Reduced aging defects in estrogen receptive brainstem nuclei in the female hamster

Neurobiology of Aging

Volumn 33, Issue 12, 2012, Pages 2920-2934

  Gerrits, Peter O ^a   Kortekaas, Rudie ^a   Veening, Jan G ^a,b,c   de Weerd, Henk ^a   van der Want, Johannes J L ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Aging; Cardiovascular regulation; Estrus; Lipofuscin; Neuronal degeneration; Neuroprotection; Reproductive behavior

Indexed keywords

ESTROGEN RECEPTOR ALPHA; LIPOFUSCIN;

AGED; AGING; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NUCLEUS; CONTROLLED STUDY; DIESTRUS; ELECTRON MICROSCOPY; ESTRUS; FEMALE; HAMSTER; IMMUNOREACTIVITY; MICROPHOTOGRAPHY; MORPHOMETRICS; NERVE CELL DEGENERATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVE ENDING; NONHUMAN; NUCLEUS PARARETROAMBIGUUS; PRIORITY JOURNAL; SOLITARY TRACT NUCLEUS;

AGE FACTORS; AGING; ANIMALS; BRAIN STEM; CRICETINAE; ESTROGEN RECEPTOR ALPHA; ESTROGENS; ESTROUS CYCLE; FEMALE; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS; SEXUAL BEHAVIOR, ANIMAL; TIME FACTORS;

EID: 84866748342     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.02.018     Document Type: Article

References (115)

1. Adams M.M., Fink S.E., Shah R.A., Janssen W.G., Hayashi S., Milner T.A., McEwen B.S., Morrison J.H. Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J. Neurosci 2002, 22:3608-3614.
2. Adams M.M., Morrison J.H. Estrogen and the aging hippocampal synapse. Cereb. Cortex 2003, 13:1271-1275.
3. Akemi Sato M., Vanderlei Menani J., Ubríaco Lopes O., Colombari E. Lesions of the commissural nucleus of the solitary tract reduce arterial pressure in spontaneously hypertensive rats. Hypertension 2001, 38:560-564.
4. Attah M.Y., Besch E.L. Estrous cycle variations of food and water intake in rats in the heat. J. Appl. Physiol. Respir. Environ. Exerc. Physiol 1977, 42:874-877.
5. Becker J.B., Arnold A.P., Berkley K.J., Blaustein J.D., Eckel L.A., Hampson E., Herman J.P., Marts S., Sadee W., Steiner M., Taylor J., Young E. Strategies and methods for research on sex differences in brain and behavior. Endocrinology 2005, 146:1650-1673.
6. Blaustein J.D., Wade G.N. Ovarian hormones and meal patterns in rats: effects of progesterone and role of gastrointestinal transit. Physiol. Behav 1977, 19:23-27.
7. Boers J., Gerrits P.O., Meijer E., Holstege G. Estrogen receptor-alpha-immunoreactive neurons in the mesencephalon, pons and medulla oblongata of the female golden hamster. Neurosci. Lett 1999, 267:17-20.
8. Brunk U.T., Terman A. Lipofuscin: mechanisms of age-related accumulation and influence on cell function. Free Radic. Biol. Aging 2002, 33:611-619.
9. Calizo L.H., Flanagan-Cato L.M. Hormonal-neural integration in the female rat ventromedial hypothalamus: triple labeling for estrogen receptor-alpha, retrograde tract tracing from the periaqueductal gray, and mating-induced Fos expression. Endocrinology 2003, 144:5430-5440.
10. Chakraborty T.R., Hof P.R., Ng L., Gore A.C. Stereologic analysis of estrogen receptor alpha (ER alpha) expression in rat hypothalamus and its regulation by aging and estrogen. J. Comp. Neurol 2003, 466:409-421.
11. Ciriello J., Schultz C.G., Roder S. Collateral axonal projections from ventrolateral medullary non-catecholaminergic neurons to central nucleus of the amygdala. Brain Res 1994, 663:346-351.
12. Cooper R.L., Linnoila M. Sexual behavior in aged, noncycling female rats. Physiol. Behav 1977, 18:573-576.
13. Csakvari E., Hoyk Z., Gyenes A., Garcia-Ovejero D., Garcia-Segura L.M., Párducz A. Fluctuation of synapse density in the arcuate nucleus during the estrous cycle. Neuroscience 2007, 144:1288-1292.
14. Danielsen J., Buggy J. Depression of ad lib and angiotensin-induced sodium intake at oestrus. Brain Res. Bull 1980, 5:501-504.
15. Farkas E., Jansen A.S., Loewy A.D. Periaqueductal gray matter projection to vagal preganglionic neurons and the nucleus tractus solitarius. Brain Res 1997, 764:257-261.
16. Farkas E., Luiten P.G. Cerebral microvascular pathology in aging and Alzheimer's disease. Prog. Neurobiol 2001, 64:575-611.
17. Findlay A.L., Fitzsimons J.T., Kucharczyk J. Angiotensin-induced drinking fluctuates with the oestrous cycle [proceedings]. J. Physiol 1978, 275:29P-30P.
18. Flanagan-Cato L.M., Calizo L.H., Griffin G.D., Lee B.J., Whisner S.Y. Sexual behaviour induces the expression of activity-regulated cytoskeletal protein and modifies neuronal morphology in the female rat ventromedial hypothalamus. J. Neuroendocrinol 2006, 18:857-864.
19. Frye C.A., Cuevas C.A., Kanarek R.B. Diet and estrous cycle influence pain sensitivity in rats. Pharmacol. Biochem. Behav 1993, 45:255-260.
20. Funabashi T., Kleopoulos S.P., Brooks P.J., Kimura F., Pfaff D.W., Shinohara K., Mobbs C.V. Changes in estrogenic regulation of estrogen receptor alpha mRNA and progesterone receptor mRNA in the female rat hypothalamus during aging: an in situ hybridization study. Neurosci. Res 2000, 38:85-92.
21. Gandy S. Estrogen and neurodegeneration. Neurochem. Res 2003, 28:1003-1008.
22. Gerrits P.O., de Weerd H., van der Want J.J., Kortekaas R., Luiten P.G., Veening J.G. Microvascular changes in estrogen-α sensitive brainstem structures of aging female hamsters. Neurosci. Res 2010, 67:267-274.
23. Gerrits P.O., Holstege G. Pontine and medullary projections to the nucleus retroambiguus: a wheat germ agglutinin-horseradish peroxidase and autoradiographic tracing study in the cat. J. Comp. Neurol 1996, 373:173-185.
24. Gerrits P.O., Holstege G. Descending projections from the nucleus retroambiguus to the iliopsoas motoneuronal cell groups in the female golden hamster: possible role in reproductive behavior. J. Comp. Neurol 1999, 403:219-228.
25. Gerrits P.O., Kortekaas R., Algra A., van der Want J.J.G., Veening J.G. Neurodegeneration and Plasticity in the Brainstem of Estrous Female Golden Hamster; Ultrastructural Studies on Axo-Dendritic Relationships, Remodeling and Degeneration 2009, Society for Neuroscience, Chicago.
26. Gerrits P.O., Kortekaas R., de Weerd H., Veening J.G., van der Want J.J. Regional differences in age-related lipofuscin accumulation in the female hamster brainstem. Neurobiol. Aging 2012 2011, 33:625.e1-625.e9.
27. Gerrits P.O., Kortekaas R., Veening J.G., de Weerd H., Algra A., Mouton L.J., van der Want J.J. Estrous cycle-dependent neural plasticity in the caudal brainstem in the female golden hamster: ultrastructural and immunocytochemical studies of axo-dendritic relationships and dynamic remodeling. Horm. Behav 2008, 54:627-639.
28. Gerrits P.O., Krukerink M., Veening J.G. Columnar organization of estrogen receptor-alpha immunoreactive neurons in the periaqueductal gray projecting to the nucleus para-retroambiguus in the caudal brainstem of the female golden hamster. Neuroscience 2009, 161:459-474.
29. Gerrits P.O., Mouton L.J., de Weerd H., Georgiadis J.R., Krukerink M., Holstege G. Ultrastructural evidence for a direct excitatory pathway from the nucleus retroambiguus to lateral longissimus and quadratus lumborum motoneurons in the female golden hamster. J. Comp. Neurol 2004, 480:352-363.
30. Gerrits P.O., Smid L. A new, less toxic polymerization system for the embedding of soft tissues in glycol methacrylate and subsequent preparing of serial sections. J. Microsc 1983, 132:81-85.
31. Gerrits P.O., Veening J.G., Blomsma S.A., Mouton L.J. The nucleus para-retroambiguus: a new group of estrogen receptive cells in the caudal ventrolateral medulla of the female golden hamster. Horm. Behav 2008, 53:329-341.
32. Gerrits P.O., Vodde C., Holstege G. Retroambiguus projections to the cutaneous trunci motoneurons may form a pathway in the central control of mating. J. Neurophysiol 2000, 83:3076-3083.
33. Goldman R.K., Azar A.S., Mulvaney J.M., Hinojosa-Laborde C., Haywood J.R., Brooks V.L. Baroreflex sensitivity varies during the rat estrous cycle: role of gonadal steroids. Am. J. Physiol 2009, 296:R1419-R1426.
34. Gould E., Woolley C.S., Frankfurt M., McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci 1990, 10:1286-1291.
35. Guevara-Guzmán R., Buzo E., Larrazolo A., de la Riva C., Da Costa A.P., Kendrick K.M. Vaginocervical stimulation-induced release of classical neurotransmitters and nitric oxide in the nucleus of the solitary tract varies as a function of the oestrus cycle. Brain Res 2001, 898:303-313.
36. Hardy S.G., Horecky J.G., Presley K.G. Projections of the caudal ventrolateral medulla to the thoracic spinal cord in the rat. Anat. Rec 1998, 250:95-102.
37. Haywood S.A., Simonian S.X., van der Beek E.M., Bicknell R.J., Herbison A.E. Fluctuating estrogen and progesterone receptor expression in brainstem norepinephrine neurons through the rat estrous cycle. Endocrinology 1999, 140:3255-3263.
38. Henderson L.A., Keay K.A., Bandler R. The ventrolateral periaqueductal gray projects to caudal brainstem depressor regions: a functional-anatomical and physiological study. Neuroscience 1998, 82:201-221.
39. Herbert H., Moga M.M., Saper C.B. Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J. Comp. Neurol 1990, 293:540-580.
40. Huang H.H., Meites J. Reproductive capacity of aging female rats. Neuroendocrinology 1975, 17:289-295.
41. Huang Z.G., Subramanian S.H., Balnave R.J., Turman A.B., Moi Chow C. Roles of periaqueductal gray and nucleus tractus solitarius in cardiorespiratory function in the rat brainstem. Respir. Physiol 2000, 120:185-195.
42. Hubscher C.H., Berkley K.J. Responses of neurons in caudal solitary nucleus of female rats to stimulation of vagina, cervix, uterine horn and colon. Brain Res 1994, 664:1-8.
43. Hung A.J., Stanbury M.G., Shanabrough M., Horvath T.L., Garcia-Segura L.M., Naftolin F. Estrogen, synaptic plasticity and hypothalamic reproductive aging. Exp. Gerontol 2003, 38:53-59.
44. Inestrosa N.C., Marzolo M.P., Bonnefont A.B. Cellular and molecular basis of estrogen's neuroprotection. Potential relevance for Alzheimer's disease. Mol. Neurobiol 1998, 17:73-86.
45. Jennings W.A. Estrous cycle and temporal pattern of feeding in female rats. Psychol. Rep 1974, 34:87-98.
46. Kamino K., Tillmann T., Mohr U. Spectrum and age-related incidence of spontaneous tumours in a colony of Han:AURA hamsters. Exp. Toxicol. Pathol 2001, 52:539-544.
47. Korte S.M., Jaarsma D., Luiten P.G., Bohus B. Mesencephalic cuneiform nucleus and its ascending and descending projections serve stress-related cardiovascular responses in the rat. J. Auton. Nerv. Syst 1992, 41:157-176.
48. Laflamme N., Nappi R.E., Drolet G., Labrie C., Rivest S. Expression and neuropeptidergic characterization of estrogen receptors (ERalpha and ERbeta) throughout the rat brain: anatomical evidence of distinct roles of each subtype. J. Neurobiol 1998, 36:357-378.
49. Langub M.C., Maley B.E., Watson R.E. Estrous cycle-associated axosomatic synaptic plasticity upon estrogen receptive neurons in the rat preoptic area. Brain Res 1994, 641:303-310.
50. LeFevre J., McClintock M.K. Isolation accelerates reproductive senescence and alters its predictors in female rats. Horm. Behav 1991, 25:258-272.
51. Li C., Brake W.G., Romeo R.D., Dunlop J.C., Gordon M., Buzescu R., Magarinos A.M., Allen P.B., Greengard P., Luine V., McEwen B.S. Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:2185-2190.
52. Lisk R.D. The estrous cycle. The Hamster: Reproduction and Behavior 1985, 23-52. Plenum Press, New York. H.I. Siegel (Ed.).
53. Liu M., Kelley M.H., Herson P.S., Hurn P.D. Neuroprotection of sex steroids. Minerva Endocrinol 2009, 35:127-143.
54. McCormick C.M., Smith C., Mathews I.Z. Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav. Brain Res 2008, 187:228-238.
55. McEwen B. Estrogen actions throughout the brain. Recent Prog. Horm. Res 2002, 57:357-384.
56. McEwen B., Akama K., Alves S., Brake W.G., Bulloch K., Lee S., Li C., Yuen G., Milner T.A. Tracking the estrogen receptor in neurons: implications for estrogen-induced synapse formation. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:7093-7100.
57. McEwen B.S., Gould E., Orchinik M., Weiland N.G., Woolley C.S. Oestrogens and the structural and functional plasticity of neurons: implications for memory, ageing and neurodegenerative processes. Ciba Found. Symp 1995, 191:52-66.
58. McEwen B.S., Woolley C.S. Estradiol and progesterone regulate neuronal structure and synaptic connectivity in adult as well as developing brain. Exp. Gerontol 1994, 29:431-436.
59. McKellar S., Loewy A.D. Efferent projections of the A1 catecholamine cell group in the rat: an autoradiographic study. Brain Res 1982, 241:11-29.
60. Milner T.A., Drake C.T., Lessard A., Waters E.M., Torres-Reveron A., Graustein B., Mitterling K., Frys K., Iadecola C. Angiotensin II-induced hypertension differentially affects estrogen and progestin receptors in central autonomic regulatory areas of female rats. Exp. Neurol 2008, 212:393-406.
61. Milner T.A., Lubbers L.S., Alves S.E., McEwen B.S. Nuclear and extranuclear estrogen binding sites in the rat forebrain and autonomic medullary areas. Endocrinology 2008, 149:3306-3312.
62. Mitterling K.L., Spencer J.L., Dziedzic N., Shenoy S., McCarthy K., Waters E.M., McEwen B.S., Milner T.A. Cellular and subcellular localization of estrogen and progestin receptor immunoreactivities in the mouse hippocampus. J. Comp. Neurol 2010, 518:2729-2743.
63. Mora S., Dussaubat N., Díaz-Véliz G. Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 1996, 21:609-620.
64. Murphy D.D., Segal M. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J. Neurosci 1996, 16:4059-4068.
65. Nakamura N.H., Rosell D.R., Akama K.T., McEwen B.S. Estrogen and ovariectomy regulate mRNA and protein of glutamic acid decarboxylases and cation-chloride cotransporters in the adult rat hippocampus. Neuroendocrinology 2004, 80:308-323.
66. Navarro A., Gonzalez del Rey C., Tolivia J., Alvarez-Uria M. Ultrastructural and quantitative study of atypical age-related bodies in the hamster brain. Mech. Ageing Dev 1996, 90:75-90.
67. Okamura H., Yokosuka M., Hayashi S. Induction of substance P-immunoreactivity by estrogen in neurons containing estrogen receptors in the anterovental periventricular nucleus of female but not male rats. J. Neuroendocrinol 1994, 6:609-615.
68. Oklejewicz M., Daan S. Enhanced longevity in tau mutant Syrian hamsters, Mesocricetus auratus. J. Biol. Rhythms 2002, 17:210-216.
69. Orsini M.W. The external vaginal phenomena characterizing the stages of the estrous cycle, pregnancy, pseudopregnancy, lactation and the anestrous hamster Mesocricetus auratus Waterhouse. Proceedings of the Anim Care Panel 1961, 11:193-206.
70. Osterlund M., Kuiper G.G., Gustafsson J.A., Hurd Y.L. Differential distribution and regulation of estrogen receptor-alpha and -beta mRNA within the female rat brain. Brain Res. Mol. Brain Res 1998, 54:175-180.
71. Peters A., Palay S.L. The morphology of synapses. J. Neurocytol 1996, 25:687-700.
72. Pfaff D.W. Patterns of steroid hormone effects on electrical and molecular events in hypothalamic neurons. Mol. Neurobiol 1989, 3:135-154.
73. Pour P., Kmoch N., Greiser E., Mohr U., Althoff J., Cardesa A. Spontaneous tumors and common diseases in two colonies of Syrian hamsters. I. Incidence and sites. J. Natl. Cancer Inst 1976, 56:931-935.
74. Redman H.C., Hobbs C.H., Rebar A.H. Survival distribution of Syrian hamsters (Mesocricetus auratus, Sch: SYR) used during 1972-1977. Prog. Exp. Tumor Res 1979, 24:108-117.
75. Roder S., Ciriello J. Caudal ventrolateral medullary projections to the nucleus of the solitary tract in the cat. Neurosci. Lett 1992, 134:161-164.
76. Ryan S.M., Maier S.F. The estrous cycle and estrogen modulate stress-induced analgesia. Behav. Neurosci 1988, 102:371-380.
77. Saleh T.M., Connell B.J. Role of 17 beta-estradiol in the modulation of baroreflex sensitivity in male rats. Am. J. Physiol 1998, 275:R770-R778.
78. Saleh T.M., Connell B.J. Centrally mediated effect of 17 beta-estradiol on parasympathetic tone in male rats. Am. J. Physiol 1999, 276:R474-R481.
79. Saleh T.M., Connell B.J. 17beta-estradiol modulates baroreflex sensitivity and autonomic tone of female rats. J. Auton. Nerv. Syst 2000, 80:148-161.
80. Saleh T.M., Connell B.J. Central nuclei mediating estrogen-induced changes in autonomic tone and baroreceptor reflex in male rats. Brain Res 2003, 961:190-200.
81. Saleh T.M., Connell B.J. Central nuclei mediating estrogen-induced changes in autonomic tone and baroreceptor reflex in male rats. Brain Res 2003, 961:190-200.
82. Saleh T.M., Connell B.J. Role of oestrogen in the central regulation of autonomic function. Clin. Exp. Pharmacol. Physiol 2007, 34:827-832.
83. Saleh T.M., Connell B.J., Cribb A.E. Sympathoexcitatory effects of estrogen in the insular cortex are mediated by GABA. Brain Res 2005, 1037:114-122.
84. Saleh T.M., Connell B.J., McQuaid T., Cribb A.E. Estrogen-induced neurochemical and electrophysiological changes in the parabrachial nucleus of the male rat. Brain Res 2003, 990:58-65.
85. Saleh M.C., Connell B.J., Saleh T.M. Autonomic and cardiovascular reflex responses to central estrogen injection in ovariectomized female rats. Brain Res 2000, 879:105-114.
86. Saleh T.M., Connell B.J., Saleh M.C. Acute injection of 17 beta-estradiol enhances cardiovascular reflexes and autonomic tone in ovariectomized female rats. Auton. Neurosci. Basic Clin 2000, 84:78-88.
87. Saleh T.M., Cribb A.E., Connell B.J. Estrogen-induced recovery of autonomic function after middle cerebral artery occlusion in male rats. Am. J. Physiol 2001, 281:R1531-R1539.
88. Sato M.A., Colombari E., Morrison S.F. Inhibition of neurons in commissural nucleus of solitary tract reduces sympathetic nerve activity in SHR. Am J Physiol Heart Circ Physiol 2002, 282:H1679-H1684.
89. Sato M.A., Schoorlemmer G.H., Menani J.V., Lopes O.U., Colombari E. Recovery of high blood pressure after chronic lesions of the commissural NTS in SHR. Hypertension 2003, 42:713-718.
90. Sawchenko P.E. Central connections of the sensory and motor nuclei of the vagus nerve. J. Auton. Nerv. Syst 1983, 9:13-26.
91. Schwaber J.S., Kapp B.S., Higgins G.A., Rapp P.R. Amygdaloid and basal forebrain direct connections with the nucleus of the solitary tract and the dorsal motor nucleus. J. Neurosci 1982, 2:1424-1438.
92. Seyedabadi M., Li Q., Padley J.R., Pilowsky P.M., Goodchild A.K. A novel pressor area at the medullo-cervical junction that is not dependent on the RVLM: efferent pathways and chemical mediators. J. Neurosci 2006, 26:5420-5427.
93. Sher S.P. Tumors in control hamsters, rats, and mice: literature tabulation. Crit. Rev. Toxicol 1982, 10:49-79.
94. Shughrue P.J., Lane M.V., Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol 1997, 388:507-525.
95. Soya H., Nakamura T., Deocaris C.C., Kimpara A., Iimura M., Fujikawa T., Chang H., McEwen B.S., Nishijima T. BDNF induction with mild exercise in the rat hippocampus. Biochem. Biophys. Res. Commun 2007, 358:961-967.
96. Spary E.J., Maqbool A., Batten T.F. Changes in Oestrogen Receptor alpha Expression in the Nucleus of the Solitary Tract of the Rat Over the Oestrous Cycle and Following Ovariectomy. J. Neuroendocrinol 2010, 22:492-502.
97. Spencer J.L., Waters E.M., Milner T.A., Lee F.S., McEwen B.S. BDNF variant Val66Met interacts with estrous cycle in the control of hippocampal function. Proc. Natl. Acad. Sci. U. S. A. 2009, 107:4395-4400.
98. Spencer-Segal J.L., Waters E.M., Bath K.G., Chao M.V., McEwen B.S., Milner T.A. Distribution of phosphorylated TrkB receptor in the mouse hippocampal formation depends on sex and estrous cycle stage. J. Neurosci 2011, 31:6780-6790.
99. Tanaka T., Nishikawa A., Shima H., Sugie S., Shinoda T., Yoshimi N., Iwata H., Mori H. Inhibitory effects of chlorogenic acid, reserpine, polyprenoic acid (E-5166), or coffee on hepatocarcinogenesis in rats and hamsters. Basic Life Sci 1990, 52:429-440.
100. Toran-Allerand C.D. Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro: implications for sexual differentiation. Brain Res 1976, 106:407-412.
101. Turcotte J.C., Blaustein J.D. Projections of the estrogen receptor-immunoreactive ventrolateral hypothalamus to other estrogen receptor-immunoreactive sites in female guinea pig brain. Neuroendocrinology 1999, 69:63-76.
102. VanderHorst V.G., Holstege G. Estrogen induces axonal outgrowth in the nucleus retroambiguus-lumbosacral motoneuronal pathway in the adult female cat. J. Neurosci 1997, 17:1122-1136.
103. Veening J.G., De Weerd H., Van der Want J.J.L., Luiten P.G.M., Gerrits P.O. Microvascular Changes in the Brainstem of Aging Female Hamsters 2009, Society for Neuroscience, Chicago.
104. Veening J.G., Swanson L.W., Sawchenko P.E. The organization of projections from the central nucleus of the amygdala to brainstem sites involved in central autonomic regulation: a combined retrograde transport-immunohistochemical study. Brain Res 1984, 303:337-357.
105. Waters E.M., Mitterling K., Spencer J.L., Mazid S., McEwen B.S., Milner T.A. Estrogen receptor alpha and beta specific agonists regulate expression of synaptic proteins in rat hippocampus. Brain Res 2009, 1290:1-11.
106. Waters E.M., Yildirim M., Janssen W.G., Lou W.Y., McEwen B.S., Morrison J.H., Milner T.A. Estrogen and aging affect the synaptic distribution of estrogen receptor beta-immunoreactivity in the CA1 region of female rat hippocampus. Brain Res 2011, 1379:86-97.
107. Williams T.J., Akama K.T., Knudsen M.G., McEwen B.S., Milner T.A. Ovarian hormones influence corticotropin releasing factor receptor colocalization with delta opioid receptors in CA1 pyramidal cell dendrites. Exp. Neurol 2011, 230:186-196.
108. Woolley C.S. Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Horm. Behav 1998, 34:140-148.
109. Woolley C.S., Gould E., Frankfurt M., McEwen B.S. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J. Neurosci 1990, 10:4035-4039.
110. Woolley C.S., McEwen B.S. Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J. Neurosci 1994, 14:7680-7687.
111. Woolley C.S., Weiland N.G., McEwen B.S., Schwartzkroin P.A. Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J. Neurosci 1997, 17:1848-1859.
112. Yildirim M., Janssen W.G., Lou W.Y., Akama K.T., McEwen B.S., Milner T.A., Morrison J.H. Effects of estrogen and aging on the synaptic distribution of phosphorylated Akt-immunoreactivity in the CA1 region of the female rat hippocampus. Brain Res 2011, 1379:98-108.
113. Yildirim M., Janssen W.G., Tabori N.E., Adams M.M., Yuen G.S., Akama K.T., McEwen B.S., Milner T.A., Morrison J.H. Estrogen and aging affect synaptic distribution of phosphorylated LIM kinase (pLIMK) in CA1 region of female rat hippocampus. Neuroscience 2008, 152:360-370.
114. Yildirim M., Mapp O.M., Janssen W.G., Yin W., Morrison J.H., Gore A.C. Postpubertal decrease in hippocampal dendritic spines of female rats. Exp. Neurol 2008, 210:339-348.
115. Yuri K., Kawata M. Estrogen affects calcitonin gene-related peptide- and methionine-enkephalin-immunoreactive neuron in the female rat preoptic area. Neurosci. Lett 1994, 169:5-8.