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The Journal of Neurophysiology Vol. 83 No. 1 January 2000, pp. 70-80
Copyright ©2000 by the American Physiological Society
1Department of Cell Biology and Anatomy, New York Medical College, Valhalla, New York 10595; and 2Department of Neurology and Neurological Sciences, Stanford University, Stanford, California 94305
Kang, Jian,
John R. Huguenard, and
David A. Prince.
Voltage-Gated Potassium Channels Activated During Action
Potentials in Layer V Neocortical Pyramidal Neurons. J. Neurophysiol. 83: 70-80, 2000. To investigate
voltage-gated potassium channels underlying action potentials (APs), we
simultaneously recorded neuronal APs and single K+ channel
activities, using dual patch-clamp recordings (1 whole cell and 1 cell-attached patch) in single-layer V neocortical pyramidal neurons of
rat brain slices. A fast voltage-gated K+ channel with a
conductance of 37 pS (Kf) opened briefly during AP
repolarization. Activation of Kf channels also was
triggered by patch depolarization and did not require Ca2+
influx. Activation threshold was about 
20 mV and inactivation was
voltage dependent. Mean duration of channel activities after single APs
was 6.1 ± 0.6 ms (mean ± SD) at resting membrane
potential (64 mV), 6.7 ± 0.7 ms at 54 mV, and 62 ± 15 ms at 24 mV. The activation and inactivation properties suggest that
Kf channels function mainly in AP repolarization but not in
regulation of firing. Kf channels were sensitive to a low
concentration of tetraethylammonium (TEA, 1 mM) but not to
charybdotoxin (ChTX, 100 nM). Activities of A-type channels
(KA) also were observed during AP repolarization. KA channels were activated by depolarization with a
threshold near 45 mV, suggesting that KA channels
function in both repolarization and timing of APs. Inactivation was
voltage dependent with decay time constants of 32 ± 6 ms at 64
mV (rest), 112 ± 28 ms at 54 mV, and 367 ± 34 ms at 24
mV. KA channels were localized in clusters and were
characterized by steady-state inactivation, multiple subconductance
states (36 and 19 pS), and inhibition by 5 mM 4-aminopyridine (4-AP)
but not by 1 mM TEA. A delayed rectifier K+ channel
(Kdr) with a unique conductance of 17 pS was recorded from
cell-attached patches with TEA/4-AP-filled pipettes. Kdr channels were activated by depolarization with a threshold near 25 mV
and showed delayed long-lasting activation. Kdr channels were not activated by single action potentials. Large conductance Ca2+-activated K+ (BK) channels were not
triggered by neuronal action potentials in normal slices and only
opened as neuronal responses deteriorated (e.g., smaller or absent
spikes) and in a spike-independent manner. This study provides direct
evidence for different roles of various K+ channels during
action potentials in layer V neocortical pyramidal neurons.
Kf and KA channels contribute to AP
repolarization, while KA channels also regulate repetitive
firing. Kdr channels also may function in regulating
repetitive firing, whereas BK channels appear to be activated only in
pathological conditions.
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