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Journal of Neuroscience, Vol 15, 4449-4463, Copyright © 1995 by Society for Neuroscience
Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons
ES Nisenbaum and CJ Wilson
Department of Anatomy and Neurobiology, College of Medicine, University of Tennessee-Memphis 38163, USA.
Many of the nonlinear membrane properties displayed by neostriatal spiny
projection neurons are conferred by their voltage-gated potassium (K+)
currents, including an inwardly rectifying current (IKir), fast (IAt), and
slowly (IAs)-inactivating A-currents, and a slow, noninactivating current.
The relative contribution of these K+ currents to the pronounced inward and
outward rectification of the current- voltage (I-V) relationship of spiny
neurons was investigated in a neostriatal slice preparation. Manipulation
of the equilibrium potential for K+ (EK) showed that the voltage dependence
of activation of inward rectification was identical to that of IKir. In
addition, application of barium (100 microM), which is known to reduce IKir
in a time- and voltage-dependent manner, had equivalent effects on inward
rectification. Subsequent application of cesium (3 mM) or
tetraethylammonium (TEA, 25 mM) blocked inward rectification in a solely
voltage-dependent fashion consistent with the action of these blockers on
IKir. Administration of 4-aminopyridine (4-AP, 100 microM) at
concentrations that selectively depress IAs, reduced outward rectification
of spiny neurons at subthreshold membrane potentials. Higher concentrations
of 4-AP (2 mM), which block both IAs and IAt, revealed an early transient
overshoot in voltage deflections at potentials near spike threshold, but
rectification persisted at the end of the responses. The transient
overshoot and the residual rectification were eliminated by TEA (25 mM), a
blocker of the slow, noninactivating K+ current. Collectively, these
results indicate that all three depolarization-activated K+ currents
contribute to outward rectification at different times and membrane
potentials defined by their voltage dependence of activation and kinetics
of inactivation. The spontaneous activity of neostriatal spiny neurons
recorded in intact animals is characterized by sustained and limited shifts
in membrane potential from relatively hyperpolarized potentials to
depolarized potentials near spike threshold. The present data suggest that
the hyperpolarized state is determined principally by IKir and the limits
on the depolarized state are defined by IAf, IAs, and the noninactivating
current. These outward K+ currents also are hypothesized to govern the
spike discharge characteristics once the depolarized state has been
reached.
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