Sex Steroids and Acetylcholine Release in the Hippocampus

Vitamins and Hormones

Volumn 82, Issue , 2010, Pages 263-277

  Mitsushima, Dai ^a  

^a YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Acetylcholine; Androgen; Diurnal rhythm; Estrogen; Learning and memory; Sex difference

Indexed keywords

ACETYLCHOLINE; SEX HORMONE;

ALZHEIMER DISEASE; ANIMAL; ANIMAL BEHAVIOR; BLOOD; FEMALE; HIPPOCAMPUS; HUMAN; MALE; METABOLISM; PHYSIOLOGY; RAT; REVIEW; SECRETION; SEX DIFFERENCE;

ACETYLCHOLINE; ALZHEIMER DISEASE; ANIMALS; BEHAVIOR, ANIMAL; FEMALE; GONADAL STEROID HORMONES; HIPPOCAMPUS; HUMANS; MALE; RATS; SEX FACTORS;

EID: 77955898882     PISSN: 00836729     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0083-6729(10)82014-X     Document Type: Chapter

References (85)

1. Auerbach, J.M., Segal, M., Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus. J. Physiol. 492 (1996), 479–493.
2. Beatty, W.W., Hormonal organization of sex differences in play fighting and spatial behavior. Prog. Brain Res. 61 (1984), 315–330.
3. Brown, R.T., Early experience and problem-solving ability. J. Comp. Physiol. Psychol. 65 (1968), 433–440.
4. Buzsáki, G., Bickford, R.G., Ponomareff, G., Thal, L.J., Mandel, R., Gage, F.H., Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J. Neurosci. 8 (1988), 4007–4026.
5. Cherrier, M.M., Matsumoto, A.M., Amory, J.K., Asthana, S., Bremner, W., Peskind, E.R., Raskind, M.A., Craft, S., Testosterone improves spatial memory in men with Alzheimer disease and mild cognitive impairment. Neurology 64 (2005), 2063–2068.
6. Cole, A.E., Nicoll, R.A., Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science 221 (1983), 1299–1301.
7. Coyle, J.T., Price, D.L., DeLong, M.R., Alzheimer's disease: A disorder of cortical cholinergic innervation. Science 219 (1983), 1184–1190.
8. Cummings, J.L., Alzheimer's disease. N. Engl. J. Med. 351 (2004), 56–67.
9. 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. 32 (1997), 217–225.
10. Day, J., Damsma, G., Fibiger, H.C., Cholinergic activity in the rat hippocampus, cortex and striatum correlates with locomotor activity: An in vivo microdialysis study. Pharmacol. Biochem. Behav. 38 (1991), 723–729.
11. Eckel-Mahan, K.L., Phan, T., Han, S., Wang, H., Chan, G.C., Scheiner, Z.S., Storm, D.R., Circadian oscillation of hippocampal MAPK activity and cAMP: Implications for memory persistence. Nat. Neurosci. 11 (2008), 1074–1082.
12. Einon, D., Spatial memory and response strategies in rats: Age, sex and rearing differences in performance. Q. J. Exp. Psychol. 32 (1980), 473–489.
13. Endo, Y., Mizuno, T., Fujita, K., Funabashi, T., Kimura, F., Soft-diet feeding during development enhances later learning abilities in female rats. Physiol. Behav. 56 (1994), 629–633.
14. Falvo, R.E., Buhl, A., Nalbandov, A.V., Testosterone concentrations in the peripheral plasma of androgenized female rats and in the estrous cycle of normal female rats. Endocrinology 95 (1974), 26–29.
15. 3-receptor activation induces long-lasting synaptic enhancement in CA1 pyramidal neurons. J. Neurosci. 28 (2008), 1469–1478.
16. Ferri, C.P., Prince, M., Brayne, C., Brodaty, H., Fratiglioni, L., Ganguli, M., Hall, K., Hasegawa, K., Hendrie, H., Huang, Y., Jorm, A., Mathers, C., et al. Global prevalence of dementia: A Delphi consensus study. Lancet 366 (2005), 2112–2117.
17. Gibbs, R.B., Pfaff, D.W., Effects of estrogen and fimbria / fornix transaction on p75NGFR and ChAT expression in the medial septum and diagonal band of Broca. Exp. Neurol. 116 (1992), 23–39.
18. Gold, P.E., Acetylcholine modulation of neural systems involved in learning and memory. Neurobiol. Learn. Mem. 80 (2003), 194–210.
19. Greenough, W.T., Madden, T.C., Fleischmann, T.B., Effects of isolation, daily handling, and enriched rearing on maze learning. Psychon. Sci. 27 (1972), 279–280.
20. Herrera-Morales, W., Mar, I., Serrano, B., Bermúdez-Rattoni, F., Activation of hippocampal postsynaptic muscarinic receptors is involved in long-term spatial memory formation. Eur. J. Neurosci. 25 (2007), 1581–1588.
21. Hironaka, N., Tanaka, K., Izaki, Y., Hori, K., Nomura, M., Memory-related acetylcholine efflux from the rat prefrontal cortex and hippocampus: A microdialysis study. Brain Res. 901 (2001), 143–150.
22. Hyman, J.M., Wyble, B.P., Goyal, V., Rossi, C.A., Hasselmo, M.E., Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J. Neurosci. 23 (2003), 11725–11731.
23. Hymovitch, B., The effects of experimental variations on problem solving in the rat. J. Comp. Physiol. Psychol. 45 (1952), 313–321.
24. Juraska, J.M., Henderson, C., Muller, J., Differential rearing experience, gender, and radial maze performance. Dev. Psychobiol. 17 (1984), 209–215.
25. Kotani, S., Yamauchi, T., Teramoto, T., Ogura, H., Pharmacological evidence of cholinergic involvement in adult hippocampal neurogenesis in rats. Neuroscience 142 (2006), 505–514.
26. Kritzer, M.F., Selective colocalization of immunoreactivity for intracellular gonadal hormone receptors and tyrosine hydroxylase in the ventral tegmental area, substantia nigra, and retrorubral fields in the rat. J. Comp. Neurol. 379 (1997), 247–260.
27. Kritzer, M.F., McLaughlin, P.J., Smirlis, T., Robinson, J.K., Gonadectomy impairs T-maze acquisition in adult male rats. Horm. Behav. 39 (2001), 167–174.
28. Lee, M.G., Chrobak, J.J., Sik, A., Wiley, R.G., Buzsáki, G., Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62 (1994), 1033–1047.
29. Luine, V.N., Renner, K.J., McEwen, B.S., Sex-dependent differences in estrogen regulation of choline acetyltransferase are altered by neonatal treatments. Endocrinology 119 (1986), 874–878.
30. Luine, V., Jacome, L.F., MacLusky, N.J., Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 144 (2003), 2836–2844.
31. Lund, T.D., Hinds, L.R., Handa, R.J., The androgen 5α-dihydrotestosterone and its metabolite 5α-androstan-3β, 17β-diol inhibit the hypothalamo-pituitary-adrenal response to stress by acting through estrogen receptor β-expressing neurons in the hypothalamus. J. Neurosci. 26 (2006), 1448–1456.
32. Markowska, A.J., Savonenko, A.V., Effectiveness of estrogen replacement in restoration of cognitive function after long-term estrogen withdrawal in aging rats. J. Neurosci. 22 (2002), 10985–10995.
33. Markram, H., Segal, M., Long-lasting facilitation of excitatory postsynaptic potentials in the rat hippocampus by acetylcholine. J. Physiol. 427 (1990), 381–393.
34. Masuda, J., Mitsushima, D., Funabashi, T., Kimura, F., Sex and housing conditions affect the 24-h acetylcholine release profile in the hippocampus in rats. Neuroscience 132 (2005), 537–542.
35. McCurry, S.M., Logsdon, R.G., Vitiello, M.V., Teri, L., Treatment of sleep and nighttime disturbances in Alzheimer's disease: A behavior management approach. Sleep Med. 5 (2004), 373–377.
36. McEwen, B.S., Neural gonadal steroid actions. Science 211 (1981), 1303–1311.
37. McEwen, B.S., Alves, S.E., Estrogen actions in the central nervous system. Endocr. Rev. 20 (1999), 279–307.
38. Mesulam, M.M., Mufson, E.J., Wainer, B.H., Levey, A.I., Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10 (1983), 1185–1201.
39. Miettinen, R.A., Kalesnykas, G., Koivisto, E.H., Estimation of the total number of cholinergic neurons containing estrogen receptor-a in the rat basal forebrain. J. Histochem. Cytochem. 50 (2002), 891–902.
40. Mitsushima, D., Mizuno, T., Kimura, F., Age-related changes in diurnal acetylcholine release in the prefrontal cortex of male rats as measured by microdialysis. Neuroscience 72 (1996), 429–434.
41. Mitsushima, D., Yamanoi, C., Kimura, F., Restriction of environmental space attenuates locomotor activity and hippocampal acetylcholine release in male rats. Brain Res. 805 (1998), 207–212.
42. Mitsushima, D., Funabashi, T., Shinohara, K., Kimura, F., Impairment of maze learning in rats by restricting environmental space. Neurosci. Lett. 297 (2001), 73–76.
43. Mitsushima, D., Masuda, J., Kimura, F., Sex differences in the stress-induced release of acetylcholine in the hippocampus and corticosterone from the adrenal cortex in rats. Neuroendocrinology 78 (2003), 234–240.
44. Mitsushima, D., Tin-Tin-Win-Shwe, Kimura, F., Sexual dimorphism in the GABAergic control of gonadotropin release in intact rats. Neurosci. Res. 46 (2003), 399–405.
45. Mitsushima, D., Takase, K., Funabashi, T., Kimura, F., Gonadal steroid hormones maintain the stress-induced acetylcholine release in the hippocampus: Simultaneous measurements of the extracellular acetylcholine and serum corticosterone levels in the same subjects. Endocrinology 149 (2008), 802–811.
46. Mitsushima, D., Takase, K., Funabashi, T., Kimura, F., Gonadal steroids maintain 24-h acetylcholine release in the hippocampus: Organizational and activational effects in behaving rats. J. Neurosci. 29 (2009), 3808–3815.
47. Mizuno, T., Kimura, F., Medial septal injection of naloxone elevates acetylcholine release in the hippocampus and induces behavioral seizures in rats. Brain Res. 713 (1996), 1–7.
48. Mizuno, T., Endo, Y., Arita, J., Kimura, F., Acetylcholine release in the rat hippocampus as measured by the microdialysis method correlates with motor activity and exhibits a diurnal variation. Neuroscience 44 (1991), 607–612.
49. Moffat, S.D., Zonderman, A.B., Metter, E.J., Kawas, C., Blackman, M.R., Harman, S.M., Resnick, S.M., Free testosterone and risk for Alzheimer disease in older men. Neurology 62 (2004), 188–193.
50. Mohapel, P., Leanza, G., Kokaia, M., Lindvall, O., Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol. Aging 26 (2005), 939–946.
51. Moor, E., DeBoer, P., Westerink, B.H.C., GABA receptors and benzodiazepine binding sites modulate hippocampal acetylcholine release in vivo. Eur. J. Pharmacol. 359 (1998), 119–126.
52. Mount, C., Downtown, D., Alzheimer disease: Progress or profit?. Nat. Med. 12 (2006), 780–784.
53. Mufson, E.J., Cai, W.J., Jaffar, S., Chen, E., Stebbins, G., Sendera, T., Kordower, J.H., Estrogen receptor immunoreactivity within subregions of the rat forebrain: Neuronal distribution and association with perikarya containing choline acetyltransferase. Brain Res. 849 (1999), 253–274.
54. Nakamura, N., Fujita, H., Kawata, M., Effects of gonadectomy on immunoreactivity for choline acetyltransferase in the cortex, hippocampus, and basal forebrain of adult male rats. Neuroscience 109 (2002), 473–485.
55. Nilsson, O.G., Leanza, G., Bjorklund, A., Acetylcholine release in the hippocampus: Regulation by monoaminergic afferents as assessed by in vivo microdialysis. Brain Res. 584 (1992), 132–140.
56. Norbury, R., Travis, M.J., Erlandsson, K., Waddington, W., Ell, P.J., Murphy, D.G.M., Estrogen therapy and brain muscarinic receptor density in healthy females: A SPET study. Horm. Behav. 51 (2007), 249–257.
57. Parducz, A., Hajszan, T., Maclusky, N.J., Hoyk, Z., Csakvari, E., Kurunczi, A., Prange-Kiel, J., Leranth, C., Synaptic remodeling induced by gonadal hormones: Neuronal plasticity as a mediator of neuroendocrine and behavioral responses to steroids. Neuroscience 138 (2006), 977–985.
58. Parent, M.B., Baxter, M.G., Septohippocampal acetylcholine: Involved in but not necessary for learning and memory?. Learn. Mem. 11 (2004), 9–20.
59. Perry, E., Walker, M., Grace, J., Perry, R., Acetylcholine in mind: A neurotransmitter correlate of consciousness?. Trend Neurosci. 22 (1999), 273–280.
60. Petersen, R.C., Thomas, R.G., Grundman, M., Bennett, D., Doody, R., Ferris, S., Galasko, D., Jin, S., Kaye, J., Levey, A., Pfeiffer, E., Sano, M., et al. Vitamin E and donepezil for the treatment of mild cognitive impairment. N. Engl. J. Med. 352 (2005), 2379–2388.
61. Pongrac, J.L., Gibbs, R.B., Defranco, D.B., Estrogen-mediated regulation of cholinergic expression in basal forebrain neurons requires extracellular signal-regulated kinase activity. Neuroscience 124 (2004), 809–816.
62. Ragozzino, M.E., Unick, K.E., Gold, P.E., Hippocampal acetylcholine release during memory testing in rats: Augmentation by glucose. Proc. Natl. Acad. Sci. USA 93 (1996), 4693–4698.
63. Romeo, R.D., McCarthy, J.B., Wang, A., Milner, T.A., McEwen, B.S., Sex differences in hippocampal estradiol-induced N-methyl-D-aspartic acid binding and ultrastructural localization of estrogen receptor-α. Neuroendocrinology 81 (2005), 391–399.
64. Rosario, E.R., Chang, L., Stanczyk, F.Z., Pike, C.J., Age-related testosterone deplation and the development of Alzheimer disease. JAMA 292 (2004), 1431–1432.
65. Rush, M.E., Blake, C.A., Serum testosterone concentrations during the 4-day estrous cycle in normal and adrenalectomized rats. Proc. Soc. Exp. Biol. Med. 169 (1982), 216–221.
66. Sarter, M., Parikh, V., Choline transporters, cholinergic transmission and cognition. Nat. Neurosci. 6 (2005), 48–56.
67. 2 muscarinic acetylcholine receptor knock-out mice show deficits in behavioral flexibility, working memory, and hippocampal plasticity. J. Neurosci. 24 (2004), 10117–10127.
68. Seymoure, P., Dou, H., Juraska, J.M., Sex differences in radial arm maze performance: Influence of rearing environment and room cues. Psychobiology 24 (1996), 33–37.
69. 1 muscarinic acetylcholine receptors in the mouse hippocampus. J. Neurosci. 25 (2005), 11194–11200.
70. Shors, T.J., Chua, C., Falduto, J., Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J. Neurosci. 21 (2001), 6292–6297.
71. Smith, H.V., Effects of environmental enrichment on open-field activity and Hebb–Williams problem solving in rats. J. Comp. Physiol. Psychol. 80 (1972), 163–168.
72. Stancampiano, R., Cocco, S., Cugusi, C., Sarais, L., Fadda, F., Serotonin and acetylcholine release response in the rat hippocampus during a spatial memory task. Neuroscience 89 (1999), 1135–1143.
73. Starkstein, S.E., Jorge, R., Mizrahi, R., Robinson, R.G., The construct of minor and major depression in Alzheimer's disease. Am. J. Psychiatry 162 (2005), 2086–2093.
74. Swaab, D.F., Hofman, M.A., Sexual differentiation of the human hypothalamus in relation to gender and sexual orientation. Trend Neurosci. 18 (1995), 264–270.
75. Swanson, L.W., The projections of the ventral tegmental area and adjacent regions: A combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 9 (1982), 321–353.
76. Takase, K., Funabashi, T., Mogi, K., Mitsushima, D., Kimura, F., Feeding with powdered diet after weaning increases visuospatial ability in association with increases in the expression of N-methyl-D-aspartate receptors in the hippocampus of female rats. Neurosci. Res. 53 (2005), 169–175.
77. Takase, K., Mitsushima, D., Masuda, J., Mogi, K., Funabashi, T., Endo, Y., Kimura, F., Feeding with powdered diet after weaning affects sex difference in acetylcholine release in the hippocampus in rats. Neuroscience 136 (2005), 593–599.
78. Takase, K., Kimura, F., Yagami, T., Mitsushima, D., Sex-specific 24-h acetylcholine release profile in the medial prefrontal cortex: Simultaneous measurement of spontaneous locomotor activity in behaving rats. Neuroscience 159 (2009), 7–15.
79. van Praag, H., Christie, B.R., Sejnowski, T.J., Gage, F.H., Running enhances neurogenesis, learning and long-term potentiation in mice. Proc. Natl. Acad. Sci. USA 96 (1999), 13427–13431.
80. 2 dopamine receptor mRNA in rat brain. Proc. Natl. Acad. Sci. USA 88 (1991), 1859–1863.
81. Widmer, H., Ferrigan, L., Davies, C.H., Cobb, S.R., Evoked slow muscarinic acetylcholinergic synaptic potentials in rat hippocampal interneurons. Hippocampus 16 (2006), 617–628.
82. Williams, C.L., Meck, W.H., The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology 16 (1991), 155–176.
83. Winblad, B., Kilander, L., Eriksson, S., Minthon, L., Båtsman, S., Wetterholm, A.L., Jansson-Blixt, C., Haglund, A., Donepezil in patients with severe Alzheimer's disease: Double-blind, parallel-group, placebo-controlled study. Lancet 367 (2006), 1057–1065.
84. Yanai, J., Rogel-Fuchs, Y., Pick, C.G., Slotkin, T., Seidler, F.J., Zahalka, E.A., Newman, M.E., Septohippocampal cholinergic changes after destruction of the A10-septal dopaminergic pathways. Neuropharmacology 32 (1993), 113–117.
85. Zandi, P.P., Carlson, M.C., Plassman, B.L., Welsh-Bohmer, K.A., Mayer, L.S., Steffens, D.C., Breitner, J.C.S., Hormone replacement therapy and incidence of Alzheimer disease in older women. JAMA 288 (2002), 2123–2129.