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Journal of Neuroscience, Vol 11, 3188-3199, Copyright © 1991 by Society for Neuroscience
Modulation of neuronal firing mode in cat and guinea pig LGNd by histamine: possible cellular mechanisms of histaminergic control of arousal
DA McCormick and A Williamson
Section of Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06510.
The thalamus is innervated by histaminergic fibers presumably arising from
neurons in the tuberomammillary nucleus of the hypothalamus. The possible
function of this histaminergic projection was addressed through
investigation of the cellular actions of histamine on guinea pig and cat
dorsal lateral geniculate (LGNd) relay neurons maintained as a slice in
vitro. Local application of histamine to LGNd relay neurons resulted in a
slow depolarization that was associated with a decrease in membrane
conductance and was blocked by the H1-antagonists pyrilamine, triprolidine,
or diphenhydramine. Current versus voltage relationships revealed that the
slow depolarization was associated with an inward current that reversed
near EK, indicating that it was due to a decrease in a potassium current.
The slow depolarizing response to histamine was occluded by maximal
activation of the slow depolarizing responses resulting from stimulation of
alpha 1-adrenergic or muscarinic receptors, suggesting that they are all
mediated by reduction in the same potassium current and/or alteration of a
common second messenger. In the presence of H1-receptor antagonists,
application of histamine resulted in a small depolarization that was
associated with a marked increase in apparent membrane conductance.
Voltage-clamp recordings revealed that this response was associated with
enhancement of the hyperpolarization-activated cation current Ih. This
response to histamine was blocked by local or bath application of the
H2-antagonists cimetidine or tiotidine. The functional consequences of
these actions of histamine were addressed with extracellular and
intracellular recordings in guinea pig and cat LGNd relay neurons.
Extracellular recordings in cat LGNd revealed the occurrence of highly
regular 1-4 Hz rhythmic burst discharges. Application of histamine halted
rhythmic bursting and replaced it with a prolonged period of single-spike
activity. Intracellular recordings indicate that the histamine-induced
switch in firing mode is due largely to the slow depolarizing response
mediated by H1-receptors, but is also facilitated by the enhancement of Ih
mediated by H2-receptors. These postsynaptic actions indicate that
increased activity in the tuberomammillary histaminergic system may result
in a switch of thalamic neuronal activity from rhythmic burst firing to
single-spike activity and thereby promote the accurate transmission and
processing of sensory information and cognition.
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