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Received March 18, 2005
Revised April 12, 2005
Accepted after revision May 5, 2005
1 Institute of Physiology, University of Oslo
* To whom correspondence should be addressed. E-mail: j.f.storm{at}medisin.uio.no.
In hippocampal pyramidal cells, a single action potential (AP) or a burst of APs is followed by a medium afterhyperpolarization (mAHP, lasting ~0.1 s). The currents underlying the mAHP are considered to regulate excitability and cause early spike frequency adaptation, thus dampening the response to sustained excitatory input relative to responses to abrupt excitation. The mAHP was originally suggested to be primarily caused by M-channels (at depolarized potentials) and h-channels (at more negative potentials), but not SK-channels. In recent reports, however, the mAHP was suggested to be generated mainly by SK-channels or only by h-channels. We have now reexamined the mechanisms underlying the mAHP and early spike frequency adaptation in CA1 pyramidal cells, by using sharp electrode and whole cell recording in rat hippocampal slices. The specific M-channel blocker XE991 (10 µM) suppressed the mAHP following 1-5 APs, evoked by current injection at -60 mV. XE991 also enhanced the excitability of the cell, i.e. increased the number of APs evoked by a constant depolarizing current pulse, reduced their rate of adaptation, enhanced the after-depolarization (ADP) and promoted bursting. Conversely, the M-channel opener retigabine reduced excitability. The h-channel blocker ZD7288 (10 µM) fully suppressed the mAHP at -80 mV, but had little effect at -60 mV, whereas XE991 did not measurably affect the mAHP at -80 mV. Likewise, ZD7288 had little or no effect on excitability or adaptation during current pulses injected from -60 mV, but changed the initial discharge during depolarizing pulses injected from -80 mV. In contrast to previous reports, we found that blockade of calcium-activated K+ channels of the SK/KCa2 type by apamin (100-400 nM) failed to affect the mAHP or adaptation. A computational model of a CA1 pyramidal cell predicted that M- and h-channels will generate mAHPs in a voltage-dependent manner, as indicated by the experiments. We conclude that M- and h-channels generate the somatic mAHP in hippocampal pyramidal cells, with little or no net contribution from SK channels.
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