The Effect of Ovariectomy on Learning and Memory and Relationship to Changes in Brain Volume and Neuronal Density

REFERENCES

• Fox NC, Warrington EK, Rossor MN. Serial magnetic resonance imaging of cerebral atrophy in preclinical Alzheimer's disease. Lancet. 1999;353:21–5.
   Web of Science ®Google Scholar
• Misra C, Fan Y, Davatzikos C. Baseline and longitudinal patterns of brain atrophy in MCI patients, and their use in prediction of short-term conversion to AD: results from ADNI. Neuroimage. 2009;44:1415–22.
   PubMed Web of Science ®Google Scholar
• Chetelat G, Landeau B, Eustache F, Mezenge F, Viader F, de la Sayette V, Desgranges B, Baron JC. Using voxel-based morphometry to map the structural changes associated with rapid conversion in MCI: a longitudinal MRI study. Neuroimage. 2005;27:934–46.
   PubMed Web of Science ®Google Scholar
• Driscoll I, Davatzikos C, An Y, Wu X, Shen D, Kraut M, Resnick SM. Longitudinal pattern of regional brain volume change differentiates normal aging from MCI. Neurology. 2009;72:1906–13.
   PubMed Web of Science ®Google Scholar
• Smith CD, Chebrolu H, Wekstein DR, Schmitt FA, Jicha GA, Cooper G, Markesbery WR. Brain structural alterations before mild cognitive impairment. Neurology. 2007;68:1268–73.
   PubMedGoogle Scholar
• Henderson VW. Estrogen, cognition, and a woman's risk of Alzheimer's disease. Am J Med. 1997;103:11S–8S.
   Google Scholar
• Rehman HU, Masson EA. Neuroendocrinology of female aging. Gender Medicine. 2005;2:41–56.
   PubMedGoogle Scholar
• Genazzani AR, Pluchino N, Luisi S, Luisi M. Estrogen, cognition and female ageing. Hum Reprod Update. 2007;13:175–87.
   PubMed Web of Science ®Google Scholar
• Daniel JM, Hulst JL, Berbling JL. 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;147:607–14.
   PubMed Web of Science ®Google Scholar
• Gibbs RB, Gabor R, Cox T, Johnson DA. Effects of raloxifene and estradiol on hippocampal acetylcholine release and spatial learning in the rat. Psychoneuroendocrinology. 2004;29:741–48.
   Web of Science ®Google Scholar
• Iivonen S, Heikkinen T, Puolivali J, Helisalmi S, Hiltunen M, Soininen H, Tanila H. Effects of estradiol on spatial learning, hippocampal cytochrome P450 19, and estrogen alpha and beta mRNA levels in ovariectomized female mice. Neuroscience. 2006;137:1143–52.
   PubMed Web of Science ®Google Scholar
• Zurkovsky L, Brown SL, Korol DL. Estrogen modulates place learning through estrogen receptors in the hippocampus. Neurobio Learn Mem. 2006;86:336–43.
   PubMed Web of Science ®Google Scholar
• Sanchez-Criado JE, de Las Mulas JM, Bellido C, Aguilar R, Garrido-Gracia JC. Gonadotrope oestrogen receptor-alpha and -beta and progesterone receptor immunoreactivity after ovariectomy and exposure to oestradiol benzoate, tamoxifen or raloxifene in the rat: correlation with LH secretion. J Endocrinol. 2005;184:59–68.
   PubMed Web of Science ®Google Scholar
• Packard MG, Teather LA. Amygdala modulation of multiple memory systems: hippocampus and caudate-putamen. Neurobio Learn Mem. 1998;69:163–203.
   PubMed Web of Science ®Google Scholar
• Matsuda H. The role of neuroimaging in mild cognitive impairment. Neuropathology. 2007;27:570–7.
   PubMed Web of Science ®Google Scholar
• O'Brien JT. Role of imaging techniques in the diagnosis of dementia. Br J Radiol. 2007;80(2):71–7.
   Google Scholar
• Scheltens P, Korf ES. Contribution of neuroimaging in the diagnosis of Alzheimer's disease and other dementias. Curr Opin Neurol. 2000;13:391–6.
   PubMedGoogle Scholar
• Chetelat G, Fouquet M, Kalpouzos G, Denghien I, De la Sayette V, Viader F, Mezenge F, Landeau B, Baron JC, Eustache F, Desgranges B. Three-dimensional surface mapping of hippocampal atrophy progression from MCI to AD and over normal aging as assessed using voxel-based morphometry. Neuropsychologia. 2008;46:1721–31.
   PubMed Web of Science ®Google Scholar
• Hjornevik T, Leergaard TB, Darine D, Moldestad O, Dale AM, Willoch F, Bjaalie JG. Three-dimensional atlas system for mouse and rat brain imaging data. Front Neuroinform. 2007;1:4–8.
   Google Scholar
• Mishchenko Y. Automation of 3D reconstruction of neural tissue from large volume of conventional serial section transmission electron micrographs. J Neurosci Methods. 2009;176:276–89.
   PubMed Web of Science ®Google Scholar
• Paxinos G, Watson C. The rat brain in stereotaxic coordinates. New York: Academic Press; 2004.
   Google Scholar
• Langston RF, Stevenson CH, Wilson CL, Saunders I, Wood ER. The role of hippocampal subregions in memory for stimulus associations. Behav Brain Res. 2010;215:275–91.
   PubMed Web of Science ®Google Scholar
• Guzowski JF, Knierim JJ, Moser EI. Ensemble dynamics of hippocampal regions CA3 and CA1. Neuron. 2004;44:581–4.
   PubMed Web of Science ®Google Scholar
• Keefe DL. Sex hormones and neural mechanisms. Arch Sex Behav. 2002;31:401–3.
   PubMed Web of Science ®Google Scholar
• Erickson KI, Voss MW, Prakash RS, Chaddock L, Kramer AF, Espeland MA, Tindle HA, Bushnell CA, Jaramillo SA, Kuller LH, Margolis KL, Mysiw WJ, Maldjian JA, Melhem ER, Resnick SM. A cross-sectional study of hormone treatment and hippocampal volume in postmenopausal women: evidence for a limited window of opportunity. Neuropsychology. 2010;24:68–76.
   PubMed Web of Science ®Google Scholar
• Espeland MA, Tindle HA, Bushnell CA, Jaramillo SA, Kuller LH, Margolis KL, Mysiw WJ, Maldjian JA, Melhem ER, Resnick SM. Brain volumes, cognitive impairment, and conjugated equine estrogens. J Gerontol A Biol Sci Med Sci. 2009;64:1243–50.
   PubMed Web of Science ®Google Scholar
• Lord C, Buss C, Lupien SJ, Pruessner JC. Hippocampal volumes are larger in postmenopausal women using estrogen therapy compared to past users, never users and men: a possible window of opportunity effect. Neurobiol Aging. 2008;29: 95–101.
   PubMed Web of Science ®Google Scholar
• Boccardi M, Ghidoni R, Govoni S, Testa C, Benussi L, Bonetti M, Binetti G, Frisoni GB. Effects of hormone therapy on brain morphology of healthy postmenopausal women: a Voxel-based morphometry study. Menopause. 2006;13:584–91.
   PubMed Web of Science ®Google Scholar
• Hu L, Yue Y, Zuo PP, Jin ZY, Feng F, You H, Li ML, Ge QS. Evaluation of neuroprotective effects of long-term low dose hormone replacement therapy on postmenopausal women brain hippocampus using magnetic resonance scanner. Chin Med Sci J. 2006;21:214–8.
   PubMedGoogle Scholar
• Erickson KI, Colcombe SJ, Raz N, Korol DL, Scalf P, Webb A, Cohen NJ, McAuley E, Kramer AF. Selective sparing of brain tissue in postmenopausal women receiving hormone replacement therapy. Neurobiol Aging. 2005;26: 1205–13.
   PubMed Web of Science ®Google Scholar
• Eberling JL, Wu C, Tong-Turnbeaugh R, Jagust WJ. Estrogen- and tamoxifen-associated effects on brain structure and function. Neuroimage 2004;31:364–71.
   Google Scholar
• Low LF, Anstey KJ, Maller J, Kumar R, Wen W, Lux O, Salonikas C, Naidoo D, Sachdev P. Hormone replacement therapy, brain volumes and white matter in postmenopausal women aged 60–64 years. Neuroreport. 2006;17:101–4.
   PubMed Web of Science ®Google Scholar
• Sullivan EV, Marsh L, Pfefferbaum A. Preservation of hippocampal volume throughout adulthood in healthy men and women. Neurobiol Aging. 2005;26:1093–98.
   Web of Science ®Google Scholar
• Raz N, Rodrigue KM, Kennedy KM, Acker JD. Hormone replacement therapy and age-related brain shrinkage: regional effects. Neuroreport. 2004;15:2531–34.
   Web of Science ®Google Scholar
• Bimonte-Nelson HA, Acosta JI, Talboom JS. Neuroscientists as cartographers: mapping the crossroads of gonadal hormones, memory and age using animal models. Molecules. 2010;15:6050–105.
   PubMed Web of Science ®Google Scholar
• Behl C, Widmann M, Trapp T, Holsboer F. 17-beta estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochem Biophys Res Commun. 1995;216: 473–82.
   PubMed Web of Science ®Google Scholar
• Goodman Y, Bruce AJ, Cheng B, Mattson MP. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons. J Neurochem. 1996;66:1836–44.
   PubMed Web of Science ®Google Scholar
• Gandy S, Petanceska S. Regulation of alzheimer beta-amyloid precursor trafficking and metabolism. Adv Exp Med Biol. 2001;487:85–100.
   PubMed Web of Science ®Google Scholar
• Chang D, Kwan J, Timiras PS. Estrogens influence growth, maturation, and amyloid beta-peptide production in neuroblastoma cells and in a beta-APP transfected kidney 293 cell line. Adv Exp Med Biol. 1997;429:261–71.
   PubMed Web of Science ®Google Scholar
• Woolley CS, McEwen BS. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol. 1993;336: 293–306.
   PubMed Web of Science ®Google Scholar
• O'Neal MF, Means LW, Poole MC, Hamm RJ. Estrogen affects performance of ovariectomized rats in a two-choice water-escape working memory task. Psychoneuroendocrinology. 1996;21:51–65.
   PubMed Web of Science ®Google Scholar
• Daniel JM, Lee CD. Estrogen replacement in ovariectomized rats affects strategy selection in the Morris water maze. Neurobiol Learn Mem. 2004;82:142–9.
   PubMed Web of Science ®Google Scholar
• Daniel JM, Roberts SL, Dohanich GP. Effects of ovarian hormones and environment on radial maze and water maze performance of female rats. Physiol Behav. 1999;66:11–20.
   PubMed Web of Science ®Google Scholar
• Gibbs RB. Impairment of basal forebrain cholinergic neurons associated with aging and long-term loss of ovarian function. Exp Neurol. 1998;151:289–302.
   PubMed Web of Science ®Google Scholar
• Gibbs RB. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiol Aging. 2000;21:107-16.
   PubMed Web of Science ®Google Scholar
• Gibbs RB, Aggarwal P. Estrogen and basal forebrain cholinergic neurons: implications for brain aging and Alzheimer's disease-related cognitive decline. Horm Behav. 1998;34:98–111.
   PubMed Web of Science ®Google Scholar
• Talboom JS, Williams BJ, Baxley ER, West SG, Bimonte-Nelson HA. Higher levels of estradiol replacement correlate with better spatial memory in surgically menopausal young and middle-aged rats. Neurobiol Learn Mem. 2008;90:155-63.
   PubMed Web of Science ®Google Scholar
• Markowska AL, Savonenko AV. Effectiveness of estrogen replacement in restoration of cognitive function after long-term estrogen withdrawal in aging rats. J Neurosci. 2002;22:10985–95.
   PubMed Web of Science ®Google Scholar
• Savonenko AV, Markowska AL. The cognitive effects of ovariectomy and estrogen replacement are modulated by aging. Neuroscience. 2003;119:821–30.
   PubMed Web of Science ®Google Scholar
• Squire LR. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev. 1992;99:195–231.
   PubMed Web of Science ®Google Scholar
• Burgess N, Maguire EA, O'Keefe J. The human hippocampus and spatial and episodic memory. Neuron. 2002;35: 625–41.
   PubMed Web of Science ®Google Scholar
• Broadbent NJ, Squire LR, Clark RE. Spatial memory, recognition memory, and the hippocampus. Proc Natl Acad Sci USA. 2004;101:14515–20.
   PubMed Web of Science ®Google Scholar
• Kesner RP. Behavioral functions of the CA3 subregion of the hippocampus. Learn Mem. 2007;14:771–81.
   PubMed Web of Science ®Google Scholar
• Wang S, Ren P, Li X, Guan Y, Zhang YA. 17beta-Estradiol Protects Dopaminergic Neurons in Organotypic Slice of Mesencephalon by MAPK-Mediated Activation of Anti-apoptosis Gene BCL2. J Mol Neurosci MN. 2011;45:236–45.
   PubMed Web of Science ®Google Scholar
• Liu Z, Gastard M, Verina T, Bora S, Mouton PR, Koliatsos VE. Estrogens modulate experimentally induced apoptosis of granule cells in the adult hippocampus. J Comp Neurol. 2001;441:1–8.
   PubMed Web of Science ®Google Scholar