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* To whom correspondence should be addressed. E-mail: jdisterhoft{at}northwestern.edu.
CA1 pyramidal neurons from animals that have acquired a hippocampus-dependent task show a reduced slow post-burst afterhyperpolarization (slow AHP). To understand the functional significance of this change, we examined and characterized the slow AHP activated by different patterns of synaptic stimuli and its impact on postsynaptic signal integration. Whole cell current-clamp recordings were performed on rat CA1 pyramidal neurons, and trains of stratum radiatum stimuli varying in duration, frequency, and intensity were used to activate the AHP. At -68 mV, a short train of subthreshold stimuli (20 - 150 Hz) generated only the mAHP. In contrast, just two suprathreshold stimuli > 50 Hz triggered a prominent slow AHP sensitive to bath-applications of isoproterenol, carbachol, or intracellularly-applied BAPTA, suggesting that the underlying current is the Ca2+-activated K+ current, the sIAHP. The slow AHP magnitude was positively related to stimulus train duration and frequency, consistent with its dependence on intracellular Ca2+ accumulation for activation. About 20% of neurons recorded did not have a slow AHP. In response to high frequency suprathreshold stimuli, these neurons developed a pronounced afterdepolarization (ADP) and multiple action potential firing. The ADP magnitude increased with successive stimuli, and was positively related to stimulus intensity and frequency. It was sensitive to bath-applications of thapsigargin and nitrendipine, and abolished by d-AP5, indicating that it is supported by intracellular Ca2+ release, the L-type Ca2+ influx, and NMDA receptor-mediated influx. In the presence of d-AP5, we were unable to trigger an ADP with maximal stimulus intensity. Pharmacologically eliminating the slow AHP allowed neurons with a slow AHP to develop an ADP with the original stimulus train. We propose that the slow AHP acts to facilitate Mg2+ re-block of the activated NMDA receptors, thereby reducing temporal summation and preventing an NMDA receptor-dependent ADP during intense synaptic events. Neuromodulation of the slow AHP may thus affect information throughput and regulate NMDA-receptor mediated plasticity.
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