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The Journal of Neuroscience, July 16, 2003, 23(15):6338-6344

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Estradiol Regulates the Slow Ca²⁺-Activated K⁺ Current in Hippocampal Pyramidal Neurons

Hugo F. Carrer,¹ Alfonso Araque,² and Washington Buño²

¹Instituto de Investigación Médica M. y M. Ferreyra—Consejo Nacional de Investigaciones Científicas y Técnicas, 5000 Córdoba, Argentina, and ²Instituto Cajal, Consejo Superior de Investigaciones Científicas, Madrid 28001, Spain

The slow Ca²⁺-activated K⁺ current (sI_AHP) was recorded in CA1 pyramidal neurons in hippocampal slices obtained from ovariectomized (OVX) or sham OVX (control) female rats. The sI_AHP was significantly larger in cells from OVX rats than in cells from control rats. Superfusion with 5–100 nM 17-estradiol (E2) caused a progressive decrease in the sI_AHP in cells from OVX rats but not in cells from control rats. In slices from OVX rats injected with 10 µg of E2 24 and 48 hr before they were killed, superfusion with E2 did not modify the sI_AHP. In neurons from OVX rats, but not in neurons from control rats, E2 significantly increased both the number of action potentials and the burst duration generated by depolarizing pulses. The inactive isomer 17-estradiol had no effect. The impermeant protein conjugate E2—BSA was as effective as free E2 at decreasing the sI_AHP. Ca²⁺ spikes were also depressed by E2 in neurons from OVX rats, but not in control rats. A decrease in the intracellular Ca²⁺ signal, correlating with the inhibition of the Ca²⁺ spike and sI_AHP produced by E2, was observed only in neurons from OVX rats. Our results indicate that ovariectomy increases the sI_AHP and depresses excitability, whereas bath application or priming with E2 decreases the sI_AHP, thus promoting excitability. These effects of E2 on the sI_AHP and excitability, which are stereospecific and presumably mediated by membrane-bound receptors, could contribute to the hormonal regulation of synaptic plasticity and epileptiform activity as well as to learning and cognitive abilities dependent on the function of hippocampal neural circuits.

Key words: estradiol; excitability; hyperpolarizing potassium current; calcium-dependent potassium current; calcium signal; hippocampus; estrogen effects

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Received Jan. 13, 2003; revised May. 13, 2003; accepted May. 13, 2003.

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