Calcium activates two types of potassium channels in rat hippocampal neurons in culture

Several calcium-dependent potassium currents can contribute to the electrophysiological properties of neurons. In hippocampal pyramidal cells, 2 afterhyperpolarizations (AHPs) are mediated by different calcium-activated potassium currents. First, a rapidly activated current contributes to action-potential repolarization and the fast AHP following individual action potentials. In addition, a slowly developing current underlies the slow AHP, which occurs after a burst of action potentials and contributes substantially to the spike- frequency accommodation observed in these cells during a prolonged depolarizing current pulse. In order to investigate the single Ca2(+)- dependent channels that might underlie these currents, we performed patch-clamp experiments on hippocampal neurons in primary culture. When excised inside-out patches were exposed to 1 microM Ca2+, 2 types of channel activity were observed. In symmetrical bathing solutions containing 140 mM K+, the channels had conductances of 19 pS and 220 pS, and both were permeable mainly to potassium ions. The properties of these 2 channels differed in a number of ways. At negative membrane potentials, the small-conductance channels were more sensitive to Ca2+ than the large channels. At positive potentials, the small-conductance channels displayed a flickery block by Mg2+ ions on the cytoplasmic face of the membrane. Low concentrations of tetraethylammonium (TEA) on the extracellular face of the membrane specifically caused an apparent reduction of the large-channel conductance. The properties of the large- and small-conductance channels are in accord with those of the fast and slow AHP, respectively.

[1]  N. Akaike,et al.  Delayed activation of large-conductance Ca2+-activated K channels in hippocampal neurons of the rat. , 1989, Biophysical journal.

[2]  F Franciolini,et al.  Calcium and voltage dependence of single Ca2+-activated K+ channels from cultured hippocampal neurons of rat. , 1988, Biochimica et biophysica acta.

[3]  N. Standen,et al.  The action of external tetraethylammonium ions on unitary delayed rectifier potassium channels of frog skeletal muscle. , 1987, The Journal of physiology.

[4]  J. W. Goh,et al.  Pharmacological and physiological properties of the after‐hyperpolarization current of bullfrog ganglion neurones. , 1987, The Journal of physiology.

[5]  T. Smart Single calcium‐activated potassium channels recorded from cultured rat sympathetic neurones. , 1987, The Journal of physiology.

[6]  R. Nicoll,et al.  Properties of two calcium‐activated hyperpolarizations in rat hippocampal neurones. , 1987, The Journal of physiology.

[7]  B. Lancaster,et al.  Potassium currents evoked by brief depolarizations in bull‐frog sympathetic ganglion cells. , 1987, Journal of Physiology.

[8]  A. Constanti,et al.  Calcium‐dependent potassium conductance in guinea‐pig olfactory cortex neurones in vitro. , 1987, The Journal of physiology.

[9]  A. Noma,et al.  Voltage‐dependent magnesium block of adenosine‐triphosphate‐sensitive potassium channel in guinea‐pig ventricular cells. , 1987, The Journal of physiology.

[10]  F. Alvarez-Leefmans,et al.  Intracellular free magnesium in excitable cells: its measurement and its biologic significance. , 1987, Canadian journal of physiology and pharmacology.

[11]  A. K. Ritchie Two distinct calcium‐activated potassium currents in a rat anterior pituitary cell line. , 1987, The Journal of physiology.

[12]  J. Storm,et al.  Action potential repolarization and a fast after‐hyperpolarization in rat hippocampal pyramidal cells. , 1987, The Journal of physiology.

[13]  C. Vandenberg Inward rectification of a potassium channel in cardiac ventricular cells depends on internal magnesium ions. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Peter C. Jordan,et al.  How pore mouth charge distributions alter the permeability of transmembrane ionic channels. , 1987, Biophysical journal.

[15]  H. Irisawa,et al.  Ohmic conductance through the inwardly rectifying K channel and blocking by internal Mg2+ , 1987, Nature.

[16]  P. Adams,et al.  A method for the rapid exchange of solutions bathing excised membrane patches. , 1986, Biophysical journal.

[17]  K. Magleby,et al.  Single apamin-blocked Ca-activated K+ channels of small conductance in cultured rat skeletal muscle , 1986, Nature.

[18]  N. Hussy,et al.  Time course of Ca and Ca-dependent K currents during molluscan nerve cell action potentials , 1986, Neuroscience Letters.

[19]  P. Adams,et al.  Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons. , 1986, Journal of neurophysiology.

[20]  J. Barker,et al.  Voltage-clamp analysis of a Ca2+- and voltage-dependent chloride conductance in cultured mouse spinal neurons. , 1986, Journal of neurophysiology.

[21]  M. Watanabe,et al.  Blockade of Ca‐activated K conductance by apamin in rat sympathetic neurones , 1986, British journal of pharmacology.

[22]  C. Bader,et al.  Sodium-activated potassium current in cultured avian neurones , 1985, Nature.

[23]  R. Nicoll,et al.  Two distinct Ca-dependent K currents in bullfrog sympathetic ganglion cells. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[24]  R. Nicoll,et al.  Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. , 1984, The Journal of physiology.

[25]  G. Yellen Ionic permeation and blockade in Ca2+-activated K+ channels of bovine chromaffin cells , 1984, The Journal of general physiology.

[26]  K. Magleby,et al.  Ion conductance and selectivity of single calcium-activated potassium channels in cultured rat muscle , 1984, The Journal of general physiology.

[27]  M. Lazdunski,et al.  The coexistence in rat muscle cells of two distinct classes of Ca2+-dependent K+ channels with different pharmacological properties and different physiological functions. , 1984, Biochemical and biophysical research communications.

[28]  K L Magleby,et al.  Calcium dependence of open and shut interval distributions from calcium‐activated potassium channels in cultured rat muscle. , 1983, The Journal of physiology.

[29]  D. A. Brown,et al.  Calcium‐activated outward current in voltage‐clamped hippocampal neurones of the guinea‐pig. , 1983, The Journal of physiology.

[30]  K L Magleby,et al.  Properties of single calcium‐activated potassium channels in cultured rat muscle , 1982, The Journal of physiology.

[31]  H Lecar,et al.  Single calcium-dependent potassium channels in clonal anterior pituitary cells. , 1982, Biophysical journal.

[32]  D. A. Brown,et al.  Intracellular Ca2+ activates a fast voltage-sensitive K+ current in vertebrate sympathetic neurones , 1982, Nature.

[33]  E. Neher,et al.  Inward current channels activated by intracellular Ca in cultured cardiac cells , 1981, Nature.

[34]  K. Magleby,et al.  Single channel recordings of Ca2+-activated K+ currents in rat muscle cell culture , 1981, Nature.

[35]  A. Marty,et al.  Ca-dependent K channels with large unitary conductance in chromaffin cell membranes , 1981, Nature.

[36]  E. Neher,et al.  Local anaesthetics transiently block currents through single acetylcholine‐receptor channels. , 1978, The Journal of physiology.

[37]  M. Endo,et al.  Calcium Induced Release of Calcium from the Sarcoplasmic Reticulum of Skinned Skeletal Muscle Fibres , 1970, Nature.

[38]  F. F. Weight,et al.  Detection of intracellular Ca2+ transients in sympathetic neurones using arsenazo III , 1983, Nature.