The origin and possible significance of substance P immunoreactive networks in the prevertebral ganglia and related structures in the guinea-pig

Abstract

The distribution and origin of substance P immunoreactive nerve elements have been studied in the guinea-pig prevertebral ganglia by the indirect immunohistochemical technique, using a monoclonal antibody to substance P. Non-varicose substance P immunoreactive nerve fibres enter or leave the ganglia in all nerves associated with them, traversing the ganglia in larger or smaller bundles. Networks, mainly singlestranded, of varicose substance P immunoreactive nerve fibres also permeate the ganglia, forming a loose meshwork among the neurons. Similar networks are present in the lumbar paravertebral ganglia. In all these ganglia, neuronal somata do not in general show substance P immunoreactivity. The various nerves connected with the inferior mesenteric ganglion have been cut, in single categories and in various combinations, and the ganglion examined, after intervals of up to six days. Cutting the colonic or hypogastric nerves, which connect the ganglion with the hindgut and pelvic organs, leads to accumulation of substance P immunoreactive material in their ganglionic stumps, extending retrogradely to intraganglionic non-varicose fibres traceable through into the intermesenteric and lumbar splanchnic nerves. There is some local depletion of intraganglionic varicose networks. Cutting the intermesenteric nerve, which connects the coeliac-superior mesenteric ganglion complex with the ganglion, leads to accumulation of substance P immunoreactive material in its cranial stump and depletion of its distal stump; a minimal depletion is detectable in the inferior mesenteric ganglion itself. Cutting the lumbar splanchnic nerves, which connect the ganglion with the upper lumbar spinal cord and dorsal root ganglia, leads to accumulation of substance P immunoreactive material in their proximal stumps and total depletion of their distal, ganglionic stumps; in the ganglion there is subtotal loss of non-varicose substance P immunoreactive fibres and of varicose nerve networks, and the few surviving non-varicose fibres are traceable across the ganglion from the intermesenteric nerve to the colonic and hypogastric nerves. Cutting the intermesenteric and lumbar splanchnic nerves virtually abolishes substance P immunoreactive elements from the ganglion within three days postoperatively. It is concluded that these arise centrally to the ganglion. Capsaicin treatm ent of guinea-pigs, which depletes substance P immunoreactivity of sensory neurons, was found to leave no more than minute occasional traces of substance P immunoreactivity in the prevertebral ganglia and in dorsal root ganglion cells and spinal laminae I and II; in the ileum, substance P immunoreactivity was abolished from the paravascular nerves and perivascular nerve networks, and from large nerve varicosities in the submucous plexus. The substance P immunoreactivity of the myenteric and submucous plexuses and of the nerve networks in the muscle and mucosal layers was however otherwise unaffected. Removal of the spinal cord caudally to the seventh thoracic segment without injury to the dorsal root ganglia is without detectable effect either on the substance P immunoreactive elements of the inferior mesenteric ganglion and associated nerves, or on the peri- and paravascular nerves of the hindgut mesenteric vessels. It is concluded that the intraganglionic substance P immunoreactive elements of the prevertebral ganglia are attributable to sensory neurons of the dorsal root ganglia, and that intraspinal and enteric neurons do not contribute significantly to them. It is further postulated with the support of indirect evidence that the intraganglionic networks of varicose substance P immunoreactive fibres, which have been shown to form synapses upon the postganglionic neurons, arise as collateral branches from the substance P immunoreactive sensory fibres which traverse the ganglia, and that these can subserve a short-loop reflex control over the excitability of the ganglionic neurons in advance of, and, or, in support of, or even independently of, the recruitment of central nervous circuits.