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Journal of Neuroscience, Vol 12, 278-289, Copyright © 1992 by Society for Neuroscience
Cellular mechanisms underlying cholinergic and noradrenergic modulation of neuronal firing mode in the cat and guinea pig dorsal lateral geniculate nucleus
DA McCormick
Section of Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06510.
The functional properties, ionic basis, and possible convergence and
interaction of postsynaptic actions mediated by muscarinic and alpha 1-
adrenergic receptors were examined in cat and guinea pig dorsal lateral
geniculate (LGNd) neurons maintained in thalamic slices in vitro. The
possible involvement of GTP-binding proteins was also examined.
Extracellular recordings from cat LGNd revealed the presence of two
subpopulations of neurons. The most prevalent generated rhythmic high-
frequency (300-500 Hz) bursts of two to six action potentials each, with an
interburst frequency of 1-3 Hz. Intracellular recordings revealed that this
activity is typical of thalamocortical relay cells in the apparent absence
of neuromodulatory input. Application of ACh or noradrenaline (NA) to
rhythmically oscillating neurons in the cat LGNd resulted in cessation of
this activity followed by the appearance of single spike firing.
Intracellular recordings revealed that this change in firing mode was
associated with a depolarization of the neuron out of the range of
intrinsic rhythmic oscillation and into or near the single spike firing
mode. The voltage characteristics of the current underlying the cholinergic
and noradrenergic slow depolarization were investigated in guinea pig LGNd
neurons. Application of the muscarinic agonist acetyl-beta-methylcholine
(MCh) to presumed relay neurons resulted in a hyperpolarization due to the
activation of an outward K+ current. This response was followed by a slow
depolarization due to reduction of a relatively non-voltage-dependent
potassium current distinct from IM and IAHP. Application of NA resulted in
a slow depolarization that was also associated with reduction of this
relatively linear K+ current. The MCh- and NA-induced slow depolarizations
displayed the property of occlusion, indicating convergence of action.
However, these responses were mediated by pharmacologically distinct
receptors since the MCh-induced reduction in K+ current was blocked by
scopolamine while that induced by NA was blocked by the alpha
1-adrenoceptor antagonist prazosin. Intracellular diffusion of GTP-gamma-S
resulted in the inward current responses to NA and MCh being irreversible,
suggesting the possible involvement of a G- protein. Prior exposure to
pertussis toxin did not affect the inward current response to NA and MCh,
while the outward K+ current responses induced by application of MCh or the
GABAB agonist baclofen were blocked. These results reveal that activation
of muscarinic or alpha 1- adrenergic postsynaptic receptors in the LGNd
result in a shift in firing mode from rhythmic oscillation to tonic single
spike activity through a decrease in a relatively linear K+ current
mediated through a pertussis toxin-insensitive G-protein.(ABSTRACT
TRUNCATED AT 400 WORDS)
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