Voltage-Gated Potassium Channels Activated During Action Potentials in Layer V Neocortical Pyramidal Neurons

Jian Kang, John R. Huguenard, David A. Prince
2000 Journal of Neurophysiology  
Voltagegated 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 ϩ 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 ϩ channel with a conductance
more » ... with a conductance of 37 pS (K f ) opened briefly during AP repolarization. Activation of K f channels also was triggered by patch depolarization and did not require Ca 2ϩ influx. Activation threshold was about Ϫ20 mV and inactivation was voltage dependent. Mean duration of channel activities after single APs was 6.1 Ϯ 0.6 ms (mean Ϯ SD) at resting membrane potential (Ϫ64 mV), 6.7 Ϯ 0.7 ms at Ϫ54 mV, and 62 Ϯ 15 ms at Ϫ24 mV. The activation and inactivation properties suggest that K f channels function mainly in AP repolarization but not in regulation of firing. K f channels were sensitive to a low concentration of tetraethylammonium (TEA, 1 mM) but not to charybdotoxin (ChTX, 100 nM). Activities of A-type channels (K A ) also were observed during AP repolarization. K A channels were activated by depolarization with a threshold near Ϫ45 mV, suggesting that K A channels function in both repolarization and timing of APs. Inactivation was voltage dependent with decay time constants of 32 Ϯ 6 ms at Ϫ64 mV (rest), 112 Ϯ 28 ms at Ϫ54 mV, and 367 Ϯ 34 ms at Ϫ24 mV. K A 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 ϩ channel (K dr ) with a unique conductance of 17 pS was recorded from cell-attached patches with TEA/4-APfilled pipettes. K dr channels were activated by depolarization with a threshold near Ϫ25 mV and showed delayed long-lasting activation. K dr channels were not activated by single action potentials. Large conductance Ca 2ϩ -activated K ϩ (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 ϩ channels during action potentials in layer V neocortical pyramidal neurons. K f and K A channels contribute to AP repolarization, while K A channels also regulate repetitive firing. K dr channels also may function in regulating repetitive firing, whereas BK channels appear to be activated only in pathological conditions. I N T R O D U C T I O N Voltage-gated potassium channels play a major role in neuronal action potential (AP) repolarization and repetitive firing (Connor and Stevens 1971a; Hille 1992; Hodgkin and Huxley Address for reprint requests: J. Kang,
doi:10.1152/jn.2000.83.1.70 pmid:10634854 fatcat:lj6n74syrfc2rfeh75bbc2szoa