The Journal of Neurophysiology Vol. 78 No. 5 November 1997, pp. 2309-2320
Copyright ©1997 The American Physiological Society

Three Kinetically Distinct Ca²⁺-Independent Depolarization-Activated K⁺ Currents in Callosal-Projecting Rat Visual Cortical Neurons

Rachel E. Locke and Jeanne M. Nerbonne

Department of Molecular Biology and Pharmacology, Washington University School of Medicine, St. Louis, Missouri 63110

Locke, Rachel E. and Jeanne M. Nerbonne. Three kinetically distinct Ca²⁺-independent depolarization-activated K⁺ currents in callosal-projecting rat visual cortical neurons. J. Neurophysiol. 78: 2309-2320, 1997. Whole cell, Ca²⁺-independent, depolarization-activated K⁺ currents were characterized in identified callosal-projecting (CP) neurons isolated from postnatal day 7-16 rat primary visual cortex. CP neurons were identified in vitro after in vivo retrograde labeling with fluorescently tagged latex microbeads. During brief (160-ms) depolarizing voltage steps to potentials between 50 and +60 mV, outward K⁺ currents in these cells activate rapidly and inactivate to varying degrees. Three distinct K⁺ currents were separated based on differential sensitivity to 4-aminopyridine (4-AP); these are referred to here as I_A, I_D, and I_K, because their properties are similar (but not identical) K⁺ currents termed I_A, I_D, and I_K in other cells. The current sensitive to high (100 µM) concentrations of 4-AP (I_A) activates and inactivates rapidly; the current blocked completely by low (50 µM) 4-AP (I_D) activates rapidly and inactivates slowly. A slowly activating, slowly inactivating current (I_K) remains in the presence of 5 mM 4-AP. I_A, I_D, and I_K also were separated and characterized in experiments that did not rely on the use of 4-AP. All CP cells express all three K⁺ current types, although the relative densities of I_A, I_D, and I_K vary among cells. The experiments here also have revealed that I_A, I_D, and I_K display similar voltage dependences of activation and steady state inactivation, whereas the kinetic properties of the currents are distinct. At +30 mV, for example, mean ± SD activation s are 0.83 ± 0.24 ms for I_A, 1.74 ± 0.49 ms for I_D, and 14.7 ± 4.0 ms for I_K. Mean ± SD inactivation s for I_A and I_D are 26 ± 7 ms and 569 ± 143 ms, respectively. Inactivation of I_K is biexponential with mean ± SD inactivation time constants of 475 ± 232 ms and 3,128 ± 1,328 ms; ~20% of the 4-AP-insensitive current is noninactivating. For all three components, activation is voltage dependent, increasing with increasing depolarization, whereas inactivation is voltage independent. Both I_A and I_K recover rapidly from steady state inactivation with mean ± SD recovery time constants of 38 ± 7 ms and 79 ± 26 ms, respectively; I_D recovers an order of magnitude more slowly (588 ± 274 ms). The properties of I_A, I_D, and I_K in CP neurons are compared with those of similar currents described previously in other mammalian central neurons and, in the accompanying paper, the roles of these conductances in regulating the firing properties of CP neurons are explored.

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