Substance P-immunoreactive peripheral branches of sensory neurons innervate guinea pig sympathetic neurons

Abstract

The presence of substance P-immunoreactive (SPI) varicose nerve networks and nerve fiber bundles in guinea pig prevertebral sympathetic ganglia has been confirmed by fluorescence immunohistochemistry. No SPI neurons have been found in sympathetic ganglia, including lumbar paravertebral ganglia. Peroxidase-antiperoxidase immunocytochemical methods have shown that SPI nerve terminal varicosities in the inferior mesenteric ganglion (IMG) form morphologically identifiable synapses on dendritic shafts. Cutting the intermesenteric nerve produces no obvious change in SP immunoreactivity in the IMG; cutting the lumbar splanchnic nerves produces nearly total depletion which becomes virtually complete if the two lesions are combined; SP immunoreactivity accumulates in the central ends of the lumbar splanchnic nerves and in the cranial end of the intermesenteric nerve. Cutting hypogastric nerves or colonic branches of the IMG leads to accumulation of SP immunoreactivity in their ganglionic stumps and to build-up (colonic nerve lesion) rather than depletion of SP immunoreactivity in the IMG. Capsaicin treatment leads to total loss of SP immunoreactivity from the prevertebral ganglia and dorsal root ganglia, severe depletion in laminae I and II and dorsolateral fasciculus of the spinal cord, and total loss from perivascular and paravascular networks of the ileum and mesentery, with sparing of the SP immunoreactivity of the enteric nerve plexuses. Capsaicin is thought to deplete sensory neurons selectively. Removal of the spinal cord below T7 without damage to the dorsal root ganglia leaves the intraganglionic SPI nerve networks and bundles intact. We conclude that these are derived from peripheral processes of sensory neurons and we propose that the SPI synapses in the IMG arise from collateral branches of these sensory peripheral processes. This implies a novel role for these processes, in forming intraganglionically in the prevertebral ganglia synapses which may take part in the reflex control of the viscera, independently of the central nervous system.