Role of the medial septum diagonal band of Broca cholinergic neurons in oestrogen-induced spine synapse formation on hippocampal CA1 pyramidal cells of female rats

European Journal of Neuroscience

Volumn 17, Issue 10, 2003, Pages 1997-2005

  Lâm, Thiên Trí ^a,b   Leranth, Csaba ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Acetylcholine; Ovariectomy; Parvalbumin; Septo hippocampal projection; Spine synapse density; Unbiased stereological calculation

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CHOLESTEROL; CHOLINE ACETYLTRANSFERASE; ENZYME ANTIBODY; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; PARVALBUMIN; SAPORIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DIAGONAL BAND OF BROCA; ELECTRON MICROSCOPY; ESTROGEN ACTIVITY; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LATERAL BRAIN VENTRICLE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SPINAL CORD; STEREOMETRY; SYNAPTOGENESIS;

ACETYLCHOLINE; ANIMALS; CHOLINE O-ACETYLTRANSFERASE; DIAGONAL BAND OF BROCA; ESTROGENS; FEMALE; MICROSCOPY, ELECTRON; NEURONAL PLASTICITY; OVARIECTOMY; PARVALBUMINS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 0038472369     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02637.x     Document Type: Article

References (67)

1. Alreja, M., Wu, M., Liu, W., Atkins, JB., Leranth, C. & Shanabrough, M. (2000) Muscarinic tone sustains impulse flow in the septohippocampal GABA but not cholinergic pathway: implications for learning and memory. J. Neurosci., 20, 8103-8110.
2. Bland, B.H. (1986) The physiology and pharmacology of hippocampal formation theta rhythms. Prog. Neurobiol., 26, 1-54.
3. Blurton-Jones, M. & Tuszynski, M.H. (2002) Estrogen receptor-beta colocalizes extensively with parvalbumin-labeled inhibitory neurons in the cortex, amygdala, basal forebrain, and hippocampal formation of intact and ovariectomized adult rats. J. Comp. Neurol., 452, 276-287.
4. Book, A.A., Wiley, R.G. & Schweitzer, J.B. (1992) Specificity of 192 IgG-saporin for NGF receptor-positive cholinergic basal forebrain neurons in the rat. Brain Res., 590, 350-355.
5. Braendgaard, H. & Gundersen, H.J. (1986) The impact of recent stereological advances on quantitative studies of the nervous system. J. Neurosci. Meth., 18, 39-78.
6. Daniel, J.M. & Dohanich, G.P. (2001) Acetylcholine mediates estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and associated improvement in working memory. J. Neurosci., 21, 6949-6956.
7. Daniel, J.M., Fader, A.J., Spencer, A.L. & Dohanich, G.P. (1997) Estrogen enhances performances of female rats during acquisition of a radial arm maze. Horm. Behav., 32, 217-225.
8. Fillit, H., Weinreb, H., Cholst, I., Luine, V., McEwen, B., Amador, R. & Zabriskie, J. (1986) Observations in a preliminary open trial of estradiol therapy for senile dementia-Alzheimer's type. Psychoendocrinology, 11, 337-345.
9. Foy, M.R. (2001) 17β-Estradiol: effect on CA1 hippocampal synaptic plasticity. Neurobiol. Learn. Mem., 76, 239-252.
10. Freund, T.F. (1989) GABAergic septo-hippocampal neurons contain parvalbumin. Brain Res., 478, 375-381.
11. Freund, T.F. & Antal, M. (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature, 336, 170-173.
12. Frotscher, M. & Leranth, C. (1985) Cholinergic innervation of the rat hippocampus as revealed by choline-acetyltransferase immunocytochemistry: a combined light and electron-microscopic study. J. Comp. Neurol., 239, 237-246.
13. Gibbs, R.B. (1994) Estrogen and nerve growth factor-related systems in brain. Effects on basal forebrain cholinergic neurons and implications for learning and memory processes and aging. Ann. NY Acad. Sci., 743, 165-196.
14. Gibbs, R.B. (1996a) Expression of estrogen receptor-like immunoreactivity by different subgroups of basal forebrain cholinergic neurons in gonadectomized male and female rats. Brain Res., 720, 61-68.
15. Gibbs, R.B. (1996b) Fluctuations in relative levels of choline acetyltransferase mRNA in different regions of the rat basal forebrain across the estrous cycle: effects of estrogen and progesterone. J. Neurosci., 16, 244-252.
16. NGFR and ChAT expression in the medial septum and diagonal band of Broca. Exp. Neurol., 116, 23-39.
17. Gould, E., Woolley, C.S., Frankfurt, M. & McEwen, B.S, (1990) Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci., 10, 1286-1291.
18. Green, J.D. & Arduni, A.A. (1954) Hippocampal electrical activity in arousal. J. Neurophysiol., 17, 533-557.
19. Heckers, S., Ohtake, T., Wiley, F.G., Lappi, D.A., Geula, C. & Mesulam, M.M. (1994) Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdale by immunotoxin against the p75 NGF receptor. J. Neurosci., 14, 1271-1289.
20. Hendersen, V.W., Paganini-Hill, A., Emanuel, C.K., Dunn, M.E. & Buckwalter, J.G. (1994) Estrogen replacement therapy in older women: Comparisons between Alzheimer's disease cases and non-demented controls. Arch. Neurol., 51, 896-900.
21. Hogervorst, E., Yaffe, K., Richards, M. & Huppert, F. (2002a) Hormone replacement therapy for cognitive function in postmenopausal women (Cochrane Review). In The Cochrane Library, Issue 4. Update Software, Oxford.
22. Hogervorst, E., Yaffe, K., Richards, M. & Huppert, F. (2002b) Hormone replacement therapy to maintain cognitive function in women with dementia (Cochrane Review). In The Cochrane Library, Issue 4. Update Software, Oxford.
23. Honjo, H., Ogino, Y., Naitoh, K., Urabe, M., Kitawaki, J., Yasuda, J., Yamamota, T., Ishihara, S., Okada, H., Yonezawa, T., Hayashi, K. & Nambara, T. (1989) In vivo effect by estrone sulfate on the central nervous system-senile dementia (Alzheimer's type). J. Steroid Biochem., 34, 521-525.
24. Jakab, R.L. & Leranth, C. (1994) Septum. In Paxinos, G. (ed.), The Rat Nervous System. Academic Press, Inc., Toronto, pp. 405-442.
25. Johnson, D.A., Zambon, N.J. & Gibbs, R.B. (2002) Selective lesion of cholinergic neurons in the medial septum by 192 IgG-saporin impairs learning and delayed matching to position T-maze paradigm. Brain Res., 943, 132-141.
26. Kampen, D.L. & Sherwin, B.B. (1994) Estrogen usa and verbal memory in healthy postmenopausal women. Obstet. Gynecol., 83, 979-983.
27. Klintsova, A., Levy, W.B. & Desmond, N.L. (1995) Astrocytic Volume fluctuates in the hippocampal CA1 region across the estrous cycle. Brain Res., 690, 269-274.
28. Kohler, C., Chan-Palay, V. & Wu, J.-Y. (1984) Septal neurons containing glutamic acid decarboxylase immunoreactivity project to the hippocampal region in the rat brain. Anat. Embryol., 169, 41-44.
29. Kordower, J.H., Chen, E.Y., Sladek, J.R.J. & Mufson, E.J. (1994) Trk-immunoreactivity in the monkey central nervous system: forebrain. J. Comp. Neurol., 349, 20-35.
30. Lâm, T.T. & Leranth, C. (2002) Gonadal hormones act extrinsic to the hippocampus to influence the density of hippocampal astroglial processes. Neuroscience, 116, 491-498.
31. Lee, M.G., Chrobak, I.J., Sik, A., Wiley, R.G. & Buzsaki, G. (1994) Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience, 62, 1033-1047.
32. Leranth, C. & Frotscher, M. (1989) Organization of the septal region in the rat brain: cholinergic-GABAergic interconnections and the termination of hippocampo-septal fibers. J. Comp. Neurol., 289, 304-314.
33. Leranth, C. & Shanabrough, M. (2001) Supramammilary area mediates subcortical estrogenic action on hippocampal synaptic plasticity. Exp. Neurol., 167, 445-450.
34. Leranth, C., Shanabrough, M. & Horvath, T.L. (1999) Estrogen receptor-alpha in the raphe serotonergic and supramammillary area calretinin-containing neurons of the female rat. Exp. Brain Res., 128, 417-420.
35. Leranth, C., Shanabrough, M. & Horvath, T.L. (2000) Hormonal regulation of hippocampal spine synapse density involves subcortical mediation. Neuroscience, 101, 349-356.
36. Leranth, C., Shanabrough, M. & Redmond, D.E. (2002) Gonadal hormones are responsible for maintaining the integrity of spine synapses in the CA1 hippocampal subfield of female non-human primates. J. Comp. Neurol., 447, 34-42.
37. Lewis, P.R. & Shute, C.CD. (1967) The cholinergic limbic system: Projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system and the subfornical organ and supraoptic crest. Brain, 90, 521-540.
38. Luine, V.N. (1985) Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats. Exp. Neurol., 89, 484-490.
39. Markowska, A.L. & Savonenko, A.V. (2002) Effectiveness of estrogen replacement in restoration of cognitive function after long-term estrogen withdrawal in aging rats. J. Neurosci., 22, 10985-10995.
40. McEwen, B.S. & Alves, S.E. (1999) Estrogen actions in the central nervous system. Endocr. Rev., 20, 279-307.
41. McMillan, P.J., Singer, C.A. & Dorsa, D.M. (1996) The effects of ovariectomy and estrogen replacement on rtkA and choline acetyltransferase mRNA expression in the basal forebrain of the adult female Sprague-Dawley rat. J. Neurosci., 16, 1860-1865.
42. Mufson, E.J., Cai, W.J., Jaffar, S., Chen, E., Stebbins, G., Sendera, T. & Kordower, J.H. (1999) Estrogen receptor immunoreactivity within subregions of the rat forebrain: neuronal distribution and association with perikarya containing choline acetyltransferase. Brain Res., 849 (1-2), 253-274.
43. Mufson, E.J., Lavine, M., Jaffar, S. & Levey, A.I. (1997) m2 muscarinic acetylcholine receptor-immunoreactive neurons are not reduced within the nucleus basalis in Alzheimer's disease. Exp. Neurol., 146, 91-103.
44. Mufson, E.J., Li, T., Sobreviela, T. & Kordower, J.H. (1996) Decreased trkA gene expression within basal forebrain neurons in Alzheimer's disease. Neuroreport., 8, 25-29.
45. Mulnard, R.A., Cotman, C.W., Kawas, C., van Dyck, C.H., Sano, M., Doody, R., Koss, E., Pfeiffer, E., Jin, S., Gamst, A., Grundman, M., Thomas, R. & Thal, L.J. (2000) Estrogen replacement therapy for treatment of mild to moderate Alzheimer disease: a randomized controlled trial. Alzheimer's Disease Cooperative Study. JAMA, 283, 1007-1015.
46. Murphy, D.D. & Segal, M. (1996) Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J. Neurosci., 16, 4059-4068.
47. Packard, M.G. (1998) Posttraining estrogen and memory modulation. Horm. Behav., 34, 126-139.
48. Paxinos, G. & Watson, C. (2001) The rat brain in stereotaxic coordinates, 3rd edn. Academic Press, Australia.
49. Pleim, E.T., Brown, T.J., MacLusky, N.J., Etgen, A.M. & Barfield, R.J. (1989) Dilute estrogen implants and progestin receptor induction in the ventromedial nucleus of the hypothalamus: correlation with receptive behavior in female rats. Endocrinology, 124, 1807-1812.
50. Rusakov, D.A., Davies, H.A., Harrison, E., Diana, G., Richter-Levin, G., Bliss, T.V.P. & Stewart, M.G. (1997) Ultrastructural synaptic correlates of spatial learning in rat hippocampus. Neuroscience, 80, 69-77.
51. Sherwin, B.B. (1988) Estrogen and/or androgen replacement therapy and cognitive functioning in surgically menopausal women. Psychoneuroendocrinology, 10, 325-335.
52. Sherwin, B.B. (1998) Estrogen and cognitive functioning in women. Proc. Soc. Exp. Biol. Med., 217, 17-22.
53. Shughrue, P.J., Scrimo, P.J. & Merchenthaler, I. (2000) Estrogen binding and estrogen receptor characterization (ERα and ERβ) in the cholinergic neurons of the rat basal forebrain. Neuroscience, 96, 41-49.
54. Singh, M., Meyer, E.M., Millard, W.J. & Simpkins, J.W. (1994) Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats. Brain Res., 644, 305-312.
55. Small, J.V. (1968) Measurement of section thickness. Proceedings of the Fourth European Conference on Electron Microscopy. Tipografia Poliglotta Vaticana, Rome, pp. 609-610.
56. Sobreviela, T., Clary, D.O., Reichardt, L.F., Brandabur, M.M., Kordower, J.H. & Mufson, E.J. (1994) TrkA-immunoreactive profiles in the central nervous system: colocalization with neurons containing p75 nerve growth factor receptor, choline acetyltransferase, and serotonin. J. Comp. Neurol., 350, 587-611.
57. Sobreviela, T.S., Jaffar, S. & Mufson, E.J. (1998) TrkA, Galanin and nitric oxide synthase within basal forebrain neurons in the rat. Neuroscience, 87, 447-461.
58. Sterio, D.C. (1984) The unbiased estimation of number and sizes of particles using the disector. J. Microsc., 134, 127-136.
59. Tang, M., Jacobs, D., Stern, Y., Marder, K., Schofield, P., Gurland, B. & Andrews, H. (1996) Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease. Lancet, 348, 429-432.
60. Waite, J.J. & Chen, A.D. (2001) Differential changes in rat cholinergic parameters subsequent to immunotoxic lesion of the basal forebrain nuclei. Brain Res., 918, 113-120.
61. Waite, J.J., Chen, A.D., Wardlow, M.L., Wiley, R.G., Lappi, D.A. & Thal, L.J. (1995) 192 immunoglobulin G-sapotin produces graded behavioral and biochemical changes accompanying the loss of cholinergic neurons of the basal forebrain and cerebellar Purkinje cells. Neuroscience, 65, 463-476.
62. Walsh, T.J., Kelly, R.M., Dougherty, K.D., Stackman, R.W., Wiley, R.G. & Kutscher, C.L. (1995) Behavioral and neurobiological alterations induced by the immmunotoxin 192 IgG-saporin: cholinergic and non-cholinergic effects following i.c.v injection. Brain Res., 702, 233-245.
63. Williams, C.L., Barnett, A.M. & Meck, W.H. (1990) Organizational effects of early gonadal secretions on sexual differentiation m spatial memory. Behav. Neurosci., 104 (1), 84-97.
64. Woolley, C.S., Gould, E., Frankfurt, M. & McEwen, B.S. (1990) Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J. Neurosci., 10, 4035-4039.
65. Woolley, C.S. & McEwen, B.S. (1992) Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci., 12, 2549-2554.
66. Wu, M., Shanabrough, M., Leranth, C. & Alreja, M. (2000) Cholinergic excitation of septohippocampal GABA but not cholinergic neurons: implications for learning and memory. J. Neurosci., 20, 3900-3908.
67. Zandi, P.P., Carlson, M.C., Plassman, B.L., Welsh-Bohmer, KA, Mayer, L.S., Steffens, D.C. & Breitner, J.C. (2002) Hormone replacement therapy and incidence of Alzheimer disease in older women: the Cache County Study. JAMA, 288, 2123-2129.