Journal of Neuroscience, Vol 15, 1891-1911, Copyright © 1995 by Society for Neuroscience
Monoamines and nitric oxide are employed by afferents engaged in midline thalamic regulation
K Otake and DA Ruggiero
Department of Neurology and Neuroscience, Cornell University Medical College, New York, New York 10021.
The neurochemical identities of afferents to the midline thalamus were
investigated in chloral hydrate-anesthetized adult Sprague-Dawley rats. The
retrograde tracers, FluoroGold or cholera toxin B subunit, were centered on
the paraventricular thalamic nucleus (n.Pvt), a periventricular member of
the diffuse thalamocortical projection system that is reciprocally linked
with visceral areas of cerebral cortex and implicated in food intake and
addictive behavior. Tissues were processed with antisera raised against
5-HT, the catecholamine- synthesizing enzymes, tyrosine hydroxylase or
phenylethanolamine N- methyltransferase or the cholinergic anabolic enzyme,
ChAT. Serotonergic afferents principally derive from dorsal and median
constituents of the mesopontine raphe. Previously unrecognized sources of
catecholaminergic afferents were detected. Adrenergic afferents were traced
to neurons in the C1 and C3 areas of rostral medullary reticular formation
and periventricular gray, respectively, and the C2 area corresponding to
the dorsal general viscerosensory field of nucleus tractus solitarii.
Noradrenergic afferents arise principally from neurons in the locus
ceruleus and A5 area. Dopaminergic projections to the n.Pvt derive from the
A14, A13 and A11 cell groups in diencephalon. Afferents presumed to
generate nitric oxide (NO) as a diffusible membrane-permeant transcellular
signal were detected by processing retrogradely labeled tissues
histochemically for NADPH-diaphorase, a molecule associated with nitric
oxide synthase. NO in the n.Pvt is generated predominantly by
noncholinergic neurons in the lateral hypothalamic area and mesopontine
tegmentum. In striking contrast, extensive interactions were predicted
between NO and ACh in the central medial and other loci in the
nondiscriminative thalamus. We conclude that the n.Pvt is a site of
interaction of NO and monoaminergic afferents derived from nuclei
implicated in sensory gating, regulation of electrocortical neural activity
and behavior. Taken collectively, our data predict that the labile
transcellular messenger NO may enable structurally differentiated subnuclei
of the diffuse thalamocortical projection system to act in concert as a
functionally unified unit.