Neuronal pathways to the rat thyroid revealed by retrograde tracing and immunocytochemistry

Abstract

The distribution and origin of the nerve fibres innervating the rat thyroid were studied by immunocytochemistry, retrograde tracing and denervation experiments. Immunocytochemistry revealed nerve fibres containing noradrenalin, neuropeptide Y, vasoactive intestinal peptide, peptide histidineisoleucine, galanin, substance P, neurokinin A and calcitonin gene-related peptide around blood vessels and follicles. Many of these transmitter candidates were found to co-exist with each other in different combinations in different subpopulations of neurons. Sympathectomy eliminated all noradrenalin- and noradrenalin/neuropeptide Y-containing fibres in the thyroid. Cervical vagotomy eliminated about 50% of the galanin-, substance P- and calcitonin generelated peptide-containing fibres. Local denervation (removal of the thyroid ganglion and the thyroid nerve) eliminated all galanin- and substance P-immunoreactive fibres and the majority of noradrenalin-,noradrenalin/neuropeptide Y-, vasoactive intestinal peptide- and calcitonin gene-related peptide-containing fibres in the thyroid gland. Injection of True Blue into the thyroid gland labelled cell bodies in the thyroid ganglion, the laryngeal ganglion, the superior cervical ganglion, the jugular-nodose ganglionic complex, the dorsal root ganglia (C 2–C 5) and the trigeminal ganglion. Judging from the number of labelled nerve cell bodies, the superior cervical ganglion and the thyroid ganglion contribute most to the thyroid innervation, while the laryngeal ganglion and the trigeminal ganglion contribute least. The True Blue-labelled ganglia were examined for the presence of various populations of nerve cell bodies (only major populations are listed). The thyroid ganglion harboured neuropeptide Y, vasoactive intestinal peptide and galanin/vasoactive intestinal peptide cell bodies (in order of predominance); the laryngeal ganglion galanin/vasoactive intestinal peptide, vasoactive intestinal peptide and calcitonin gene-related peptide cell bodies; the superior cervical ganglion noradenalin/neuropeptide Y and noradrenalin cell bodies; the jugular ganglion calcitonin gene-related peptide, substance P/calcitonin gene-related peptide and galanin/substance P/calcitonin gene-related peptide cell bodies; the nodose ganglion vasoactive intestinal peptide and vasoactive intestinal peptide/galanin cell bodies; the dorsal root ganglia (C 2–C 5) and the trigeminal ganglion calcitonin gene-related peptide, substance P/calcitonin gene-related peptide and galanin/substance P/calcitonin gene-related peptide cell bodies. Results from denervation and tracer experiments indicate that all noradrenalin-containing and the majority of neuropeptide Y-containing nerve fibres in the thyroid derive from the superior cervical ganglion (sympathetic nerve supply). All vasoactive intestinal peptide- and a minor population of neuropeptide Y- and galanin-containing fibres in the thyroid gland originate in the thyroid ganglion (parasympathetic nerve supply). Nerve fibres containing galanin, substance P and/or calcitonin generelated peptide emanate from the jugular, cervical dorsal root and/or trigeminal ganglia (sensory nerve supply). Together the findings indicate that several ganglia project to the thyroid and that many neuropeptides may be involved in the control of thyroid activity.