Comparative Study of the Innervation of the Facial Disc of Selected Mammals

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. (S il ver method of Winkelmann and Schmit [2 ], - 78 x .)

moles and resemble stemmed chali ces from which emerge numerous neuri tes that penetrate the epi dermis up to t he horny layer (Fig. 4). T hese neurites also tend to be longe r and more densely conce ntrated in the center of t he epiderm al col FIG. 4. Mye linated nerve baskets with ex panded nerve umns (Fig. 5). All of t hese nerves are reactive for ends at t he base of three epidermal mounds fr om the cholinesterases and are argy rophilic. rhinarium of a tree shrew. The in traepiderma l neurites are mostly out of foc us. T hey can be seen clearl y in F ig T he hair fo llicles on the muzzle, like t hose in the ure 5. (Sil ve r method of Winkelmann and Schmit [2 ], opossum, have numerous nerves around them (Fig. - lOO x .) 6). Potto (Perodicticus potto), Galago (G alago crass i caudatus), S low Loris (Nycticebus coucang) T he rhinaria of these three species of prosimians, like the nerves associated with them , are similar. In all three species, the gla brous nose has a pebbled outer surface, wit h corres ponding columns of epit helium which projec t into the dermis. The lower half to two-thirds of t he epit heli al columns is surrounded by myelinated nerve networks of vari a ble density and tight ness. Nearl y everywhere around t he base of the epit heli al columns are enlarged fr ee nerv e endings of diffe rent lengths, and ga lagos also have glomerate bodi es which resemble mucocutaneous end -o rgans (Fig. 7). Some nonmyelinated neurites extend for so me distance into the epidermis. T he nerves described here, myelinated or not, are all cholinestera e reactive. As in the other animals described here, the hair fo llicles around the nose are all abundantly inner vated but t hose over the body are not. M acaques (Macaca mulatta, M. speciosa, and M. fascicularis) The outer surface of t he simian primate nose (suborder Cercopit hecoid ea) and t he inside of t he choanae a re hairy. In most species, as in man, F IG. 5. Intraepidermal neurites in t he nose of a tree t hese hairs are small and associated with la rge shrew. Note that t he longest nerves tend to congregate sebaceous glands. In all t hree species of macaque, toward the ce nter. (Sil ve r method of Winkelmann and we have found relatively numerous cholinesterase- Schmit [2 ], - 340 x .) Nov. 1975 NERVES IN MAMMALIAN FA CIAL DISC 461 traepidermal nerves are numerous inside the ves tibule of the nares (Fig. 10) . All of the follicles in the nose, inside or out, are profusely innervated. The only glabrous areas of the nose are t he lower

FIG. 8. Cholinesterase-reactive haarscheib en on the nose of the tump-ta il ed macaque (- 125 x ).

FIG. 6. Numerous argyrophilic fib ers around a small h ·r fo llicle on the muzz le of a tree shrew. (S Ilver method o;Winkelmann and Schmit [2 ], - 390 x .)

FIG. 9. Enlarged detail of a single haarscheibe to show its neural ma ke- up (- 210 ).

FIG. 7. Great numbers of acetylcholinesterase·reac t"ve nerves at the bases of epidermal pegs in the rhina ~urn of a potto. Some intraepidermal nerves can be seen. (Modified cholinesterase method of Roman et al [3 j, - 125 )( .)

reactive masses, from which emerge single nerves I or bundles of nerves. These masses are found underneath thickening of the epidermis which resernbles haarscheiben; they a re particularly nu merous in the alae of the nose of M . fa scicularis FIr.. 10. erves around hair folli cles. haarscheiben, (Figs. 8, 9). Our techniques enable us to see me and in traepid ermal neurites in the hoanae of a stump nonrnyelinated neurites inside the epidermis; in - tailed macaque (- 54 x ). 462 MONTAGNA, ROMAN, AND MACPHERSON Vol. 65, No.5

(ventral) depressions of the choanae. J ust lateral to the nose and along t he labial borders are many very small sinus fo lli cles, all heavily innervated [7]. Large sinus fo llicles are found primarily in the mystacial areas and above the brows. The innerva tion of t he fo lli cles of the muzz le decreases percept ibly at the periphery of the facial disc. All of the nerve elements described here can be demon strated with the techniques used for both cholines terases, and most are argyrophilic. Man Most of the follicles on t he nose are so small as to be a ppendages of the large sebaceous follicles; in complex, they form a thick sebaceous blanket over the surface of the nose. Notwithstanding t heir small size, all of these follicles, like t he others on FIG. 11. Low magnification of the surface of the hu t he human body, are equipped wit h a sensory man nose in whi ch the cholinesterase-reactive nerve end organs can be seen around each fo lli cle. (Acetylcholin nerve end-organ (Fig. 11) [8 ]. Since all fo llicles esterase technique of Roman et al [3], - 19 x .J elsewhere, large or small , are also similarl y en dowed, there is nothing unusual about the nose or facial disc. The terminal dilated ducts of the sebaceous 1'011 icles are also enwrapped wit h nerves and resemble haarscheiben (Fig. 12). Intraepid er mal neurites are seen occasiona ll y on t he nose. All of t hese nerve structures are reactive for acetylcho linesterase and are mostly argy rophilic. Cat and Dog In both animals, the surface of the nose is deeply pebbled on the outer surface and has a co mplex labyrinthine structure on the underside. The few intraepidermal neurites that penetrate the epider mis of the rhinarium are patternless and are distributed singly (Fig. 13). The dense network of nerves that adheres to the underside of the epider mal projections, t he expanded free ends, and the intraepidermal nerves are reactive for both acetyl FIG. 12. holinesterase-reactiv e nerves a round the cholinesterase and butyrylcholinesterase, and fhey duct of' a sebaceous fo ll ic le and around ve ll us hair fo llicles in the human nose. (Acetylcholi nesterase technique of are also argyrophilic. T he small dense hai rs around Roman et al [3 J, - 80 x .J t he nose, lips, a nd muzz le are all well innervated as are some of the large ones as far as t he periphery of t he fac ial di sc. Large, often luxuriant vibrissae extend from the mystacial areas and above t he brows.

Rat The small , glabrous surface of t he rhinarium is smooth and the underside of its epidermis some what f1at . As in the cat and dog, t he short, intraepidermal neurites are sparse and patternless. Below the epidermis is a network of myelinated fibers and some free expanded endings. These elements are reactive for cholinesterases and are argyrophilic. The follicles of t he muzzle are well innervated but those in the rest of the body are not. Pig F IG. 13. S ingle in traepidermal fib ers in the nose of a T he innervation of t he snout and muzzle of the cat. (Sil ver method of Winkelmann and Schmit [2] _ pig has been studied by a number of authors SO x .) , Nov. 1975 NEHVES IN MAMMALIAN FACIAL D ISC 463

[6 ,9,10 ], but t he observations that fo llow are unique. The up\?er part of the nat snout has a hard h orny plate, thick and glabrous and adapted for routing. The surface of t he funnel-li ke depressions of the expanded nares is also glabrous, but t he nat of the snout between the t1ared nares is pock marked with large orifices of sinus hair follicles from which emerge stout vibrissae of variable length; there are no ?rdinary follicles in this area. Throughout the entIre snout the surface of the underside of the thick epidermis is specialized differently in the ha.iry and glabrous areas. Where the flat snout IS hairy, each sinus hair fo llicle is su rrounded by very long, narrow, concentric ridges; where it is ?Iabrous, the underside presents a somewhat reticulated appearance, as described by Montagna and Macpherso n [6 ]. Many large myelll1ated nerve bundles ri se up to the lo ng epidermal ri.dges in both t he hairy and glabroUS ~reas an.d be,fore reaching the bases divide into neuntes which torm masses resembling end organS and. gr?uped at t he base~ of t h ~ epiden;nal ridges and lI1 slde the dermal papilla (Fig. 14). Fitz Gerald (11] call ed these masses bulbous cor puscles. They are composed of glomerate skeins of nerves, easily demonstrated with sil ve r methods. From t he myelinated subepidermal nerves also FIG. 15. Nerve trunks underneath the epidermis of the emerge fine , parallel neurites, some of which go snout of the pig, sending branches upwa rd in to t he narrow epidermal ridges and inside the dermal papillae inside t he epidermal . ridges, and some penetrate between t hem . (Sil ve r method of Winkelmann and the thin dermal papIllae between the epidermal Schmit [2 ], - lOO x .) ridges (Fig. 15) . Expanded nerves as well as intraepidermal ~nd dermal papillae neurites are more numerous. 111 the glabrous areas around the Elephant choanae than In t he areas which contain sinus hairs. All the myelinated fibers and t he expanded We have studied in detail only t he prehensive nerve end-organs are cholinesterase positive. All li ps at the tip of the trunk since elsewhere, whether in the trunk or fa cial disc, cutaneous nerves are myelinated and n~nmyelinated nerves described here are acetylcholll1esterase reactive and argyro- sparse. Our limited search of the literature has yie lded no pertinent reference. Under the epider philic. mis of the tips of the truncal lips are numerous cholinesterase-reactive, small, encapsulated, Paci ni -like corpuscles which resemble both end-bulbs (endkapeln), formerly called Krause end-bulbs, and t he Grandry corpuscles found at t he edge of the bi ll of ducks and geese [12]. These corpuscles are scattered singly or in clusters at the base of the epidermal ridges, hi gh in the papillary body be tween the epidermal fo lds, or even deep in the dermis (Fig. 16). Chains of corpuscles are often connected by nerves from which spring variable numbers of neurites whic h rise in to the dermal papilla and some of which penetrate the epi dermis (Fig. 17). T hose that remain in the dermis form glomerate skeins of argyrophilic nerves (Fig. 18).

DISCUSSION T he major organs of touch in all mammals are located principally in the face and specifically FIG. 14. Bu!bous corpuscles from the s n ~ ut of t he pig at the base of the epidermal n dges and hi gh up in the around the nose (in quadrupeds, the foremost part derma) papill ae. (Silver technique of Winkelmann and of the body) , t he mouth, and t he eyes. Numerous Schmit [2J, - 125 x .) sensory nerves are also found in the perineum, a 464 MONTAGNA, ROMAN, AND MACPHERSON Vol. 65, No.5

FIG. 16. Encapsulated Grandry-like or Pacini-like cor F IG. 18. Two Grandry-lik e corpuscles in the papill a ry puscles in the trunk of an elephant. (C holinesterase dermis of the trunk of a n elephant. Note their resem technique of Roman et al [3], - 80 x .) bl ance to mucocuta neo us end -o rga ns. (Sil ver method of Winkelmann and Schmit l2 ], - 125 x .)

them.) Among t he many peculiarities of man, then, are his hair follicl es, which though mostly archaic, have a well-developed nerve end-organ; the entire follicle is li terally enwrapped in a complex nerve net (8). Thus, despite the lack of comparative data, human skin is indubitably more sensitive than that of any other mammal. These findings suggest that t he high develop ment of the sensory mechanism of touch around the primary sense organs of the faci al disc has the special mission of protecting this most importa nt a nd most vulnerable part of the body. Not all mammals with similar life styles, however, acquire the same degree of tactile sensation even though their mechanisms are morphologically similar. In nocturnal animals, for example, vibrissae are ex ~ tremely large in opossums, cats, and rodents but small and sparse in moles. We find that the animals with small vibrissae have more numerous intraepidermal nerves and a ri cher innervation of all hair follicles around the nose and mouth or both. These structural mechanisms, together with data on human beings [13], lead one to infer that tactile sensory mechanisms have the lowest thresh old on the fac ial disc and that the nerves we have just described are the morphologic rece ptors of the FIG. 17. Nerve trunks at the base of the thick epidermis in the trunk of an elephant divide into branches, some of modali ties of touch. . which penetrate the epidermal ridges, some remain in the We have also shown that intraepidermal nerves dermal 2apillae. (Silver method of Winkelmann and exist in mammalian skin, at least in specialized Schmit 12 ], - 100 x .) areas (4 ,6,14]. Even in man they are more numer ous than had been suspected; we have found them major erotic area, and at the distal parts of the to be especially plentiful in mucocutaneous and appendages. The skin of hirsute mammals is friction surfaces. insulated from the outsid e environment by a pelt of Long-snouted, nocturnal, or burrowing animals varied thickness and density; cutaneous sensory such as hedgehogs (15], moles (1], opossums [4 - 6 - nerves, particularly those around hair follicles, are 15 J, tree shrews [6,16), lorises (17), and others sparse and nearly negligible i·n these animals. The abound in nerves inside the peg- like thickenings of known exception is the mole, in which Giacometti epidermis that correspond to the elevation on the and Machida [1] found a phosphatase-reactive surface of the rhinarium. Such neurites originate end-organ around nearly every follicle. (Our own directly from chalice-like configurations of myeli investigations support this finding, but the follicles nated nerves around the base of the epidermal pegs of body hairs have only a very few nerves around and not from "tactile disks " as Winkelmann (1 8J Nov, 1975 NERVES IN MAMMALIAN FACIAL DISC 465 orted, We found no "tactile disks," only ex many haarscheiben present. Those interested in rep ded free nerve endings, The intraepidermal the anatomy and physiology of these structures pa~rites , together with the nerve baskets from would do well to study them there, n~, ch th ey arise, form clearly structured sensory This study has shown t hat the distribution of W d_organs which resemble Eimer corpuscles, and cutaneous sensory organs in the facial disc repre en sUggest that they be so designated since, de sents a strategic plan. T his plan is to guide the :;ite species modification, they all have basic sim- animal in moving about without the aid of vision ilarities, , and to make it aware of di sturbances that might be The partIcular configuration of the nerves of injurious to the other sensory organs. E'rner corpuscles in t he mole is achi eved by the 1 tripetal bending of the lateral intraepidermal REFERENCES ~~~rites, This s,uggests that son:e factor(s) i~ t he 1. Giacometti L, Machida H: The skin of the mole 'derm is provIdes a more satIsfactory envlron (Scapanus town.sendii). Anat Rec 153:31 - 40, 1965 epl nt for fibers in the center of the epit helial 2. Winkelmann RK, Schmit RW: A simple silver rnelurnns th an at the sides, This pattern, conspicu- method for nerve axoplasm. Proc Staff Meet Mayo co ' I b d ' Clinic 37:217- 222, 1957 in moles, IS a so 0 serve In opossums, tree 3. Roman NA, Ford D, Montagna W: The demonstra o~;ews, and lorises where ,the long,est neurites and tion of cutaneous nerves. 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