Premium
Large conductance Ca(2+)‐activated K+ channels are involved in both spike shaping and firing regulation in Helix neurones.
Author(s) -
Crest M,
Gola M
Publication year - 1993
Publication title -
the journal of physiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.802
H-Index - 240
eISSN - 1469-7793
pISSN - 0022-3751
DOI - 10.1113/jphysiol.1993.sp019676
Subject(s) - biophysics , voltage clamp , chemistry , conductance , patch clamp , current clamp , calcium , depolarization , electrophysiology , ion channel , helix pomatia , voltage dependent calcium channel , membrane potential , neuroscience , biology , biochemistry , physics , snail , receptor , ecology , organic chemistry , condensed matter physics
1. The role of BK‐type calcium‐dependent K+ channels (K+Ca) in cell firing regulation was evaluated by performing whole‐cell voltage clamp and patch clamp experiments on the U cell neurones in the snail Helix pomatia. These cells were selected because most of the repolarizing K+ current flowed through K+Ca channels. 2. U cells generated overshooting Ca(2+)‐dependent spikes in Na(+)‐free saline. In response to prolonged depolarizing current, they fired a limited number of spikes of decreasing amplitude, and behaved like fast‐adapting or phasic neurones. 3. Under voltage clamp conditions, the K+Ca current had a slow onset at voltages that induced small Ca2+ entries. By manipulating the Ca2+ entry (either with appropriate voltage programmes or by changing the Ca2+ content of the bath), the K+Ca channel opening was found to be rate limited by the Ca2+ binding step and not by the voltage‐dependent conformational change to the open state. 4. Despite the slow activation rate observed in voltage‐clamped cells, 25‐30% of the available K+Ca current was found to be active during isolated spikes. These data were based on patch clamp, spike‐like voltage clamp and hybrid current clamp‐voltage clamp experiments. 5. The fact that spikes led the slowly rising K+Ca current to shift into a fast activating mode was accounted for by the large surge of Ca2+ current concomitant with spike upstroke. The early calcium surge resulted in local increases in cytosolic calcium, which speeded up the binding of calcium ions to the closed K+Ca channels. From changes in the null Ca2+ current voltage, it was calculated that the submembrane [Ca2+]i increase to 50‐80 microM during the spike. 6. Due to their fast voltage dependence, K+Ca channels appeared to play no role in shaping the interspike trajectory. 7. Even in the fast activating mode, the K+Ca current had a finite rate of rise and was not involved in repolarizing short duration Na(+‐dependent action potentials. The current became more and more active, however, when voltage‐gated K+ channels were progressively inactivated during firing. 8. The fast adaptation exhibited by U cells upon sustained depolarization was not paralleled by a recruitment of K+Ca channels because of the cumulative Ca2+ entries. During a spike burst, the K+Ca current progressively overlapped the depolarizing Ca2+ current, which ultimately stopped the firing. The early opening of K+Ca channels was ascribed to residual Ca2+ accumulation that kept part of the channels in the Ca(2+)‐bound state ready to be opened quickly by cell depolarization.(ABSTRACT TRUNCATED AT 400 WORDS)