 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
The Journal of Neuroscience, June 1, 2003, 23(11):4479-4490
Previous Article | Next Article
A Role for the Basal Forebrain Cholinergic System in Estrogen-Induced Disinhibition of Hippocampal Pyramidal Cells
Charles N. Rudick,1 Robert B. Gibbs,2 andCatherine S. Woolley1 1 Department of Neurobiology and Physiology and Northwestern University Institute for Neuroscience, Northwestern University, Evanston, Illinois 60208, and 2 Department of Pharmaceutical Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania 15261
Estrogen transiently disinhibits hippocampal CA1 pyramidal cells in adult female rats and prolongs the decay time of IPSCs in these cells. Estrogen-induced changes in synaptic inhibition are likely to be causally related to subsequent enhancements in excitatory synaptic function in CA1 pyramidal cells. Currently, it is unknown how or on what cells estrogen acts to regulate synaptic inhibition in the hippocampus. We used whole-cell voltage-clamp recording of synaptically evoked IPSCs, spontaneous IPSCs, and miniature IPSCs in CA1 pyramidal cells to evaluate estrogen-induced changes in synaptic inhibition in ovariectomized rats that either were pretreated with the estrogen receptor (ER) antagonist tamoxifen or in which basal forebrain cholinergic neurons were eliminated by previous infusion of 192IgG-saporin toxin into the medial septum. We found that estrogen-induced disinhibition and prolongation of IPSCs are entirely dependent on a tamoxifen-sensitive ER. Estrogen-induced disinhibition is partially dependent on basal forebrain cholinergic neurons, but the prolongation of IPSCs is not at all dependent on these cells. Paired-pulse experiments and recordings of action potential-related spontaneous IPSCs suggest that estrogen-induced disinhibition is associated with a decrease in probability of release at GABAergic synapses, which decreases the amplitude of IPSCs produced by inhibitory neuron action potentials. Our findings lend novel insights into estrogen regulation of inhibitory synapses in the hippocampus and point to estrogen action on basal forebrain cholinergic neurons as critically involved in mediating the effects of estrogen in the hippocampus.
Key words: GABA; IPSCs; tamoxifen; ChAT; estradiol; 192IgG-saporin; CA1
Received Dec. 26, 2002; revised Mar. 13, 2003; accepted Mar. 17, 2003.
This article has been cited by other articles:
G. Barreto, M. Santos-Galindo, Y. Diz-Chaves, O. Pernia, P. Carrero, I. Azcoitia, and L. M. Garcia-Segura
Selective Estrogen Receptor Modulators Decrease Reactive Astrogliosis in the Injured Brain: Effects of Aging and Prolonged Depletion of Ovarian Hormones
Endocrinology, November 1, 2009; 150(11): 5010 - 5015.
[Abstract] [Full Text] [PDF]
L. A. Tremere, J. K. Jeong, and R. Pinaud
Estradiol Shapes Auditory Processing in the Adult Brain by Regulating Inhibitory Transmission and Plasticity-Associated Gene Expression
J. Neurosci., May 6, 2009; 29(18): 5949 - 5963.
[Abstract] [Full Text] [PDF]
V. A. Ledoux, T. Smejkalova, R. M. May, B. M. Cooke, and C. S. Woolley
Estradiol Facilitates the Release of Neuropeptide Y to Suppress Hippocampus-Dependent Seizures
J. Neurosci., February 4, 2009; 29(5): 1457 - 1468.
[Abstract] [Full Text] [PDF]
S. A. Hart, M. A. Snyder, T. Smejkalova, and C. S. Woolley
Estrogen Mobilizes a Subset of Estrogen Receptor-{alpha}-Immunoreactive Vesicles in Inhibitory Presynaptic Boutons in Hippocampal CA1
J. Neurosci., February 21, 2007; 27(8): 2102 - 2111.
[Abstract] [Full Text] [PDF]
J. H. Morrison, R. D. Brinton, P. J. Schmidt, and A. C. Gore
Estrogen, Menopause, and the Aging Brain: How Basic Neuroscience Can Inform Hormone Therapy in Women
J. Neurosci., October 11, 2006; 26(41): 10332 - 10348.
[Full Text] [PDF]
E. M. Szego, K. Barabas, J. Balog, N. Szilagyi, K. S. Korach, G. Juhasz, and I. M. Abraham
Estrogen Induces Estrogen Receptor {alpha}-Dependent cAMP Response Element-Binding Protein Phosphorylation via Mitogen Activated Protein Kinase Pathway in Basal Forebrain Cholinergic Neurons In Vivo
J. Neurosci., April 12, 2006; 26(15): 4104 - 4110.
[Abstract] [Full Text] [PDF]
J. Hao, P. R. Rapp, A. E. Leffler, S. R. Leffler, W. G. M. Janssen, W. Lou, H. McKay, J. A. Roberts, S. L. Wearne, P. R. Hof, et al.
Estrogen Alters Spine Number and Morphology in Prefrontal Cortex of Aged Female Rhesus Monkeys
J. Neurosci., March 1, 2006; 26(9): 2571 - 2578.
[Abstract] [Full Text] [PDF]
C. C. Smith and L. L. McMahon
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., August 24, 2005; 25(34): 7780 - 7791.
[Abstract] [Full Text] [PDF]
V. A. Ledoux and C. S. Woolley
Evidence That Disinhibition Is Associated with a Decrease in Number of Vesicles Available for Release at Inhibitory Synapses
J. Neurosci., January 26, 2005; 25(4): 971 - 976.
[Abstract] [Full Text] [PDF]
O. Kretz, L. Fester, U. Wehrenberg, L. Zhou, S. Brauckmann, S. Zhao, J. Prange-Kiel, T. Naumann, H. Jarry, M. Frotscher, et al.
Hippocampal Synapses Depend on Hippocampal Estrogen Synthesis
J. Neurosci., June 30, 2004; 24(26): 5913 - 5921.
[Abstract] [Full Text] [PDF]
H. E. Scharfman, T. C. Mercurio, J. H. Goodman, M. A. Wilson, and N. J. MacLusky
Hippocampal Excitability Increases during the Estrous Cycle in the Rat: A Potential Role for Brain-Derived Neurotrophic Factor
J. Neurosci., December 17, 2003; 23(37): 11641 - 11652.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|