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Volume 17, Number 17,
Issue of September 1, 1997
pp. 6512-6521
Copyright ©1997 Society for Neuroscience
Slow Recovery from Inactivation of Na+ Channels
Underlies the Activity-Dependent Attenuation of Dendritic Action
Potentials in Hippocampal CA1 Pyramidal Neurons
Received April 11, 1997; revised June 6, 1997; accepted June 11, 1997.
Costa M. Colbert,
Jeffrey C. Magee,
Dax A. Hoffman, and
Daniel Johnston
Division of Neuroscience, Baylor College of Medicine, Houston,
Texas 77030
Na+ action potentials propagate into the
dendrites of pyramidal neurons driving an influx of
Ca2+ that seems to be important for associative
synaptic plasticity. During repetitive (10-50 Hz) firing, dendritic
action potentials display a marked and prolonged voltage-dependent
decrease in amplitude. Such a decrease is not apparent in somatic
action potentials. We investigated the mechanisms of the different
activity dependence of somatic and dendritic action potentials in CA1
pyramidal neurons of adult rats using whole-cell and cell-attached
patch-clamp methods. There were three main findings. First, dendritic
Na+ currents decreased in amplitude when repeatedly
activated by brief (2 msec) depolarizations. Recovery was slow and
voltage-dependent. Second, Na+ currents decreased
much less in somatic than in dendritic patches. Third, although
K+ currents remained constant during trains,
K+ currents were necessary for dendritic action
potential amplitude to decrease in whole-cell experiments. These
results suggest that regional differences in Na+ and
K+ channels determine the differences in the
activity dependence of somatic and dendritic action potential
amplitudes.
Key words:
potassium channels;
modulation;
whole-cell;
cell-attached;
electrophysiology;
rat
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|