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Journal of Neuroscience, Vol 14, 4998-5010, Copyright © 1994 by Society for Neuroscience
Pathway-specific variants of AMPA receptors and their contribution to neuronal signaling
IM Raman, S Zhang and LO Trussell
Neuroscience Training Program, University of Wisconsin-Madison 53706.
Neurons of the nucleus magnocellularis (nMAG) of the chick express AMPA
(alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionate) receptors
displaying unusually rapid kinetics of desensitization (Raman and Trussell,
1992a). To investigate whether fast AMPA receptors are present in other
auditory neurons, we compared the properties of AMPA receptors in auditory
as well as nonauditory cells. These included neurons of nMAG, the nucleus
angularis, the nucleus laminaris, the cochlear ganglion, the Purkinje cell
layer of the cerebellum, the ventral horn of the spinal cord, and the
brainstem nucleus of the glossopharyngeal nerve (ncIX). Rapid application
of glutamate to voltage-clamped outside-out membrane patches indicated that
AMPA receptors in the four types of auditory cells had significantly faster
kinetics of desensitization than did the three types of nonauditory
neurons. Channel kinetics in auditory (nMAG) and nonauditory (ncIX) cells
were also compared by means of spectral analysis and the time course of
current deactivation upon removal of glutamate. Both techniques revealed a
burst duration for nMAG channels of 400-500 musec at room temperature, two
to three times shorter than for ncIX cells. Single channels in nMAG had a
burst duration of 550 musec and an open time of approximately 150 musec.
Miniature excitatory postsynaptic currents of brainstem auditory neurons in
slices were also brief, with decay constants of 150-250 musec at 29-32
degrees C. We demonstrated that the fast kinetics of this AMPA receptor are
physiologically important, since cyclothiazide, which reduces
desensitization and prolongs synaptic currents, doubled the relative
refractory period of orthodromic spikes in nMAG cells in brain slices. We
conclude that auditory brainstem neurons express a specialized subtype of
AMPA receptors. This "fast" AMPA receptor may be useful in transmitting
signals necessary for sound localization.
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