An immunohistochemical study of sensory and autonomic innervation of the dog tongue with special reference to substance P- and calcitonin gene-related peptide-containing fibers in blood vessels and the intralingual ganglia.

Abstract

The distribution, pathways and origins of peptide-containing nerve fibers in the anterior two thirds of the dog tongue were investigated using immunohistochemistry combined with retrograde axonal tracing and denervation experiments. Within the epithelium of the fungiform papillae, varicose nerve fibers immunoreactive to substance P (SP) and calcitonin gene-related peptide (CGRP) were present. These disappeared completely after severance of the lingual nerve (LN) alone. Dense CGRP-immunoreactive varicose fibers surrounded cell bodies in the intralingual ganglia (ILG), which consisted of neurons immunoreactive to vasoactive intestinal polypeptide (VIP), neuropeptide Y (NPY) and SP. These CGRP-immunoreactive fibers disappeared following severance of the chorda tympani (CT) alone. SP-, CGRP-, VIP-, NPY- and tyrosine hydroxylase (TH)-immunoreactive nerve fibers were distributed around the walls of blood vessels, especially arteriovenous anastomoses (AVAs). None of these immunoreactive fibers completely disappeared after severance of the LN or CT alone, but SP- and CGRP-immunoreactive fibers disappeared following severance of both the LN and CT. TH-immunoreactive fibers disappeared after ganglionectomy of the superior cervical ganglion (SCG) or severance of the hypoglossal nerve (HGN). VIP- and NPY-immunoreactive fibers invariably remained after various denervation experiments. In tracing experiments, CGRP-immunoreactive as well as SP and CGRP-immunoreactive cells in the trigeminal ganglion were labelled from the LN, and those in the geniculate ganglion and jugular ganglion were labelled from the CT. A large number of neurons in the SCG were labelled from the HGN, with some of these being SP and CGRP-immunoreactive. These results demonstrate that SP- and CGRP-immunoreactive fibers from the trigeminal ganglion are distributed to the lingual epithelium; vascular walls receive SP- and CGRP-immunoreactive sensory fibers from the LN as well as CT, some SP and CGRP-immunoreactive fibers from the SCG in addition to catecholaminergic sympathetic fibers, and VIP- and NPY-immunoreactive parasympathetic fibers from the ILG. The ILG is also considered to be innervated by CGRP-immunoreactive sensory fibers from the CT.