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Journal of Neuroscience, Vol 13, 660-673, Copyright © 1993 by Society for Neuroscience

ARTICLE

Modal gating of Na+ channels as a mechanism of persistent Na+ current in pyramidal neurons from rat and cat sensorimotor cortex

C Alzheimer, PC Schwindt and WE Crill
Department of Physiology and Biophysics, School of Medicine, University of Washington, Seattle 98195.

The kinetic behavior of brain Na+ channels was studied in pyramidal cells from rat and cat sensorimotor cortex using either the thin slice preparation or acutely isolated neurons. Single-channel recordings were obtained in the cell-attached and inside-out configuration of the patch- clamp technique. Na+ channels had a conductance of about 16 pS. Patches always contained several Na+ channels, usually 4-12. In both preparations, long depolarizing pulses revealed two distinct patterns of late Na+ channel activity following transient openings. (1) Na+ channels displayed sporadic brief late openings sometimes clustered to "minibursts" of 10-40 msec. These events occurred at a low frequency, yielding open probability (NPo) values below 0.01 (mean = 0.0034). (2) In the second gating mode, an individual Na+ channel in the patch failed to inactivate and produced a burst of openings often lasting to the end of the pulse. This behavior was observed in about 1% of depolarizations. Shifts to the bursting mode were usually confined to a single 400 msec pulse, but rarely occurred during two or more consecutive pulses applied at 2 sec intervals. Sustained bursts did not require preceding transient openings to occur since they were also observed during slow depolarizing voltage ramps. The similar incidence of inactivation failures in cell-attached versus inside-out recordings suggests that the bursting mode is a property of the channel and/or adjacent membrane-bound structures. Calculations indicate that brief late openings and rare sustained bursts suffice to generate a small but significant whole-cell current. Since the Na+ channels mediating early, brief late, and sustained openings were identical in terms of their elementary electrical properties, we propose that the fast and the persistent Na+ currents of cortical pyramidal cells are generated by an electrophysiologically uniform population of Na+ channels that can individually switch between different gating modes.


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I. Lampl, P. Schwindt, and W. Crill
Reduction of Cortical Pyramidal Neuron Excitability by the Action of Phenytoin on Persistent Na+ Current
J. Pharmacol. Exp. Ther., January 1, 1998; 284(1): 228 - 237.
[Abstract] [Full Text]

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 J. Neurophysiol.Home page
C.M.A. Pennartz, M. A. Bierlaagh, and A.M.S. Geurtsen
Cellular Mechanisms Underlying Spontaneous Firing in Rat Suprachiasmatic Nucleus: Involvement of a Slowly Inactivating Component of Sodium Current
J Neurophysiol, October 1, 1997; 78(4): 1811 - 1825.
[Abstract] [Full Text] [PDF]

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 J. Neurophysiol.Home page
D. Golomb and Y. Amitai
Propagating Neuronal Discharges in Neocortical Slices: Computational and Experimental Study
J Neurophysiol, September 1, 1997; 78(3): 1199 - 1211.
[Abstract] [Full Text] [PDF]

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 J. Neurophysiol.Home page
T. Mittmann, S. M. Linton, P. Schwindt, and W. Crill
Evidence for Persistent Na+ Current in Apical Dendrites of Rat Neocortical Neurons From Imaging of Na+-Sensitive Dye
J Neurophysiol, August 1, 1997; 78(2): 1188 - 1192.
[Abstract] [Full Text] [PDF]

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M. M. Segal and A. F. Douglas
Late Sodium Channel Openings Underlying Epileptiform Activity Are Preferentially Diminished by the Anticonvulsant Phenytoin
J Neurophysiol, June 1, 1997; 77(6): 3021 - 3034.
[Abstract] [Full Text] [PDF]

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M. D. Baker and H. Bostock
Low-Threshold, Persistent Sodium Current in Rat Large Dorsal Root Ganglion Neurons in Culture
J Neurophysiol, March 1, 1997; 77(3): 1503 - 1513.
[Abstract] [Full Text] [PDF]

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J. C. Callaway and W. N. Ross
Spatial Distribution of Synaptically Activated Sodium Concentration Changes in Cerebellar Purkinje Neurons
J Neurophysiol, January 1, 1997; 77(1): 145 - 152.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
D. Jaeger, E. De Schutter, and J. M. Bower
The Role of Synaptic and Voltage-Gated Currents in the Control of Purkinje Cell Spiking: A Modeling Study
J. Neurosci., January 1, 1997; 17(1): 91 - 106.
[Abstract] [Full Text] [PDF]

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 ScienceHome page
J. Magee and D Johnston
Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons
Science, April 14, 1995; 268(5208): 301 - 304.
[Abstract] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
I. Timofeev, F. Grenier, and M. Steriade
Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: An intracellular study
PNAS, February 13, 2001; 98(4): 1924 - 1929.
[Abstract] [Full Text] [PDF]


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