The Journal of Neuroscience, April 1, 2000, 20(7):2731-2741
Progressive Postnatal Assembly of Limbic-Autonomic Circuits
Revealed by Central Transneuronal Transport of Pseudorabies Virus
Linda
Rinaman1,
Pat
Levitt2, and
J. Patrick
Card1
1 Department of Neuroscience, University of Pittsburgh,
Pittsburgh, Pennsylvania 15260, and 2 Department of
Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh,
Pennsylvania 15260
The development of neuronal projections to a target and the
establishment of synaptic connections with that target can be temporally distinct events, which typically are distinguished by
functional assessments. We have applied a novel neuroanatomical approach to characterize the development of limbic forebrain synaptic inputs to autonomic neurons in neonatal rats. Transneuronal labeling of
preautonomic forebrain neurons was achieved by inoculating the ventral
stomach wall with pseudorabies virus (PRV) on postnatal day 1 (P1), P4,
or P8. In each age group, PRV-positive neurons were present in
autonomic and preautonomic regions of the spinal cord and brainstem
62-64 hr after inoculation. Transneuronal forebrain labeling in rats
injected on P8 was similar to the transneuronal labeling reported
previously in adult rats and included neurons in the medial and lateral
hypothalamus, amygdala, bed nucleus of the stria terminalis, and
visceral cortices. However, no cortex labeling and only modest amygdala
and bed nucleus labeling were observed in rats injected with PRV on P4,
and only medial hypothalamic labeling was observed in rats injected on
P1. Additional tracing experiments involving central injections of PRV
or cholera toxin 
indicated that lateral hypothalamic and
telencephalic regions projected to the medullary dorsal vagal complex
several days before establishing synaptic connections with
gastric-related autonomic neurons. These results demonstrate a novel
strategy for evaluating synaptic connectivity in developing neural
circuits and show a temporally segregated postnatal emergence of medial
hypothalamic, lateral hypothalamic, and telencephalic synaptic inputs
to central autonomic neurons.
Key words:
development; sympathetic; parasympathetic; lateral
hypothalamic area; paraventricular nucleus of the hypothalamus; central
nucleus of the amygdala; bed nucleus of the stria terminalis; insular
cortex; medial prefrontal cortex; dorsal motor nucleus of the vagus; nucleus of the solitary tract; stomach; gastrointestinal
Copyright © 2000 Society for Neuroscience 0270-6474/00/2072731-11$05.00/0
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