Long-Term Oestradiol Treatment Enhances Hippocampal Synaptic Plasticity that is Dependent on Muscarinic Acetylcholine Receptors in Ovariectomised Female Rats

Journal of Neuroendocrinology

Volumn 24, Issue 6, 2012, Pages 887-896

  Stelly, C E ^a,c   Cronin, J ^a,b   Daniel, J M ^a,b   Schrader, L A ^a,b  

^a TULANE UNIVERSITY   (United States)

^b Tulane University   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Estrogen; LTP; MAChRs; NMDAR; Ovariectomy; Scopolamine

Indexed keywords

CHOLESTEROL; ESTRADIOL; MUSCARINIC RECEPTOR; SCOPOLAMINE BROMIDE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; LONG TERM CARE; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

ANIMALS; ESTRADIOL; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; HIPPOCAMPUS; LONG-TERM POTENTIATION; NEURONAL PLASTICITY; OVARIECTOMY; RATS; RATS, LONG-EVANS; RECEPTORS, MUSCARINIC; SCOPOLAMINE HYDROBROMIDE; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 84860906139     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2012.02287.x     Document Type: Article

References (106)

1. Daniel JM. Effects of oestrogen on cognition: what have we learned from basic research? J Neuroendocrinol 2006; 18: 787-795.
2. Rudick CN, Woolley CS. Estrogen regulates functional inhibition of hippocampal CA1 pyramidal cells in the adult female rat. J Neurosci 2001; 21: 6532-6543.
3. Woolley CS, McEwen BS. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 1992; 12: 2549-2554.
4. Woolley CS, Gould E, Frankfurt M, McEwen BS. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 1990; 10: 4035-4039.
5. Woolley CS, Wenzel HJ, Schwartzkroin PA. Estradiol increases the frequency of multiple synapse boutons in the hippocampal CA1 region of the adult female rat. J Comp Neurol 1996; 373: 108-117.
6. Woolley CS, McEwen BS. Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J Neurosci 1994; 14: 7680-7687.
7. 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.
8. Segal M, Murphy D. Estradiol induces formation of dendritic spines in hippocampal neurons: functional correlates. Horm Behav 2001; 40: 156-159.
9. MacLusky NJ, Luine VN, 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.
10. Leranth C, Shanabrough M, Horvath TL. Hormonal regulation of hippocampal spine synapse density involves subcortical mediation. Neuroscience 2000; 101: 349-356.
11. Malenka RC, Bear MF. LTP and LTD: an emmbarrassment of riches. Neuron 2004; 44: 5-21.
12. Toni N, Buchs PA, Nikonenko I, Povilaitite P, Parisi L, Muller D. Remodeling of synaptic membranes after induction of long-term potentiation. J Neurosci 2001; 21: 6245-6251.
13. Toni N, Buchs PA, Nikonenko I, Bron CR, Muller D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 1999; 402: 421-425.
14. Desmond NL, Levy WB. Changes in the numerical density of synaptic contacts with long-term potentiation in the hippocampal dentate gyrus. J Comp Neurol 1986; 253: 466-475.
15. Chang FL, Greenough WT. Transient and enduring morphological correlates of synaptic activity and efficacy change in the rat hippocampal slice. Brain Res 1984; 309: 35-46.
16. Warren SG, Humphreys AG, Juraska JM, Greenough WT. LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats. Brain Res 1995; 703: 26-30.
17. Bi R, Foy MR, Vouimba RM, Thompson RF, Baudry M. Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proc Natl Acad Sci USA 2001; 98: 13391-13395.
18. Cordoba Montoya DA, Carrer HF. Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats. Brain Res 1997; 778: 430-438.
19. Wong M, Moss RL. Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. J Neurosci 1992; 12: 3217-3225.
20. Teyler TJ, Vardaris RM, Lewis D, Rawitch AB. Gonadal steroids: effects on excitability of hippocampal pyramidal cells. Science 1980; 209: 1017-1018.
21. Sharrow KM, Kumar A, Foster TC. Calcineurin as a potential contributor in estradiol regulation of hippocampal synaptic function. Neuroscience 2002; 113: 89-97.
22. Foy MR, Teyler TJ. 17-Alpha-estradiol and 17-beta-estradiol in hippocampus. Brain Res Bull 1983; 10: 735-739.
23. Kramar EA, Chen LY, Brandon NJ, Rex CS, Liu F, Gall CM, Lynch G. Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity. J Neurosci 2009; 29: 12982-12993.
24. Kim JS, Kim HY, Kim JH, Shin HK, Lee SH, Lee YS, Son H. Enhancement of rat hippocampal long-term potentiation by 17 beta-estradiol involves mitogen-activated protein kinase-dependent and -independent components. Neurosci Lett 2002; 33: 65-69.
25. Foy MR, Xu J, Xie X, Brinton RD, Thompson RF, Berger TW. 17beta-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J Neurophysiol 1999; 81: 925-929.
26. Foy MR, Baudry M, Diaz Brinton R, Thompson RF. Estrogen and hippocampal plasticity in rodent models. J Alzheimers Dis 2008; 15: 589-603.
27. Smejkalova T, Woolley CS. Estradiol acutely potentiates hippocampal excitatory synaptic transmission through a presynaptic mechanism. J Neurosci 2010; 30: 16137-16148.
28. Smith CC, McMahon LL. Estrogen-induced increase in the magnitude of long-term potentiation occurs only when the ratio of NMDA transmission to AMPA transmission is increased. J Neurosci 2005; 25: 7780-7791.
29. Smith CC, McMahon LL. Estradiol-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors. J Neurosci 2006; 26: 8517-8522.
30. Cyr M, Ghribi O, Thibault C, Morissette M, Landry M, Di Paolo T. Ovarian steroids and selective estrogen receptor modulators activity on rat brain NMDA and AMPA receptors. Brain Res Brain Res Rev 2001; 37: 153-161.
31. Daniel JM, Dohanich GP. Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J Neurosci 2001; 21: 6949-6956.
32. McKinney M, Coyle JT, Hedreen JC. Topographic analysis of the innervation of the rat neocortex and hippocampus by the basal forebrain cholinergic system. J Comp Neurol 1983; 217: 103-121.
33. Rye DB, Wainer BH, Mesulam MM, Mufson EJ, Saper CB. Cortical projections arising from the basal forebrain: a study of cholinergic and noncholinergic components employing combined retrograde tracing and immunohistochemical localization of choline acetyltransferase. Neuroscience 1984; 13: 627-643.
34. Selcher JC, Weeber EJ, Christian J, Nekrasova T, Landreth GE, Sweatt JD. A role for ERK MAP kinase in physiologic temporal integration in hippocampal area CA1. Learn Mem 2003; 10: 26-39.
35. Mitsushima D, Takase K, Funabashi T, Kimura F. Gonadal steroids maintain 24h acetylcholine release in the hippocampus: organizational and activational effects in behaving rats. J Neurosci 2009; 29: 3808-3815.
36. Gibbs RB, Pfaff DW. Effects of estrogen and fimbria/fornix transection on p75NGFR and ChAT expression in the medial septum and diagonal band of Broca. Exp Neurol 1992; 116: 23-39.
37. Gibbs RB, Wu D, Hersh LB, Pfaff DW. Effects of estrogen replacement on the relative levels of choline acetyltransferase, trkA, and nerve growth factor messenger RNAs in the basal forebrain and hippocampal formation of adult rats. Exp Neurol 1994; 129: 70-80.
38. Luine VN. Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats. Exp Neurol 1985; 89: 484-490.
39. Rodgers SP, Bohacek J, Daniel JM. Transient estradiol exposure during middle age in ovariectomized rats exerts lasting effects on cognitive function and the hippocampus. Endocrinology 2010; 151: 1194-1203.
40. Singh M, Meyer EM, Millard WJ, Simpkins JW. Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats. Brain Res 1994; 644: 305-312.
41. Gibbs RB. Effects of gonadal hormone replacement on measures of basal forebrain cholinergic function. Neuroscience 2000; 101: 931-938.
42. Towart LA, Alves SE, Znamensky V, Hayashi S, McEwen BS, Milner TA. Subcellular relationships between cholinergic terminals and estrogen receptor-alpha in the dorsal hippocampus. J Comp Neurol 2003; 463: 390-401.
43. Sherwin BB. Estrogen and cognitive functioning in women. Endocr Rev 2003; 24: 133-151.
44. Zucker RS. Short-term synaptic plasticity. Annu Rev Neurosci 1989; 12: 13-31.
45. Katz B, Miledi R. The role of calcium in neuromuscular facilitation. J Physiol 1968; 195: 481-492.
46. 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: 10985-10995.
47. Markham JA, Pych JC, Juraska JM. Ovarian hormone replacement to aged ovariectomized female rats benefits acquisition of the morris water maze. Horm Behav 2002; 42: 284-293.
48. Gibbs RB. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiol Aging 2000; 21: 107-116.
49. Frick KM, Fernandez SM. Enrichment enhances spatial memory and increases synaptophysin levels in aged female mice. Neurobiol Aging 2003; 24: 615-626.
50. Foster TC, Sharrow KM, Kumar A, Masse J. Interaction of age and chronic estradiol replacement on memory and markers of brain aging. Neurobiol Aging 2003; 24: 839-852.
51. Vaucher E, Reymond I, Najaffe R, Kar S, Quirion R, Miller MM, Franklin KB. Estrogen effects on object memory and cholinergic receptors in young and old female mice. Neurobiol Aging 2002; 23: 87-95.
52. Frick KM, Fernandez SM, Bulinski SC. Estrogen replacement improves spatial reference memory and increases hippocampal synaptophysin in aged female mice. Neuroscience 2002; 115: 547-558.
53. Muller D, Toni N, Buchs PA. Spine changes associated with long-term potentiation. Hippocampus 2000; 10: 596-604.
54. McLaughlin KJBimonte-Nelson H, Neisewander JL, Conrad CD. Assessment of estradiol influence on spatial tasks and hippocampal CA1 spines: evidence that the duration of hormone deprivation after ovariectomy compromises 17beta-estradiol effectiveness in altering CA1 spines. Horm Behav 2008; 54: 386-395.
55. Luine VN, Jacome LF, Maclusky NJ. Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 2003; 144: 2836-2844.
56. Fernandez SM, Lewis MC, Pechenino AS, Harburger LL, Orr PT, Gresack JE, Schafe GE, Frick KM. Estradiol-induced enhancement of object memory consolidation involves hippocampal extracellular signal-regulated kinase activation and membrane-bound estrogen receptors. J Neurosci 2008; 28: 8660-8667.
57. Beltran-Campos V, Prado-Alcala RA, Leon-Jacinto U, Aguilar-Vazquez A, Quirarte GL, Ramirez-Amaya V, Díaz-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.
58. 2+ channels. J Neurosci 1998; 18: 3171-3179.
59. Norris CM, Halpain S, Foster TC. Alterations in the balance of protein kinase/phosphatase activities parallel reduced synaptic strength during aging. J Neurophysiol 1998; 80: 1567-1570.
60. Foy MR, Baudry M, Foy JG, Thompson RF. 17beta-estradiol modifies stress-induced and age-related changes in hippocampal synaptic plasticity. Behav Neurosci 2008; 122: 301-309.
61. Foster TC, Kumar A. Susceptibility to induction of long-term depression is associated with impaired memory in aged Fischer 344 rats. Neurobiol Learn Mem 2007; 87: 522-535.
62. Vouimba RM, Foy MR, Foy JG, Thompson RF. 17beta-estradiol suppresses expression of long-term depression in aged rats. Brain Res Bull 2000; 53: 783-787.
63. Yoshii A, Constantine-Paton M. BDNF induces transport of PSD-95 to dendrites through PI3K-AKT signaling after NMDA receptor activation. Nat Neurosci 2007; 10: 702-711.
64. Cowansage KK, LeDoux JE, Monfils MH. Brain-derived neurotrophic factor: a dynamic gatekeeper of neural plasticity. Curr Mol Pharmacol 2010; 3: 12-29.
65. Scharfman HE, Mercurio TC, Goodman JH, Wilson MA, MacLusky NJ. Hippocampal excitability increases during the estrous cycle in the rat: a potential role for brain-derived neurotrophic factor. J Neurosci 2003; 23: 11641-11652.
66. Singh M, Meyer EM, Simpkins JW. The effect of ovariectomy and estradiol replacement on brain-derived neurotrophic factor messenger ribonucleic acid expression in cortical and hippocampal brain regions of female Sprague-Dawley rats. Endocrinology 1995; 136: 2320-2324.
67. Gibbs RB. Levels of trkA and BDNF mRNA, but not NGF mRNA, fluctuate across the estrous cycle and increase in response to acute hormone replacement. Brain Res 1998; 810: 294.
68. Murphy DD, Cole NB, Segal M. Brain-derived neurotrophic factor mediates estradiol-induced dendritic spine formation in hippocampal neurons. Proc Natl Acad Sci USA 1998; 95: 11412-11417.
69. Scharfman HE, Maclusky NJ. Similarities between actions of estrogen and BDNF in the hippocampus: coincidence or clue? Trends Neurosci 2005; 28: 79-85.
70. Kobayashi M, Ohno M, Shibata S, Yamamoto T, Watanabe S. Concurrent blockade of beta-adrenergic and muscarinic receptors suppresses synergistically long-term potentiation of population spikes in the rat hippocampal CA1 region. Brain Res 1997; 777: 242-246.
71. Hirotsu I, Hori N, Katsuda N, Ishihara T. Effect of anticholinergic drug on long-term potentiation in rat hippocampal slices. Brain Res 1989; 482: 194-197.
72. Yamasaki M, Matsui M, Watanabe M. Preferential localization of muscarinic M1 receptor on dendritic shaft and spine of cortical pyramidal cells and its anatomical evidence for volume transmission. J Neurosci 2010; 30: 4408-4418.
73. Giessel AJ, Sabatini BL. M1 muscarinic receptors boost synaptic potentials and calcium influx in dendritic spines by inhibiting postsynaptic SK channels. Neuron 2010; 68: 936-947.
74. Buchanan KA, Petrovic MM, Chamberlain SE, Marrion NV, Mellor JR. Facilitation of long-term potentiation by muscarinic M(1) receptors is mediated by inhibition of SK channels. Neuron 2010; 68: 948-963.
75. + channels modulate synaptic plasticity and memory encoding. J Neurosci 2002; 22: 10163-10171.
76. 2+-mediated feedback loop in dendritic spines. Nat Neurosci 2005; 8: 642-649.
77. +) channel subunits, SK1, SK2, and SK3, in the adult rat central nervous system. Mol Cell Neurosci 2000; 15: 476-493.
78. + current in hippocampal pyramidal neurons. Proc Natl Acad Sci USA 1999; 96: 4662-4667.
79. Kumar A, Foster TC. 17beta-estradiol benzoate decreases the AHP amplitude in CA1 pyramidal neurons. J Neurophysiol 2002; 88: 621-626.
80. Power JM, Wu WW, Sametsky E, Oh MM, Disterhoft JF. Age-related enhancement of the slow outward calcium-activated potassium current in hippocampal CA1 pyramidal neurons in vitro. J Neurosci 2002; 22: 7234-7243.
81. Wu WW, Oh MM, Disterhoft JF. Age-related biophysical alterations of hippocampal pyramidal neurons: implications for learning and memory. Ageing Res Rev 2002; 1: 181-207.
82. Kramar EA, Lin B, Lin CY, Arai AC, Gall CM, Lynch G. A novel mechanism for the facilitation of theta-induced long-term potentiation by brain-derived neurotrophic factor. J Neurosci 2004; 24: 5151-5161.
83. Shah MM, Migliore M, Valencia I, Cooper EC, Brown DA. Functional significance of axonal Kv7 channels in hippocampal pyramidal neurons. Proc Natl Acad Sci USA 2008; 105: 7869-7874.
84. Shah MM, Mistry M, Marsh SJ, Brown DA, Delmas P. Molecular correlates of the M-current in cultured rat hippocampal neurons. J Physiol 2002; 544: 29-37.
85. Peters HC, Hu H, Pongs O, Storm JF, Isbrandt D. Conditional transgenic suppression of M channels in mouse brain reveals functions in neuronal excitability, resonance and behavior. Nat Neurosci 2005; 8: 51-60.
86. + current in a vertebrate neurone. Nature 1980; 283: 673-676.
87. Wu WW, Adelman JP, Maylie J. Ovarian hormone deficiency reduces intrinsic excitability and abolishes acute estrogen sensitivity in hippocampal CA1 pyramidal neurons. J Neurosci 2011; 31: 2638-2648.
88. Descarries L, Gisiger V, Steriade M. Diffuse transmission by acetylcholine in the CNS. Prog Neurobiol 1997; 53: 603-625.
89. Buno W, Cabezas C, Fernandez de Sevilla D. Presynaptic muscarinic control of glutamatergic synaptic transmission. J Mol Neurosci 2006; 30: 161-164.
90. Fernandez de Sevilla D, Buno W. Presynaptic inhibition of Schaffer collateral synapses by stimulation of hippocampal cholinergic afferent fibres. Eur J Neurosci 2003; 17: 555-558.
91. Hounsgaard J. Presynaptic inhibitory action of acetylcholine in area CA1 of the hippocampus. Exp Neurol 1978; 62: 787-797.
92. Qian J, Saggau P. Presynaptic inhibition of synaptic transmission in the rat hippocampus by activation of muscarinic receptors: involvement of presynaptic calcium influx. Br J Pharmacol 1997; 122: 511-519.
93. Cardoso CC, Pereira RT, Koyama CA, Porto CS, Abdalla FM. Effects of estrogen on muscarinic acetylcholine receptors in the rat hippocampus. Neuroendocrinology 2004; 80: 379-386.
94. Cardoso CC, Ricardo VP, Frussa-Filho R, Porto CS, Abdalla FM. Effects of 17beta-estradiol on expression of muscarinic acetylcholine receptor subtypes and estrogen receptor alpha in rat hippocampus. Eur J Pharmacol 2010; 634: 192-200.
95. El-Bakri NK, Adem A, Suliman IA, Mulugeta E, Karlsson E, Lindgren JU, Winblad B, Islam A. Estrogen and progesterone treatment: effects on muscarinic M(4) receptor subtype in the rat brain. Brain Res 2002; 948: 131-137.
96. Shinoe T, Matsui M, Taketo MM, Manabe T. Modulation of synaptic plasticity by physiological activation of M1 muscarinic acetylcholine receptors in the mouse hippocampus. J Neurosci 2005; 25: 11194-11200.
97. Sheridan RD, Sutor B. Presynaptic M1 muscarinic cholinoceptors mediate inhibition of excitatory synaptic transmission in the hippocampus in vitro. Neurosci Lett 1990; 108: 273-278.
98. Leung LS, Peloquin P. Cholinergic modulation differs between basal and apical dendritic excitation of hippocampal CA1 pyramidal cells. Cereb Cortex 2010; 20: 1865-1877.
99. Kremin T, Gerber D, Giocomo LM, Huang SY, Tonegawa S, Hasselmo ME. Muscarinic suppression in stratum radiatum of CA1 shows dependence on presynaptic M1 receptors and is not dependent on effects at GABA(B) receptors. Neurobiol Learn Mem 2006; 85: 153-163.
100. Seeger T, Fedorova I, Zheng F, Miyakawa T, Koustova E, Gomeza J, Basile AS, Alzheimer C, Wess J. M2 muscarinic acetylcholine receptor knock-out mice show deficits in behavioral flexibility, working memory, and hippocampal plasticity. J Neurosci 2004; 24: 10117-10127.
101. Dutar P, Nicoll RA. Classification of muscarinic responses in hippocampus in terms of receptor subtypes and second-messenger systems: electrophysiological studies in vitro. J Neurosci 1988; 8: 4214-4224.
102. Shirey JK, Xiang Z, Orton D, Brady AE, Johnson KA, Williams R, Ayala JE, Rodriguez AL, Wess J, Weaver D, Niswender CM, Conn PJ. An allosteric potentiator of M4 mAChR modulates hippocampal synaptic transmission. Nat Chem Biol 2008; 4: 42-50.
103. Dasari S, Gulledge AT. M1 and M4 receptors modulate hippocampal pyramidal neurons. J Neurophysiol 2011; 105: 779-792.
104. Sarter M, Parikh V, Howe WM. Phasic acetylcholine release and the volume transmission hypothesis: time to move on. Nat Rev Neurosci 2009; 10: 383-390.
105. Umbriaco D, Watkins KC, Descarries L, Cozzari C, Hartman BK. Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: an electron microscopic study in serial sections. J Comp Neurol 1994; 348: 351-373.
106. Umbriaco D, Garcia S, Beaulieu C, Descarries L. Relational features of acetylcholine, noradrenaline, serotonin and GABA axon terminals in the stratum radiatum of adult rat hippocampus (CA1). Hippocampus 1995; 5: 605-620.