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Primary gustatory neurons and their peripheral and central processes were evaluated histochemically in the geniculate and petrosal cranial nerve ganglia, lingual fungiform taste buds, and the nucleus of the solitary tract (NST) using 1) the plant lectin Griffonia simplicifolia I-B4, which binds specifically to D-galactose residues and selectively labels primarily nonpeptide-containing peripheral somatosensory neurons, and 2) calcitonin gene-related peptide immunoreactivity (CGRP-IR), which labels most peptidergic somatosensory neurons. Lectin reactivity was expressed by the vast majority of geniculate and petrosal ganglion cells, while CGRP-IR labeled very few cells. Peripherally, gustatory intragemmal axons penetrating fungiform taste buds were labeled only by the lectin and were depleted following chorda tympani transection. However, both lectin-labeled and CGRP-IR subpopulations of somatosensory perigemmal axons surrounding the taste buds were observed and were eliminated by section of the lingual nerve. The differing brainstem projection patterns of lectin-reactive vs. CGRP-IR central axons reflected their distinct ganglionic origins and the differential distributions of lectin reactivity and CGRP-IR among taste buds. Central lectin-reactive terminals were found throughout the entire rostrocaudal extent of the NST, including its rostral lateral "gustatory" zone; the extensive lectin-reactive visceral afferent projection can be presumed to have originated mainly from the large proportion of lectin-labeled neurons in the nodose ganglion. The lectin also prominently and selectively labeled the area postrema. CGRP-IR central terminals, however, was relatively sparse and restricted primarily to the caudal and medial "visceral" divisions of the NST. The results are discussed with respect to the possible functional implications of cell surface glycoconjugate expression by gustatory axons innervating taste bud receptor cells of the tongue.

The distribution of calcitonin-gene-related peptide (CGRP) immunoreactivity (IR) was studied in peripheral tissues of rats. The ganglionic origin, somatosensory nature, and anatomic relations of this thin-axon population were evaluated with particular emphasis on possible nociceptive roles. In animals untreated with colchicine, CGRP-IR is found in a vast proportion of small- and medium-diameter sensory ganglion cells that give rise to numerous thinly myelinated and unmyelinated axons that display CGRP-IR throughout the body. The integumentary innervation consists, in part, of an extensive subpapillary network largely traced to dermal blood vessels, sweat glands, and "free" nerve endings, some of which are found within regions containing only mast cells, fibroblasts, and collagen. Dermal papillae contain CGRP-IR axons surrounding each vascular loop; other papillary axons end freely or occasionally surround Meissner corpuscles. Intraepithelial axons enter glabrous epidermal pegs, branching and exhibiting terminals throughout the stratum spinosum. A similar pattern is found in hairy skin with additional innervation entering the base and surrounding the lower third of each hair follicle, but apparently not supplying sebaceous glands and arrector pili muscle. Axons innervating nonkeratinized oral epithelium are similar or greater in number and distribution compared to epidermis, often with more extensive branching. The high density of intraepithelial CGRP-IR innervation does not appear to correlate with the sensitive mechanoreceptor-based increase in spatial sensory discriminative capacities in the distal portions of the limb. In deep somatic tissues, CGRP-IR is principally related to vasculature and motor end plates of striated muscle, but there is an extensive network of thin axons within bone, principally in the periosteum, and focally in joint capsules, but not in relation to muscle spindles or tendon organs. These findings, together with the distribution in cranial tissues described in an accompanying paper (Silverman and Kruger: J. Comp. Neurol. 280:303-330, '89), are considered in the context of a "noceffector" concept incorporating the efferent role of these sensory axons in various tissues. It is suggested that involvement in tissue maintenance and renewal during normal function, as well as following injury, may predominate over the relatively infrequent nociceptive role of this peptidergic sensory system.

The distribution of calcitonin-gene-related peptide-like immunoreactivity (CGRP-IR) was studied in sections of decalcified rat head and selected whole-mount preparations in order to address the complex peptidergic innervation patterns in peripheral cephalic specialized zones and to examine neuronal ganglia in situ. Labeled neuron somata in trigeminal, glossopharyngeal, and vagal ganglia comprised a large proportion of small to medium size type B ganglion cells. Parasympathetic ganglia (ciliary, otic, sphenopalatine, submandibular) revealed a small population of labeled somata and numerous perisomatic IR axons, whereas sympathetic ganglion cells (superior cervical) were devoid of label though richly innervated by perisomatic IR axons. The gustatory geniculate ganglion contained only a few labeled neurons and axons. Coarse peripheral CGRP-IR axons were traced to skeletal muscle motor end plates (e.g., lingual, tensor tympani, etc.), and thin sensory axons most densely innervated the cornea, iris, general integument, all mucosal epithelia lining the tympanic, nasal, sinus and oropharyngeal cavities, and the cerebral meninges. Blood vessels, glands, ducts, and their orifices were often heavily innervated, and specific specializations and exceptions are discussed. Distinctive patterns of IR innervation characterized the various specialized sensory systems, including 1) cochlear and vestibular hair cells; 2) lingual, palatal, oropharyngeal, and laryngoepiglottal taste buds; 3) main olfactory epithelium and axons projecting to glomeruli in specific sectors of main olfactory bulb; 4) septal-olfactory organ; 5) vomeronasal organ; and 6) the nervus terminalis system. Secretory epithelia (ciliary body, choroid plexus, and stria vascularis) were notably lacking in CGRP-IR. Despite the multiplicity of functionally distinct CGRP neuronal and axonal populations, certain generalizations merit consideration. The extensive innervation of chemosensory nasal and oral epithelia may contribute to specific chemical sensitivities (e.g., relating to olfactory and gustatory senses) as well as evoking "nociceptive" responses to chemical irritants as part of a "common chemical sense." An efferent role for some of these peptidergic afferent axons may also be inferred from their specific distributions. Sites involved in regulating access to and sensitivity of sense organs to external stimuli (e.g., cochlear and vestibular hair cells, taste bud orifices, and main olfactory epithelium) are heavily innervated. Other IR axons are in position to exert control over airflow through nasal turbinates, glandular secretion, blood circulation, and duct transport systems.(ABSTRACT TRUNCATED AT 400 WORDS)