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J Neurophysiol 77: 2373-2384, 1997;
0022-3077/97 $5.00
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The Journal of Neurophysiology Vol. 77 No. 5 May 1997, pp. 2373-2384
Copyright ©1997 The American Physiological Society

Fast and Slow Activation Kinetics of Voltage-Gated Sodium Channels in Molluscan Neurons

William F. Gilly1, Rhanor Gillette2, and Matthew McFarlane1, 3

1 Department of Biological Sciences, Hopkins Marine Station of Stanford University, Pacific Grove, California 93950; 2 Department of Physiology and Biophysics, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801; and 3 Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, California 94305

Gilly, William F., Rhanor Gillette, and Matthew McFarlane. Fast and slow activation kinetics of voltage-gated sodium channels in molluscan neurons. J. Neurophysiol. 77: 2373-2384, 1997. Whole cell patch-clamp recordings of Na current (INa) were made under identical experimental conditions from isolated neurons from cephalopod (Loligo, Octopus) and gastropod (Aplysia, Pleurobranchaea, Doriopsilla) species to compare properties of activation gating. Voltage dependence of peak Na conductance (gNa) is very similar in all cases, but activation kinetics in the gastropod neurons studied are markedly slower. Kinetic differences are very pronounced only over the voltage range spanned by the gNa-voltage relation. At positive and negative extremes of voltage, activation and deactivation kinetics of INa are practically indistinguishable in all species studied. Voltage-dependent rate constants underlying activation of the slow type of Na channel found in gastropods thus appear to be much more voltage dependent than are the equivalent rates in the universally fast type of channel that predominates in cephalopods. Voltage dependence of inactivation kinetics shows a similar pattern and is representative of activation kinetics for the two types of Na channels. Neurons with fast Na channels can thus make much more rapid adjustments in the number of open Na channels at physiologically relevant voltages than would be possible with only slow Na channels. This capability appears to be an adaptation that is highly evolved in cephalopods, which are well known for their high-speed swimming behaviors. Similarities in slow and fast Na channel subtypes in molluscan and mammalian neurons are discussed.




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