The evolving role of dendritic spines and memory: Interaction(s) with estradiol

Hormones and Behavior

Volumn 74, Issue , 2015, Pages 28-36

  Frankfurt, Maya ^a   Luine, Victoria ^b  

^a DONALD AND BARBARA ZUCKER SCHOOL OF MEDICINE AT HOFSTRA NORTHWELL   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Dendritic spines; Estradiol; Estrogen; Hippocampus; Memory; Prefrontal cortex; Synaptic plasticity

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR;

ARTIFICIAL NEURAL NETWORK; BRAIN CORTEX; BRAIN FUNCTION; BRAIN REGION; DENDRITIC SPINE; DENTATE GYRUS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; LONG TERM DEPRESSION; LONG TERM MEMORY; LONG TERM POTENTIATION; MEDIAL PREFRONTAL CORTEX; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; REVIEW; SHORT TERM MEMORY; SPATIAL MEMORY; STRIATE CORTEX; SYNAPSE; TASK PERFORMANCE; AGING; ANIMAL; COGNITION; DRUG EFFECTS; FEMALE; GENETICS; HUMAN; LONGEVITY; MEMORY; PHYSIOLOGY; PREFRONTAL CORTEX;

AGING; ANIMALS; COGNITION; DENDRITIC SPINES; ESTRADIOL; FEMALE; HIPPOCAMPUS; HUMANS; LONGEVITY; MEMORY; NEURONAL PLASTICITY; PREFRONTAL CORTEX;

EID: 84941745652     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2015.05.004     Document Type: Review

References (110)

1. Babayan A.H., Kramár E.A. Rapid effects of oestrogen on synaptic plasticity: interactions with actin and its signaling proteins. J. Neuroendocrinol. 2013, 11:1163-1172.
2. Beltran-Campos V., Pado-Alcala R.A., Leon-Jacinto U., Aguilar-Vazquez A., Quirarte G.L., Ramirez-Amaya V., Diaz-Cintra S. Increase of mushroom spine density in CA1 apical dendrites produced by water maze training is prevented by ovariectomy. Brain Res. 2011, 1369:119-130.
3. Bosch M., Hayashi Y. Structural plasticity of dendritic spines. Curr. Opin. Neurobiol. 2012, 22:383-388.
4. 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.
5. Bourne J.N., Harris K.M. Balancing structure and function at hippocampal dendritic spines. Annu. Rev. Neurosci. 2008, 31:47-67.
6. Bowman R.E., Luine V., Khandaker H., Villafane J.J., Frankfurt M. Adolescent bisphenol-A exposure decreases dendritic spine density: role of sex and age. Synapse 2014, 68:498-507.
7. Bowman R.E., Luine V., Weinstein S.D., Khandaker H., DeWolf S., Frankfurt M. Bisphenol-A exposure during adolescence leads to enduring alterations in cognition and dendritic spine density in adult male and female rats. Horm. Behav. 2015, 69:89-97.
8. Broadbent N.J., Gaskin S., Squire L.R., Clark R.E. Object recognition memory and the rodent hippocampus. Learn. Mem. 2009, 17:5-11.
9. Calizo L.H., Flanagon-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. Carroll J.C., Pike C.J. Selective estrogen receptor modulators differentially regulate Alzheimer-like changes in female 3xTg-AD mice. Endocrinology 2008, 149:2607-2611.
11. Chen J.R., Yan Y.T., Wang T.J., Chen L.J., Wang Y.J., Tseng G.F. Gonadal hormones modulate the dendritic spine densities of primary cortical pyramidal neurons in adult female rat. Cereb. Cortex 2009, 19:2719-2727.
12. Chen X., Hu J., Jiang L., Xu S., Zheng B., Wang C., Zhang J., Wei X., Chang L., Wang Q. Brilliant Blue G improves cognition in an animal model of Alzheimer's disease and inhibits amyloid-β-induced loss of filopodia and dendrite spines in hippocampal neurons. Neurosci. 2014, 279:94-101.
13. Choi Y., Lee K., Ryu J., Kim H.G., Jeong A.Y., Woo R., Lee J., Hyun J., Hahn S., Kim.K., Kim H. Neuritin attenuates cognitive function impairments in Tg2576 mouse model of Alzheimer's disease. PLoS One 2014, 9(8):e104121. 10.1371/journal.pone.0104121.
14. Churchwell J.C., Kesner R.P. Hippocampal-prefrontal dynamics in spatial working memory: interactions and independent parallel processing. Behav. Brain Res. 2011, 225:389-395.
15. Conrad C.D., McLaughlin K.J., Huynh T.N., El-Ashmawy M., Sparks M. Chronic stress and a cyclic regimen of estradiol administration separately facilitate spatial memory: relationship with hippocampal CA1 spine density and dendritic complexity. Behav. Neurosci. 2012, 126:142-156.
16. Daniel J.M., Roberts S.L., Dohanich G.P. Effects of ovarian hormones and environment on radial maze and water maze performance of female rats. Physiol. Behav. 1999, 66:11-20.
17. de Castilhos J., Forti C.D., Achaval M., Rasia-Filho A.A. Dendritic spine density of posterodorsal medial amygdala neurons can be affected by gonadectomy and sex steroid manipulations in adult rats: a Golgi study. Brain Res. 2008, 1240:73-81.
18. Deller T., Korte M., Chabanis S., Drakew A., Schwegler H., Stefani G.G., Zuniga A., Schwarz K., Bonhoeffer T., Zeller R., Frotscher M., Mundel P. Synaptopodin-deficient mice lack a spine apparatus and show deficits in synaptic plasticity. PNAS 2003, 100:10494-10499.
19. Diaz Weinstein S.1., Villafane J.J., Juliano N., Bowman R.E. Adolescent exposure to Bisphenol-A increases anxiety and sucrose preference but impairs spatial memory in rats independent of sex. Brain Res. 2013, 1529:56-65.
20. Dumitriu D.J., Hao Y., Hara1, J., Kaufmann W., Janssen G.M., Lou W., Rapp P.R., Morrison J.H. Selective changes in thin spine density and morphology in monkey prefrontal cortex correlate with aging-related cognitive impairment. J. Neurosci. 2010, 30:7507-7515.
21. Eilam-Stock T., Serrano P., Frankfurt M., Luine V. Bisphenol-A impairs memory and reduces dendritic spine density in adult male rats. Behav. Neurosci. 2012, 126:175-185.
22. Ennaceur A., Aggleton J.P. Spontaneous recognition of object configurations in rats: effects of fornix lesions. Exp. Brain Res. 1994, 100:85-92.
23. 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.
24. Fortin D.A., Srivastava T., Soderling T.R. Structural modulation of dendritic spines during synaptic plasticity. Neuroscientist 2012, 50:496-501.
25. Fortress A.M., Fan L., Orr P.T., Zhao Z., Frick K.M. Estradiol-induced object recognition memory consolidation is dependent on activation of mTOR signaling in the dorsal hippocampus. Learn. Mem. 2013, 20:147-155.
26. Fortress A.M., Heisler J.D., Frick K.M. The mTOR and canonical Wnt signaling pathways mediate the mnemonic effects of progesterone in the dorsal hippocampus. Hippocampus 2014, 2014, Dec. 8. ([Epub ahead of print]). 10.1002/hipo.22398.
27. Foy M.R., Xu J., Xie X., Brinton R.D., Thompson R.F., Berger T.W. 17beta-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J. Neurophysiol. 1999, 81:925-929.
28. Frankfurt M., Gould E., Woolley C.S., McEwen B.S. Gonadal steroids modify dendritic spine density ventromedial hypothalamic neurons: a Golgi study in the adult rat. Neuroendo. 1990, 51:530-535.
29. Frankfurt M., Salas-Ramirez K., Friedman E., Luine V. Cocaine alters dendritic spine density in cortical and subcortical brain regions of the postpartum and virgin female rat. Synapse 2011, 65:955-961.
30. Frankfurt M., Wang H.Y., Marmolejo N., Bakshi K., Friedman E. Prenatal cocaine increases dendritic spine density in cortical and subcortical brain regions of the rat. Dev. Neurosci. 2009, 31:71-75.
31. Frick K.M. Building a better hormone therapy? How understanding the rapid effects of sex steroid hormones could lead to new therapeutics for age-related memory decline. Behav. Neurosci. 2012, 126:29-53.
32. Frick K.M., Burlingame L.A., Arters J.A., Berger-Sweeney J. Reference memory, anxiety, and estrous cyclicity in C57BL/6NIA mice are affected by age and sex. Neuroscience 2000, 95:293-307.
33. Funahashi S. Space representation in the prefrontal cortex. Prog. Neurobiol. 2013, 103:131-155.
34. García-López P., García-Marín V., Freire M. The discovery of dendritic spines by Cajal in 1888 and its relevance in the present neuroscience. Prog. Neurobiol. 2007, 83:110-130.
35. 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.
36. 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.
37. Hajszan T., Leranth C. Bisphenol A interferes with synaptic remodeling. Front Neuroendocrinol. 2010, 31:519-530.
38. Higley M.J. Localized GABAergic inhibition of dendritic Ca(2+) signalling. Nat. Rev. Neurosci. 2014, 15:567-572.
39. Inagaki T., Gautreaux C., Luine V. Acute estrogen treatment facilitates recognition memory consolidation and alters monoamine levels in memory-related brain areas. Horm. Behav. 2010, 58:415-426.
40. Inagaki T., Frankfurt M., Luine V. Estrogen-induced memory enhancements are blocked by acute bisphenol A in adult female rats: role of dendritic spines. Endocrinology 2012, 53:3357-3367.
41. Jacome L.F., Gautreaux C., Inagaki T., Mohan G., Alves S., Lubbers L.S., Luine V. Estradiol and ERβ agonists enhance recognition memory, and DPN, an ERβ agonist, alters brain monoamines. Neurobiol. Learn. Mem. 2010, 4:488-498.
42. Jedlicka P., Vlachos A., Schwarzacher S.W., Deller T. A role for the spine apparatus in LTP and spatial learning. Behav. Brain Res. 2008, 192:12-19.
43. Kasai H., Fukuda M., Watanabe S., Hayashi-Takagi A., Noguchi J. Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci. 2010, 33:121-129.
44. Kato A., Hojo Y., Higo S., Komatsuzaki Y., Murakami G., Yoshino H., Uebayashi M., Kawato S. Female hippocampal estrogens have a significant correlation with cyclic fluctuation of hippocampal spines. Front. Neural Circ. 2013, 7:149.
45. Kelley A.E. Memory and addiction: shared neural circuitry and molecular mechanisms. Neuron 2004, 44:161-179.
46. Khan M.M., Dhandapani K.M., Zhang Q., Brann D.W. Estrogen regulation of spine density and excitatory synapses in rat prefrontal and somatosensory cerebral cortex. Steroids 2013, 78:614-623.
47. 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.
48. Koffie R.M., Hyman B.T., Spires-Jones T.L. Alzheimer's disease: synapses gone cold. Mol. Neurodegener. 2011, 26:63-72.
49. Koleske A.J. Molecular mechanisms of dendrite stability. Nat. Rev. Neurosci. 2013, 8:536-550.
50. Kramár E.A., Chen L.Y., Brandon N.J., Rex C.S., Liu F., Gall C.M., Lynch G. Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity. J. Neurosci. 2009, 29:12982-12993.
51. Lamprecht R. The actin cytoskeleton in memory formation. Prog. Neurobiol. 2014, 117:1-19.
52. Lan Y.L., Zhao J., Li S. Update on the neuroprotective effect of estrogen receptor alpha against Alzheimer's disease. J. Alzheimers Dis. 2015, 2015(43):1137-1148.
53. Lazcano Z., Solis O., Bringas M.E., Limón D., Diaz A., Espinosa B., García-Peláez I., Flores G., Guevara J. Unilateral injection of Aβ25-35 in the hippocampus reduces the number of dendritic spines in hyperglycemic rats. Synapse 2014, 68:585-594.
54. Lee S.J., Romeo R.D., Svenningsson P., Campomanes C.R., Allen P.B., Greengard P., McEwen B.S. Estradiol affects spinophilin protein differently in gonadectomized males and females. Neuroscience 2004, 127:983-988.
55. Leranth C., Hajszan T., Szigeti-Buck K., Bober J., MacLusky N.J. Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates. PNAS 2008, 105:14187-14191.
56. Leranth C., Shanabrough M., Redmond D.E. Gonadal hormones are responsible for maintaining the integrity of spine synapses in the CA1 hippocampal subfield of female nonhuman primates. J. Comp. Neurol. 2002, 447:34-42.
57. Leuner B., Falduta J., Shors T.A. Associative memory formation increases the observation of dendritic spines in the hippocampus. J. Neurosci. 2003, 23:659-665.
58. Li C., Brake W., Romeo R., Dunlop J., Gordon M., Buzescu R., Magarinos A., Allen P., Greengard P., Luine V., McEwen B.S. Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory tasks in female mice. PNAS 2004, 101:2185-2190.
59. Liao D., Lin H., Law P.Y., Loh H.H. Mu-opioid receptors modulate the stability of dendritic spines. PNAS 2005, 102:1725-1730.
60. Luine V.N. Estradiol and cognition function: past, present and future. Horm. Behav. 2014, 66:602-618.
61. Luine V. Recognition memory tasks in neuroendocrine research. Behavioural Brain Research, SI: object recognition memory in rats and mice edited by Abdel Ennaceur 2015, 285:158-164.
62. Luine V., Frankfurt M. Estrogens facilitate memory processing through membrane mediated mechanisms and spine density changes. Front. Neuroendocrinol. 2012, 33:388-402.
63. Luine V., Frankfurt M. Interactions between estradiol, BDNF and dendritic spines in promoting memory. Neurosci. 2013, 239:34-45.
64. 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.
65. Luine V., Attalla S., Mohan G., Costa A., Frankfurt M. Dietary phytoestrogens enhance spatial memory and spine density in the hippocampus and prefrontal cortex of ovariectomized rats. Brain Res. 2006, 1126:183-187.
66. Luine V.N., Wallace M.E., Frankfurt M. Age-related deficits in spatial memory and hippocampal spines in virgin, female Fischer 344 rats. Curr Gerontol Geriatr Res. 2011, 316386. 10.1155/2011/316386.
67. Macbeth A.H., Luine V.N. Changes in anxiety and cognition due to reproductive experience: a review of data from rodent and human mothers. Neurosci. Biobehav. Rev. 2010, 34:452-467.
68. MacLusky N.J., Luine V.N., Hajszan T., Leranth C. The 17alpha and 17beta isomers of estradiol both induce rapid spine synapse formation in the CA1 hippocampal subfield of ovariectomized female rats. Endocrinology 2005, 146:287-293.
69. Markham J.A., Pych J.C., Juraska J.M. Ovarian hormone replacement to aged ovariectomized female rats benefits acquisition of the morris water maze. Horm. Behav. 2002, 42:284-293.
70. Markowska A.L. Sex dimorphisms in the rate of age-related decline in spatial memory: relevance to alterations in the estrous cycle. J. Neurosci. 1999, 19:8122-8133.
71. Matsuzaki M., Honkura N., Ellis-Davies G.C., Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
72. Matus A., Ackerman M., Pehling G., Byers H.R., Fujiwara K. High actin concentrations in brain dendritic spines and postsynaptic densities. PNAS 1982, 79:7590-7594.
73. Moser M.B., Trommald M., Anderson P. An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. PNAS 1994, 9:12673-12675.
74. Muller D., Toni N., Buchs P.A. Spine changes associated with long-term potentiation. Hippocampus 2000, 10:596-604.
75. Murakami G., Tsurugizawa T., Hatanaka Y., Komatsuzaki Y., Tanabe N., Mukai H., Hojo Y., Kominami S., Yamazaki T., Kimoto T., Kawato S. Comparison between basal and apical dendritic spines in estrogen-induced rapid spinogenesis of CA1 principal neurons in the adult hippocampus. Biochem. Biophys. Res. Commun. 2006, 351:553-558.
76. Nelson B.S., Witty C.F., Williamson E.A., Daniel J.M. A role for hippocampal actin rearrangement in object placement memory in female rats. Neurobiol. Learn. Mem. 2012, 98:284-290.
77. Nimchinsky E.A., Sabatini B.L., Svoboda K. Structure and function of dendritic spines. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2002, 64:313-353.
78. Packard M.G. Posttraining estrogen and memory modulation. Horm. Behav. 1998, 34:126-139.
79. Palop J.J., Mucke L. Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks. Nat. Neurosci. 2010, 7:812-818.
80. Paravalas J.G., Lynch G., Brecha N., Cotman C.W., Globus A. Spine loss and regrowth in hippocampus following deafferentiation. Nature 1974, 248:71-73.
81. Patisol H.B. Phytoestrogen action in the adult and developing brain. J. Neuroendocrinol. 2005, 17:57-64.
82. Penzes P., Rafalovich I. Regulation of the actin cytoskeleton in dendritic spines. Adv. Exp. Med. Biol. 2012, 970:81-95.
83. Pfaff D.W. Autoradiographic localization of radioactivity in the rat brain after injection of tritiated sex hormones. Science 1968, 161:1355-1356.
84. Phan A., Lancaster K.E., Armstrong J.N., MacLusky N.J., Choleris E. Rapid effects of estrogen receptor α and β selective agonists on learning and dendritic spines in female mice. Endo 2011, 152:1492-1502.
85. Prange-Kiel J., Fester L., Zhou L., Lauke H., Carrétero J., Rune G.M. Inhibition of hippocampal estrogen synthesis causes region-specific down regulation of synaptic protein expression in hippocampal neurons. Hippocampus 2006, 16:464-471.
86. Rasia-Filho A.A., Dalpian F., Menezes I.C., Brusco J., Moreira J.E., Cohen R.S. Dendritic spines of the medial amygdala: plasticity, density, shape, and subcellular modulation by sex steroids. Histol. Histopathol. 2012, 27:985-1011.
87. Robinson T.E., Kolb B. Morphine alters the structure of neurons in the nucleus accumbens and neocortex of rats. Synapse 1999, 33:160-162.
88. Robinson T.E., Kolb B. Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 2004, 47(Suppl. 1):33-46.
89. Russo S.J., Dietz D.M., Dumitriu D., Morrison J.H., Malenka R.C., Nestler E.J. The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci. 2010, 33:267-276.
90. Sehgal M., Song C., Ehlers V.L., Moyer J.R. Learning to learn - intrinsic plasticity as a metaplasticity mechanism for memory formation. Neurobiol. Learn. Mem. 2013, 105:186-199.
91. Srivastava D.P., Penzes P. Rapid estradiol modulation of neuronal connectivity and its implications for disease. Front. Endocrinol. (Lausanne) 2011, 2:77. 2011 Nov 22. 10.3389/fendo.2011.00077.
92. Srivastava D.P., Woolfrey K.M., Liu F., Brandon N.J., Penzes P.J. Estrogen receptor β activity modulates synaptic signaling and structure. Neurosci. 2010, 30:13454-13460.
93. Tang Y., Janssen W.G., Hao J., Roberts J.A., McKay H., Lasley B., Allen P.B., Greengard P., Rapp P.R., Kordower J.H., Hof P.R., Morrison J.H. Estrogen replacement increases spinophilin-immunoreactive spine number in the prefrontal cortex of female rhesus monkeys. Cereb. Cortex 2004, 14:215-223.
94. Tuscher J.J., Frankfurt M., Luine V., Frick K. Dorsal hippocampal infusion of 17β-estradiol increases dendritic spine density in the CA1 subfield of the hippocampus in ovariectomized female mice. Program No. 451.13 2014. Neuroscience Meeting Planner 2014, Society for Neuroscience, Washington D.C., (2014. Online).
95. Urbanska M., Swiech L., Jaworski J. Developmental plasticity of the dendritic compartment: focus on the cytoskeleton. Adv. Exp. Med. Biol. 2012, 970:265-284.
96. Valverde F. Apical dendritic spines of the visual cortex and light deprivation in the mouse. Exp. Brain Res. 1967, 3:337-352.
97. Velázquez-Zamora D.A., Garcia-Segura L.M., González-Burgos I. Effects of selective estrogen receptor modulators on allocentric working memory performance and on dendritic spines in medial prefrontal cortex pyramidal neurons of ovariectomized rats. Horm. Behav. 2012, 61:512-517.
98. Vierk R., Glassmeier G., Zhou L., Brandt N., Fester L., Dudzinski D., Wilkars W., Bender R.A., Lewerenz M., Gloger S., Graser L., Schwarz J., Rune G.M. Aromatase inhibition abolishes LTP generation in female but not in male mice. J. Neurosci. 2012, 32:8116-8126.
99. Vierk R., Brandt N., Rune G.M. Hippocampal estradiol synthesis and its significance for hippocampal synaptic stability in male and female animals. Neurosci. 2014, 274:24-32. (Epub 2014 May 15). 10.1016/j.neuroscience.2014.05.003.
100. von Bohlen Und Halbach O. Structure and function of dendritic spines within the hippocampus. Ann. Anat. 2009, 19:518-531.
101. von Bohlen und Halbach O., Zacher C., Gass P., Unsicker K. Age-related alterations in hippocampal spines and deficiencies in spatial memory in mice. J. Neurosci. Res. 2006, 83:525-531.
102. Walf A.A., Rhodes M.E., Frye C.A. Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats. Neurobiol. Learn. Mem. 2006, 1:35-46.
103. Wallace M., Luine V., Arellano A., Frankfurt M. Ovariectomized rats show decreased recognition memory and spine density in hippocampus and prefrontal cortex. Brain Res. 2006, 1126:176-182.
104. Wallace M., Frankfurt M., Arellanos A., Inagaki T., Luine V. Impaired recognition memory and decreased prefrontal cortex spine density in aged female rat. Imaging and the Aging Brain Annals NYAS 2007, 1097:54-57.
105. Woolley C.S., McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 1992, 25:49-54.
106. 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.
107. Yuste R. Dendritic Spines 2010, MIT Press.
108. Yuste R. Dendritic spines and distributed circuits. Neuron 2011, 71:772-781.
109. Zhou L., Fester L., von Blittersdorff B., Hassu B., Nogens H., Prange-Kiel J., Jarry H., Wegscheider K., Rune G.M. Aromatase inhibitors induce spine synapse loss in the hippocampus of ovariectomized mice. Endocrinology 2010, 151:1153-1160.
110. Ziv N.E., S.J., Smith S.S. Evidence for a role in dendritic filopodia in synaptogenesis and spine formation. Neuron 1996, 17:91-102.