estrogen shapes dopamine-dependent cognitive processes: implications for women's health. J. Neurosci. 2011, 31:5286-5293.
120. Jacome L.F., Gautreaux C., Inagaki T., Mohan G., Alves S., Lubbers L.S., Luine V. Estradiol and ERbeta agonists enhance recognition memory, and DPN, an ERbeta agonist, alters brain monoamines. Neurobiol. Learn. Mem. 2010, 94:488-498.
121. Jakubs K., Nanobashvili A., Bonde S., Ekdahl C.T., Kokaia Z., Kokaia M., Lindvall O. Environment matters: synaptic properties of neurons born in the epileptic adult brain develop to reduce excitability. Neuron 2006, 52:1047-1059.
122. Jasnow A.M., Schulkin J., Pfaff D.W. Estrogen facilitates fear conditioning and increases corticotropin-releasing hormone mRNA expression in the central amygdala in female mice. Horm. Behav. 2006, 49:197-205.
123. Jessberger S., Kempermann G. Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur. J. Neurosci. 2003, 18:2707-2712.
124. Jessberger S., Nakashima K., Clemenson G.D., Mejia E., Mathews E., Ure K., Ogawa S., Sinton C.M., Gage F.H., Hsieh J. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J. Neurosci. 2007, 27:5967-5975.
125. Jin K., Peel A.L., Mao X.O., Xie L., Cottrell B.A., Henshall D.C., Greenberg D.A. Increased hippocampal neurogenesis in Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:343-347.
126. Joffe H., Cohen L.S. Estrogen, serotonin, and mood disturbance: where is the therapeutic bridge?. Biol. Psychiatry 1998, 44:798-811.
127. Jonasson Z. Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data. Neurosci. Biobehav. Rev. 2005, 28:811-825.
128. Jones M.W., Errington M.L., French P.J., Fine A., Bliss T.V.P., Garel S., Charnay P., Bozon B., Laroche S., Davis S. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat. Neurosci. 2001, 4:289-296.
129. Kaufman S.B. Sex differences in mental rotation and spatial visualization ability: can they be accounted for by differences in working memory capacity?. Intelligence 2007, 35:211-223.
130. Kee N., Teixeira C.M., Wang A.H., Frankland P.W. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci. 2007, 10:355-362.
131. Key T., Appleby P., Barnes I., Reeves G. Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J. Natl. Cancer Inst. 2002, 94:606-616.
132. Kinsley C.H., Madonia L., Gifford G.W., Tureski K., Griffin G.R., Lowry C., Williams J., Collins J., McLearie H., Lambert K.G. Motherhood improves learning and memory. Nature 1999, 402:137-138.
133. Kinsley C.H., Trainer R., Stafisso-Sandoz G., Quadros P., Marcus L.K., Hearon C., Meyer E.A., Hester N., Morgan M., Kozub F.J., Lambert K.G. Motherhood and the hormones of pregnancy modify concentrations of hippocampal neuronal dendritic spines. Horm. Behav. 2006, 49:131-142.
134. Kinsley C.H., Franssen R.A., Meyer E.A. Reproductive experience may positively adjust the trajectory of senescence. Curr. Top. Behav. Neurosci. 2012, 10:317-345.
135. Kiss A., Delattre A.M., Pereira S.I., Carolino R.G., Szawka R.E., Anselmo-Franci J.A., Zanata S.M., Ferraz A.C. 17beta-estradiol replacement in young, adult and middle-aged female ovariectomized rats promotes improvement of spatial reference memory and an antidepressant effect and alters monoamines and BDNF levels in memory- and depression-related brain areas. Behav. Brain Res. 2012, 227:100-108.
136. Kjelstrup K.G., Tuvnes F.A., Steffenach H.A., Murison R., Moser E.I., Moser M.B. Reduced fear expression after lesions of the ventral hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:10825-10830.
137. Klaus F., Hauser T., Lindholm A.K., Cameron H.A., Slomianka L., Lipp H.P., Amrein I. Different regulation of adult hippocampal neurogenesis in Western house mice (Mus musculus domesticus) and C57BL/6 mice. Behav. Brain Res. 2012, 227:340-347.
138. Kolb B., Cioe J. Sex-related differences in cortical function after medial frontal lesions in rats. Behav. Neurosci. 1996, 110:1271-1281.
139. Korol D.L., Malin E.L., Borden K.A., Busby R.A., Couper-Leo J. Shifts in preferred learning strategy across the estrous cycle in female rats. Horm. Behav. 2004, 45:330-338.
140. Kubik S., Miyashita T., Guzowski J.F. Using immediate-early genes to map hippocampal subregional functions. Learn. Mem. 2007, 14:758-770.
141. Kuhn H.G., Dickinson-Anson H., Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 1996, 16:2027-2033.
142. Lagace D.C., Fischer S.J., Eisch A.J. Gender and endogenous levels of estradiol do not influence adult hippocampal neurogenesis in mice. Hippocampus 2007, 17:175-180.
143. Lavenex P., Steele M.A., Jacobs L.F. The seasonal pattern of cell proliferation and neuron number in the dentate gyrus of wild adult eastern grey squirrels. Eur. J. Neurosci. 2000, 12:643-648.
144. Lawton C.A. Gender differences in way-finding strategies: relationship to spatial ability and spatial anxiety. Sex Roles 1994, 30:765-779.
145. Lee T.T., Wainwright S.R., Hill M.N., Galea L.A., Gorzalka B.B. Sex, drugs, and adult neurogenesis: sex-dependent effects of escalating adolescent cannabinoid exposure on adult hippocampal neurogenesis, stress reactivity, and amphetamine sensitization. Hippocampus 2014, 24:280-292.
146. Lemaire V., Billard J.M., Dutar P., George O., Piazza P.V., Epelbaum J., Le Moal M., Mayo W. Motherhood-induced memory improvement persists across lifespan in rats but is abolished by a gestational stress. Eur. J. Neurosci. 2006, 23:3368-3374.
147. Leuner B., Gould E., Shors T.J. Is there a link between adult neurogenesis and learning?. Hippocampus 2006, 16:216-224.
148. Leuner B., Waddell J., Gould E., Shors T.J. Temporal discontiguity is neither necessary nor sufficient for learning-induced effects on adult neurogenesis. J. Neurosci. 2006, 26:13437-13442.
149. 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.
150. Liu F., Day M., Muniz L.C., Bitran D., Arias R., Revilla-Sanchez R., Grauer S., Zhang G., Kelley C., Pulito V., Sung A., Mervis R.F., Navarra R., Hirst W.D., Reinhart P.H., Marquis K.L., Moss S.J., Pangalos M.N., Brandon N.J. Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat. Neurosci. 2008, 11:334-343.
151. Luine V., Rodriguez M. Effects of estradiol on radial arm maze performance of young and aged rats. Behav. Neural Biol. 1994, 62:230-236.
152. Luine V.N., Jacome L.F., Maclusky N.J. Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 2003, 144:2836-2844.
153. Ma X., Hamadeh M.J., Christie B.R., Foster J.A., Tarnopolsky M.A. Impact of treadmill running and sex on hippocampal neurogenesis in the mouse model of amyotrophic lateral sclerosis. PLoS One 2012, 7:e36048.
154. Macbeth A.H., Scharfman H.E., Maclusky N.J., Gautreaux C., Luine V.N. Effects of multiparity on recognition memory, monoaminergic neurotransmitters, and brain-derived neurotrophic factor (BDNF). Horm. Behav. 2008, 54:7-17.
155. Magiakou M.A., Mastorakos G., Webster E., Chrousos G.P. The hypothalamic-pituitary-adrenal axis and the female reproductive system. Ann. N. Y. Acad. Sci. 1997, 816:42-56.
156. Maki P.M., Rich J.B., Rosenbaum R.S. Implicit memory varies across the menstrual cycle: estrogen effects in young women. Neuropsychologia 2002, 40:518-529.
157. Malberg J.E., Eisch A.J., Nestler E.J., Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 2000, 20:9104-9110.
158. Maren S., De Oca B., Fanselow M.S. Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: positive correlation between LTP and contextual learning. Brain Res. 1994, 661:25-34.
159. Markus E.J., Zecevic M. Sex differences and estrous cycle changes in hippocampus-dependent fear conditioning. Psychobiology 1997, 25:246-252.
160. Mazzucco C.A., Lieblich S.E., Bingham B.I., Williamson M.A., Viau V., Galea L.A. Both estrogen receptor alpha and estrogen receptor beta agonists enhance cell proliferation in the dentate gyrus of adult female rats. Neuroscience 2006, 141:1793-1800.
161. McClure R.E., Barha C.K., Galea L.A. 17beta-Estradiol, but not estrone, increases the survival and activation of new neurons in the hippocampus in response to spatial memory in adult female rats. Horm. Behav. 2013, 63:144-157.
162. McEwen B.S., Milner T.A. Hippocampal formation: shedding light on the influence of sex and stress on the brain. Brain Res. Rev. 2007, 55:343-355.
163. McEwen B.S., Akama K.T., Spencer-Segal J.L., Milner T.A., Waters E.M. Estrogen effects on the brain: actions beyond the hypothalamus via novel mechanisms. Behav. Neurosci. 2012, 126:4-16.
164. McKinnon M.C., Yucel K., Nazarov A., MacQueen G.M. A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder. J. Psychiatry Neurosci. 2009, 34:41-54.
165. Méndez-López M., Méndez M., López L., Arias J.L. Sexually dimorphic c-Fos expression following spatial working memory in young and adult rats. Physiol. Behav. 2009, 98:307-317.
166. Milad M.R., Goldstein J.M., Orr S.P., Wedig M.M., Klibanski A., Pitman R.K., Rauch S.L. Fear conditioning and extinction: influence of sex and menstrual cycle in healthy humans. Behav. Neurosci. 2006, 120:1196-1203.
167. Milad M.R., Igoe S.A., Lebron-Milad K., Novales J.E. Estrous cycle phase and gonadal hormones influence conditioned fear extinction. Neuroscience 2009, 164:887-895.
168. Moffat S.D., Hampson E., Hatzipantelis M. Navigation in a "virtual" maze: sex differences and correlation with psychometric measures of spatial ability in humans. Evol. Hum. Behav. 1998, 19:73-87.
169. Moody M.S. Changes in scores on the mental rotations test during the menstrual cycle. Percept. Mot. Skills 1997, 84:955-961.
170. Moser E., Moser M.B., Andersen P. Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J. Neurosci. 1993, 13:3916-3925.
171. Nagy A.I., Ormerod B.K., Mazzucco C.A., Galea L.A. Estradiol-induced enhancement in cell proliferation is mediated through estrogen receptors in the dentate gyrus of adult female rats. Drug Dev. Res. 2006, 66:142-149.
172. Nowakowski R.S., Lewin S.B., Miller M.W. Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J. Neurocytol. 1989, 18:311-318.
173. Oatridge A., Holdcroft A., Saeed N., Hajnal J.V., Puri B.K., Fusi L., Bydder G.M. Change in brain size during and after pregnancy: study in healthy women and women with preeclampsia. AJNR Am. J. Neuroradiol. 2002, 23:19-26.
174. Olariu A., Cleaver K.M., Cameron H.A. Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle. J. Comp. Neurol. 2007, 501:659-667.
175. Olton D.S., Papas B.C. Spatial memory and hippocampal function. Neuropsychologia 1979, 17:669-682.
176. Opendak M., Gould E. Adult neurogenesis: a substrate for experience-dependent change. Trends Cogn. Sci. 2015, 19:151-161.
177. Ormerod B.K., Galea L.A. Reproductive status influences cell proliferation and cell survival in the dentate gyrus of adult female meadow voles: a possible regulatory role for estradiol. Neuroscience 2001, 102:369-379.
178. Ormerod B.K., Lee T.T., Galea L.A. Estradiol initially enhances but subsequently suppresses (via adrenal steroids) granule cell proliferation in the dentate gyrus of adult female rats. J. Neurobiol. 2003, 55:247-260.
179. Ormerod B.K., Lee T.T., Galea L.A. Estradiol enhances neurogenesis in the dentate gyri of adult male meadow voles by increasing the survival of young granule neurons. Neuroscience 2004, 128:645-654.
180. Packard M.G. Posttraining estrogen and memory modulation. Horm. Behav. 1998, 34:126-139.
181. Parent J.M. Adult neurogenesis in the intact and epileptic dentate gyrus. Prog. Brain Res. 2007, 163:529-540.
182. Paris J.J., Frye C.A. Estrous cycle, pregnancy, and parity enhance performance of rats in object recognition or object placement tasks. Reproduction 2008, 136:105-115.
183. Parsons T. Sex differences in mental rotation and spatial rotation in a virtual environment. Neuropsychologia 2004, 42:555-562.
184. Pawluski J.L., Galea L.A. Hippocampal morphology is differentially affected by reproductive experience in the mother. J. Neurobiol. 2006, 66:71-81.
185. Pawluski J.L., Galea L.A. Reproductive experience alters hippocampal neurogenesis during the postpartum period in the dam. Neuroscience 2007, 149:53-67.
186. Pawluski J.L., Vanderbyl B.L., Ragan K., Galea L.A. First reproductive experience persistently affects spatial reference and working memory in the mother and these effects are not due to pregnancy or 'mothering' alone. Behav. Brain Res. 2006, 175:157-165.
187. Pawluski J.L., Walker S.K., Galea L.A. Reproductive experience differentially affects spatial reference and working memory performance in the mother. Horm. Behav. 2006, 49:143-149.
188. Pawluski J.L., Brummelte S., Barha C.K., Crozier T.M., Galea L.A. Effects of steroid hormones on neurogenesis in the hippocampus of the adult female rodent during the estrous cycle, pregnancy, lactation and aging. Front. Neuroendocrinol. 2009, 30:343-357.
189. Peragine D.E., Simpson J.A., Mooney S.J., Lovern M.B., Holmes M.M. Social regulation of adult neurogenesis in a eusocial mammal. Neuroscience 2014, 268:10-20.
190. Perez S.E., Chen E.Y., Mufson E.J. Distribution of estrogen receptor alpha and beta immunoreactive profiles in the postnatal rat brain. Brain Res. Dev. Brain Res. 2003, 145:117-139.
191. Perez-Martin M., Azcoitia I., Trejo J.L., Sierra A., Garcia-Segura L.M. An antagonist of estrogen receptors blocks the induction of adult neurogenesis by insulin-like growth factor-I in the dentate gyrus of adult female rat. Eur. J. Neurosci. 2003, 18:923-930.
192. Perez-Martin M., Salazar V., Castillo C., Ariznavarreta C., Azcoitia I., Garcia-Segura L.M., Tresguerres J.A. Estradiol and soy extract increase the production of new cells in the dentate gyrus of old rats. Exp. Gerontol. 2005, 40:450-453.
193. Postma A., Jager G., Kessels R.P., Koppeschaar H.P., van Honk J. Sex differences for selective forms of spatial memory. Brain Cogn. 2004, 54:24-34.
194. Prossnitz E.R., Oprea T.I., Sklar L.A., Arterburn J.B. The ins and outs of GPR30: a transmembrane estrogen receptor. J. Steroid Biochem. Mol. Biol. 2008, 109:350-353.
195. Rao M.S., Hattiangady B., Abdel-Rahman A., Stanley D.P., Shetty A.K. Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. Eur. J. Neurosci. 2005, 21:464-476.
196. Rao M.S., Hattiangady B., Shetty A.K. The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 2006, 5:545-558.
197. Rhodes M.E., Frye C.A. ERbeta-selective SERMs produce mnemonic-enhancing effects in the inhibitory avoidance and water maze tasks. Neurobiol. Learn. Mem. 2006, 85:183-191.
198. Richardson R.M., Sun D., Bullock M.R. Neurogenesis after traumatic brain injury. Neurosurg. Clin. N. Am. 2007, 18(169-81):xi.
199. Rodgers S.P., Bohacek J., Daniel J.M. Transient estradiol exposure during middle age in ovariectomized rats exerts lasting effects on cognitive function and the hippocampus. Endocrinology 2010, 151:1194-1203.
200. Roes M.M., Galea L.A.M. The maternal brain: short and long-term effects of reproductive experience on hippocampus structure and function in adulthood. Sex Differences in the Central Nervous System 2015, Elsevier, (in press). R. Shansky, J. Johnson (Eds.).
201. Rolls A., Schori H., London A., Schwartz M. Decrease in hippocampal neurogenesis during pregnancy: a link to immunity. Mol. Psychiatry 2008, 13:468-469.
202. Rosenblatt J.S., Mayer A.D., Giordano A.L. Hormonal basis during pregnancy for the onset of maternal behavior in the rat. Psychoneuroendocrinology 1988, 13:29-46.
203. Roughton K., Kalm M., Blomgren K. Sex-dependent differences in behavior and hippocampal neurogenesis after irradiation to the young mouse brain. Eur. J. Neurosci. 2012, 36:2763-2772.
204. Ruigrok A.N., Salimi-Khorshidi G., Lai M.C., Baron-Cohen S., Lombardo M.V., Tait R.J., Suckling J. A meta-analysis of sex differences in human brain structure. Neurosci. Biobehav. Rev. 2014, 39:34-50.
205. Rummel J., Epp J.R., Galea L.A.M. Estradiol does not influence strategy choice but place strategy choice is associated with increased cell proliferation in the hippocampus of female rats. Horm. Behav. 2010, 58:582-590.
206. Ryan J., Scali J., Carriere I., Ritchie K., Ancelin M.L. Hormonal treatment, mild cognitive impairment and Alzheimer's disease. Int. Psychogeriatr. 2008, 20:47-56.
207. Ryan J., Carriere I., Scali J., Ritchie K., Ancelin M.L. Life-time estrogen exposure and cognitive functioning in later life. Psychoneuroendocrinology 2009, 34:287-298.
208. Scharfman H.E., MacLusky N.J. Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: complexity of steroid hormone-growth factor interactions in the adult CNS. Front. Neuroendocrinol. 2006, 27:415-435.
209. Scharfman H., Goodman J., Macleod A., Phani S., Antonelli C., Croll S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 2005, 192:348-356.
210. Scharfman H., Goodman J., McCloskey D. Ectopic granule cells of the rat dentate gyrus. Dev. Neurosci. 2007, 29:14-27.
211. Scheff S.W., Price D.A., Schmitt F.A., Mufson E.J. Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment. Neurobiol. Aging 2006, 27:1372-1384.
212. Seki T. Expression patterns of immature neuronal markers PSA-NCAM, CRMP-4 and NeuroD in the hippocampus of young adult and aged rodents. J. Neurosci. Res. 2002, 70:327-334.
213. Selden N.R.W., Everitt B.J., Jarrard L.E., Robbins T.W. Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues. Neuroscience 1991, 42:335-350.
214. Sharp K., Brindle P.M., Brown M.W., Turner G.M. Memory loss during pregnancy. Br. J. Obstet. Gynaecol. 1993, 100:209-215.
215. Sheng M., Greenberg M.E. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 1990, 4:477-485.
216. Sherwin B.B. Estrogen and cognitive functioning in women. Endocr. Rev. 2003, 24:133-151.
217. Sherwin B.B., Henry J.F. Brain aging modulates the neuroprotective effects of estrogen on selective aspects of cognition in women: a critical review. Front. Neuroendocrinol. 2008, 29:88-113.
218. Shors T.J., Lewczyk C., Pacynski M., Matthew P.R., Pickett J. Stages of estrous mediate the stress-induced impairment of associative learning in the female rat. NeuroReport 1998, 9:419-423.
219. Shors T.J., Townsend D.A., Zhao M., Kozorovitskiy Y., Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 2002, 12:578-584.
220. Silber M., Almkvist O., Larsson B., Uvnäs-Moberg K. Temporary peripartal impairment in memory and attention and its possible relation to oxytocin concentration. Life Sci. 1990, 47:57-65.
221. Silverman I., Choi J. Non-Euclidean navigational strategies of women: compensatory response or evolved dimorphism?. Evol. Psychol. 2006, 4:75-84.
222. Sinopoli K.J., Floresco S.B., Galea L.A.M. Systemic and local administration of estradiol into the prefrontal cortex or hippocampus differentially alters working memory. Neurobiol. Learn Mem. 2006, 86(3):293-304.
223. Smith M.S., Freeman M.E., Neill J.D. The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology 1975, 96:219-226.
224. Snyder J.S., Hong N.S., McDonald R.J., Wojtowicz J.M. A role for adult neurogenesis in spatial long-term memory. Neuroscience 2005, 130:843-852.
225. Snyder J.S., Choe J.S., Clifford M.A., Jeurling S.I., Hurley P., Brown A., Kamhi J.F., Cameron H.A. Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J. Neurosci. 2009, 29:14484-14495.
226. Snyder J.S., Radik R., Wojtowicz J.M., Cameron H.A. Anatomical gradients of adult neurogenesis and activity: young neurons in the ventral dentate gyrus are activated by water maze training. Hippocampus 2009, 19:360-370.
227. Spritzer M.D., Galea L.A.M. Testosterone and dihydrotestosterone, but not estradiol, enhance survival of new hippocampal neurons in adult male rats. Dev. Neurobiol. 2007, 67:1321-1333.
228. Spritzer M.D., Gill M., Weinberg A., Galea L.A.M. Castration differentially affects spatial working and reference memory in male rats. Arch. Sex. Behav. 2008, 37:19-29.
229. Spritzer M.D., Fox E.C., Larsen G.D., Batson C.G., Wagner B.A., Maher J. Testosterone influences spatial strategy preferences among adult male rats. Horm. Behav. 2013, 63:800-812.
230. Ström J.O., Ingberg E. Impact of methodology on estrogens' effects on cerebral ischemia in rats: an updated meta-analysis. BMC Neurosci. 2014, 15:22.
231. Ström J.O., Theodorsson E., Theodorsson A. Order of magnitude differences between methods for maintaining physiological 17beta-oestradiol concentrations in ovariectomized rats. Scand. J. Clin. Lab. Invest. 2008, 68:814-822.
232. Sundström Poromaa I., Gingnell M. Menstrual cycle influence on cognitive function and emotion processing-from a reproductive perspective. Front. Neurosci. 2014, 8:380. eCollection 2014. 10.3389/fnins.2014.00380.
233. Talboom J.S., Williams B.J., Baxley E.R., West S.G., Bimonte-Nelson H.A. Higher levels of estradiol replacement correlate with better spatial memory in surgically menopausal young and middle-aged rats. Neurobiol. Learn. Mem. 2008, 90:155-163.
234. Tanapat P., Hastings N.B., Reeves A.J., Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 1999, 19:5792-5801.
235. Tanapat P., Hastings N.B., Gould E. Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. J. Comp. Neurol. 2005, 481:252-265.
236. Taupin P. BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res. Rev. 2007, 53:198-214.
237. Theodorsson A., Hilke S., Rugarn O., Linghammar D., Theodorsson E. Serum concentrations of 17beta-estradiol in ovariectomized rats during two times six weeks crossover treatment by daily injections in comparison with slow-release pellets. Scand. J. Clin. Lab. Invest. 2005, 65:699-705.
238. Towart L.A., Alves S.E., Znamensky V., Hayashi S., McEwen B.S., Milner T.A. Subcellular relationships between cholinergic terminals and estrogen receptor-alpha in the dorsal hippocampus. J. Comp. Neurol. 2003, 463:390-401.
239. Tzeng W.Y., Chen L.H., Cherng C.G., Tsai Y.N., Yu L. Sex differences and the modulating effects of gonadal hormones on basal and the stressor-decreased newly proliferative cells and neuroblasts in dentate gyrus. Psychoneuroendocrinology 2014, 42:24-37.
240. Uban K.A., Sliwowska J.H., Lieblich S., Ellis L.A., Yu W.K., Weinberg J., Galea L.A. Prenatal alcohol exposure reduces the proportion of newly produced neurons and glia in the dentate gyrus of the hippocampus in female rats. Horm. Behav. 2010, 58:835-843.
241. Uban K.A., Rummel J., Floresco S.B., Galea L.A. Estradiol modulates effort-based decision making in female rats. Neuropsychopharmacology 2012, 37:390-401.
242. Vanston C.M., Watson N.V. Selective and persistent effect of foetal sex on cognition in pregnant women. NeuroReport 2005, 16:779-782.
243. Vasudevan N., Pfaff D.W. Non-genomic actions of estrogens and their interaction with genomic actions in the brain. Front. Neuroendocrinol. 2008, 29:238-257.
244. Viau V., Meaney M.J. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 1991, 129:2503-2511.
245. Voyer D., Voyer S., Bryden M.P. Magnitude of sex differences in spatial abilities: a meta-analysis and consideration of critical variables. Psychol. Bull. 1995, 117:250-270.
246. Warren S.G., Juraska J.M. Spatial and nonspatial learning across the rat estrous cycle. Behav. Neurosci. 1997, 111:259-266.
247. White N.M., McDonald R.J. Multiple parallel memory systems in the brain of the rat. Neurobiol. Learn. Mem. 2002, 77:125-184.
248. Williams C.L., Barnett A.M., Meek W.H. Organizational effects of early gonadal secretions on sexual differentiation in spatial memory. Behav. Neurosci. 1990, 104:84-97.
249. Winocur G., Wojtowicz J.M., Sekeres M., Snyder J.S., Wang S. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 2006, 16:296-304.
250. Witty C.F., Foster T.C., Semple-Rowland S.L., Daniel J.M. Increasing hippocampal estrogen receptor alpha levels via viral vectors increases MAP kinase activation and enhances memory in aging rats in the absence of ovarian estrogens. PLoS One 2012, 7:e51385.
251. Woolley D.G., Vermaercke B., Op de Beeck H., Wagemans J., Gantois I., D'Hooge R., Swinnen S.P., Wenderoth N. Sex differences in human virtual water maze performance: novel measures reveal the relative contribution of directional responding and spatial knowledge. Behav. Brain Res. 2010, 208:408-414.
252. Workman J.L., Raineki C., Weinberg J., Galea L.A.M. Alcohol and pregnancy: effects on maternal care, HPA axis function, and hippocampal neurogenesis in adult females. Psychoneurendocrinol. 2015, 57:37-50.
253. Wu A.H., Pike M.C., Stram D.O. Meta-analysis: dietary fat intake, serum estrogen levels, and the risk of breast cancer. J. Natl. Cancer Inst. 1999, 91:529-534.
254. Yoon T., Okada J., Jung M.W., Kim J.J. Prefrontal cortex and hippocampus subserve different components of working memory in rats. Learn. Mem. 2008, 15:97-105.
255. Zhang Q.G., Raz L., Wang R., Han D., De Sevilla L., Yang F., Vadlamudi R.K., Brann D.W. Estrogen attenuates ischemic oxidative damage via an estrogen receptor alpha-mediated inhibition of NADPH oxidase activation. J. Neurosci. 2009, 29:13823-13836.
256. Zhang Z., Yang R., Zhou R., Li L., Sokabe M., Chen L. Progesterone promotes the survival of newborn neurons in the dentate gyrus of adult male mice. Hippocampus 2010, 20:402-412.
257. Zhao H., Tian Z., Hao J., Chen B. Extragonadal aromatization increases with time after ovariectomy in rats. Reprod. Biol. Endocrinol. 2005, 3:6.
258. Zhao C., Teng E.M., Summers R.G., Ming G.L., Gage F.H. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J. Neurosci. 2006, 26:3-11.
259. Zhou J., Zhang H., Cohen R.S., Pandey S.C. 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.