Ultrastructure and distribution of substance P‐immunoreactive sensory collaterals in the guinea pig prevertebral sympathetic ganglia

Abstract

A light and electron microscopic study has been made of the substance P-immunoreactive networks formed by sensory nerve fibres in the prevertebral sympathetic ganglia of the guinea pig to seek confirmation that these networks arise from collateral branches of sensory fibres passing through the ganglia and to explore the synaptic and other specialized relationships established by these networks. Slices from coeliac-superior mesenteric and inferior mesenteric ganglia of young adult males, perfusion-fixed by paraformaldehyde, were immunostained with a monoclonal antibody to substance P, and the immunolabelling was visualized by a peroxidase reaction. Immunolabelled fibres passing through the ganglia were seen by light microscopy to give off varicose collaterals that ramified in the ganglionic neuropil. Electron microscopy showed that the parent fibres were almost exclusively unmyelinated. Many collaterals ran directly beneath the basal lamina bordering the intraganglionic tissue spaces, and the varicosities either remained superficially exposed under the basal lamina or sank deeper into the supporting Schwann cells, becoming apposed to dendrites of the ganglionic neurones, upon which they formed synapses, or to other nerve terminals. The incidence of these specific associations was quantified, singly and in combination. Synapses could be situated at the same level as unlabelled synapses on the same dendrite, and exposed varicosities could lie within 0.5 micron of exposed, postsynaptic dendrites. These observations confirm a collateral, synaptic nature for the networks and suggest additional nonsynaptic modes of release and sites of transmitter action. They are consistent with the hypothesis that the system serves a nocifensor function of axon reflex type.

Distribution, immunohistochemical characteristics and nerve pathways of primary sensory neurons supplying the porcine vas deferens

“…As already mentioned, it is now generally accepted that peripheral processes of primary sensory neurons provide synaptic collaterals to principal neurons in autonomic ganglia, thus forming the basis for "axon reflexes" permitting sensory modulation of autonomic neuron activity (Cuello et al 1982;Matthews et al 1987;Suzuki et al 1989; for review, see Maggi 1995). The present results further corroborate and extend this view to the peripheral innervation of the porcine vas deferens.…”

“…It is now generally accepted that primary sensory neurons conduct not only sensory modalities but also release biologically active substances, mostly CGRP and SP, at the peripheral terminals of their processes, thereby affecting target organ functions (for review, see Maggi 1995). Moreover, these sensory fibres provide synaptic collaterals to principal neurons in autonomic ganglia, thus forming the basis for "axon reflexes" that permit sensory modulation of autonomic neuron activity (Cuello et al 1982;Matthews et al 1987;Suzuki et al 1989). The porcine vas deferens is relatively well innervated by SP-and/or CGRP-containing nerve fibres (Kaleczyc et al 1997).…”

Neurones in the chicken ureter are innervated by substance P- and calcitonin gene-related peptide-containing nerve fibres: Immunohistochemical and electrophysiological evidence

“…A similar modulation of neuronal activity by capsaicinsensitive afferents from the ureter or other pelvic viscera via tachykinins but not CGRP has been reported in the guinea pig inferior mesenteric ganglion (Tsunoo et al, 1982;Amann et al, 1988a,b). Collaterals of SP/CGRPcontaining primary afferents have been described as synapsing on these prevertebral sympathetic neurones (Dalsgaard et al, 1982(Dalsgaard et al, , 1983Matthews et al, 1987). A modulatory role of SP has also been described in chicken postganglionic sympathetic neurones, where SP evoked slow excitatory postsynaptic potentials (Dryer and Chiappinelli, 1985).…”

Visceral Pain: The Neurophysiological Mechanism

“…In addition to the roles of dichotomized afferents and viscerovisceral convergence in the spinal cord, there could be another potential mechanism that can explain organ-to-organ cross-sensitization. This involves axon collaterals of visceral afferents synapsing on secreto/motor (S/M) neurons at the prevertebral ganglia (Aldskogius et al 1986; Matthews et al 1987). If these S/M neurons from the prevertebral ganglia (e.g., major pelvic ganglion) innervate different pelvic viscera, then it will be logical to think that the sensitization of afferents can excite the S/M resulting in altered function of the innervated viscera.…”