T Il E JOURNAL O ~' I N VEST I GAT I VE D EIlMATOLOGV , 65 :458- 465, 1975 Vol. 65. No.5 Copyright © 1975 by The Williams & Wilkins Co. Printed in U.S.A. COMPARATIVE STUDY OF THE INNERVATION OF THE FACIAL DISC OF SELECTED MAMMALS WILL IAM MONTAGNA, PH.D., NICKOLAS A. ROMA N, A.Sc., AND ELIZABET H MACPHERSON Department of Cutaneous Biology, Oregon Regional Primate Research Center, iJeau erton , Oregon The greatest concent ration of sensory nerves in t he muzzle and fa cial disc of mamma ls is in the nose. In most nocturnal m a mmals, t hese nerves penetrate the epidermis of t he naked nose either singly or in bundles which resemole the corpuscles of Eimer. The ha ir follicles around t he nose, lips, a nd eyes, as well as the heavil y innervated vibrissae follicles found in all hai ry mammals except man, a re well innervated ; those elsewhere a re not. Everywhere on the human body both large and small follicles abound in sensory nerves. These morphologic observations suggest t hat in most ma mma ls the most sensit ive a reas of the s kin a re a t the a nterior a nd posterior ends (not reported here), a nd t hat huma n skin is better equipped for cutaneous sensibility t ha n that of a ny other mammal. In this pa per we report our observations on the MATERIALS AND METHODS innervation of the epidermis a nd ha ir follicles in T he tiss ues used for these obse rvations have bee n the facial disc of various animals, including ma n. co ll ected for a number of yea rs immediately after death. The greatest concentration of nerves in epidermis For each animal described , we have had at least 3 and hair follicles, particularly in nocturnal a nimals, spec ime ns. In the case of the elephant, we had specimens is at the a nterior end-the nose-and graduall y de­ from an infant and a half-g row n animal. The observ a­ creases posteriorl y. All hairy ma mmals except man tions on human tissues were made on 5 samples from the have heavil y innervated s inus hair follicl es, wh ich victims of acc idental death. Sa mpl es of each t iss ue we re treated with the sil ver method of Winkelm ann and are larger a nd more numerous in nocturnal tha n Schmit \21a nd the cholin estera se techniques modified by in diurnal a nimals. With the possibl e ex ception of Roman, Ford , and Montagna 13]. No attempt was made the mole [1 ], man is the only mammal a ll of whose to distin gui sh precisely between true and pseudo­ ha ir follicles, large or s mall , abound in sensory cholin esterases. nerves, even those minuscule fo lli cl es on the nose which are appendages of sebaceous fo lli cles. Thus, RESULTS despite their reduced size nearly everywhere on Opossum Widelphis uir{{ iniana) the body, man' hair follicl es have made hi s skin The ou ter s urface of the rhinarium is criss­ the most responsive mammalia n epidermis to ex­ crossed by shallow incisures that form isla nds of ternal stimuli. different shapes which ha ve corresponding Mammals with a naked rhina riu m also have vari­ mounds on t he undersurface of the epidermis. The able quantities of intraepidermal nerves. Numer­ intraepidermai nerves that penetrate these epider­ ous and characteristically arranged in jug-sha ped m al pegs and t he expanded nerve endings that bundles in moles, t hey form parall el bundles in t ree form a nest at the base of the epithelia l mounds shrews, lorises, and opossums; they appear in have already been described [4,5,6 ]. From the branched fibers in the snout of the pig a nd the tangle of myelinated nerve fibers at the base of t he trunk of elepha nts and in solita ry unit fibers in ro­ epitheli al columns emerge one or more nerve dents, felines, canines, and other animals. Numer­ trunks. Expanded n erve endings from the basal ous haarscheiben we re found on the nose of eel'­ nest extend for various distances over t he surface of copithecoid primates. the epidermis and stop abruptly in a blunt end. To avoid confusion, we wi ll brief1y describe the Other nerves from the same source lose their innervation of the muzzles of 10 species of mam­ myelin sheath a nd penetrate t he epidermis as fine, mals separately a nd then draw some conclusions often wavy or kinky, long fibers, some of which about their differences a nd similarities. extend to the stratum granulosum. Whereas intra­ epidermal nerves are found everywhere in the epidermal pegs, t he longest ones a re concentrated Publi cation No. 753 of the Orego n Regional Prim ate Research Ce nter supported in part by Publi c Health in their centers. All of t he nerves mentioned above Service, Nationallnstilu tes of Hea lth Grants RR 00163 of are strongly reactive for both acetylcholinesterase the Animal Reso urces Branch, Division of Research and butyrylcholinesterase, and all a re argyroph ilic Resources, and AM 08445 of the Na tional Institute of (Fig. 1). Arthritis, Metabolism, and Di gestive Diseases. Reprint reques ts to: Dr. W. Montagna, Oregon Re­ The small ha ir follicles immediately around the gional Primate Research Center, 505 N .W. 185 th Avenu e, na ked rhinarium are all richly innervated. How­ Beaverton, Oregon 97005. ever, onl y a few of the more lateral and posterior 458 Nov. 1975 NEHVE IN MAMMALIAN FA C IAL DISC 459 acetylcholinesterase and butyrylcholinesterase [1). The large deposits of reactive product in the expanded free endings a nd t he redundant myeli­ nated nerves diffuse away from these structures and ma ke them look larger t han they are. T hese and all other nerves described here are reactive for cholinesterases and are also distinctly argyrophilic (Fig. 2) . All of the hair fo llicles from around the rhinar­ ium to the eyes, particularly the sinus hair folli­ cles, are abundant ly innervated. Beyond the facial disc, most foll icles cont inue to be innervated but t he nerves around them are scarce, except in the perineum where they resemble those on t he snout . Tree Shrew (Tupaia gUs ) We agree wi t h most systematists t hat t hese strange animals belong to the P rosimii. They have a n elongated, pointed muzzle covered near the nose with sparse, short ha irs in terspersed with long vibrissae. T he large rhinarium has an irregul ar surface, li ke t hat of the two anima ls just described, with corresponding rounded pegs of epidermis on the underside. The dermis beneath the shrew rhinarium, like t hat of the mole, is overcrowded with la rge, criss-crossing myelinated nerves whose FIG. 1. Argyrophilic intraepidermal neurites in the branches a re attached to t he nerve baskets at t he snout of the opossum . The nerves ari se directly from the base of t he epiderma l mounds (Fig. 3). network of mye l inated nerves at the base of the epithelial column. They tend to co ngregate toward the center of Expanded nerve endings a nd myelinated fibers the epithelial mound. Co mpare with Figures 2 and 5. form nerve nets similar to those in opossums and (Silver method of Winkelmann and Schmi t l2], - 390 x .) follicles have a good supply of nerves. All of the sinus fo llicles, la rge or small, are surrounded by nerves inside th e coll agenous capsule. Only some of t he fo llicles over t he rest of t he body have nerves around them, except t hose in the perineum, which resemble t hose around the rhinarium. Mole (Scapanus townsendii) The surface of t he glabrous nose is incised at t he front by sulci between which islands of epidermis continue as columns into t he dermis. At the sides, where t he rhinarium has a smooth surface, the I epidermis is penetrated by single or loose bundles of n eurites. A few intraepidermal neurites also penetrate the epidermis of t he spa rsely ha ired skin lateral to the nose. In front, at the base of each , epidermal column, is a network of myelinated nerves and long and short expa nded nerve endings which resemble those of the opposum. Non­ myelinated neurites from t hese nerve baskets enter ) the entire base of the epidermal pegs, but onl y those in the very center go straight up to the granular layer. T he ones from t he sides converge toward the center bundle a nd proceed upward, parall el to t hem, in a tigh t bundle of wavy fiber . The pattern outlined by these intraepidermal neu­ FIG . 2. A co rpuscle of Eimer in the nose of a mole. Argyroph ilic mye linated nerves at the base of an epider­ rites resembles a tall , cylindrical vase with an mal mound give off in trae pidermal neuri tes and blunt expanded base (Fig. 2), typical of an organ of ex panded nerve endings. (S ilver method of Winkelmann Eimer. All of these nerves are reactive for both and Schmi t [2 1, ~ 365 x .) 460 M ONTAGNA , ROMAN , AN D MACPH EH 'ON Vo l. 65, No.5 F IG. 3. Huge mye li nated nerves underneath t he rhina­ riu m of a t ree shrew.