Sensory Receptors of the Skin

  • Richard K. Winkelmann


Successive periods of investigation have produced anatomic, physiological, and psychological phases in our understanding of skin sensation. Each phase has been the result of technological improvement. The use of the electron microscope has brought about a decade of renewed anatomic study and reclassification of skin nerve endings. Correlation with single-unit recordings has produced a new awareness that anatomic simplicity may be attainable but that physiological responses remain complex and often proceed from stimulation of patterns of diverse receptor tissue. New chemical and immunochemical methods are providing a new degree of resolution of histological questions. Whole-mount preparations offer an excellent opportunity for correlation of sensation with structure and for quantitative study of receptor tissue. This review of cutaneous sensory receptors summarizes diverse approaches to the common problem of what receptors are present and on what evidence their independent existence and function rest. The chapter includes specific pertinent and current references. Exhaustive bibliographies on the subject will be found in the reviews of the last 20 years (Montagna and Brook-hart, 1977; Munger, 1971; Halata, 1975; Chouchkov, 1978; Winkelmann, 1960b; Sinclair, 1981; Malinovsky and Pac, 1982).


Schwann Cell Hair Follicle Nerve Ending Sensory Receptor Dermal Papilla 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Andres, K. H. Ueber die feinstruktur der rezeptoren an sinushaaren. Z. Zeilforsch. 75:339–365, 1966.CrossRefGoogle Scholar
  2. Andres, K. H. and von Duhring, L. Morphology of cutaneous mechanoreceptors, in: Handbook of Sensory Physiology, Vol. II (A. Iggo, ed.), Springer, Berlin, 1975, pp. 3–28.Google Scholar
  3. Becton, J. L., Winkelmann, R. K., and Lipscomb, P. R. Innervation of human finger tendons, as determined by histochemical techniques. J. Bone Joint Surg. 48A: 1519–1541, 1966.Google Scholar
  4. Berkhoudt, H. The morphology and distribution of cutaneous mechanoreceptors (Herbst and Grandry corpuscle) in bill and tongue of mallard (Anas platyrhynchos L.). Neth. J. Zool. 30:1–34, 1980.CrossRefGoogle Scholar
  5. Biemesdorfer, D., Munger, B. L., Binck, J., and Dubner, R. The pilo-Ruffini complex. Brain Res. 142:197–222, 1978.CrossRefGoogle Scholar
  6. Bourlond, A., and Winkelmann, R. K. Nervenendorgane der Haut beim Dachs. Acta Neuroveg. 29:149–155, 1966.CrossRefGoogle Scholar
  7. Breathnach, A. The mammalian and avian Merkel cell in the skin of vertebrates. Linnean Soc. Symp. Ser. 9:283–291, 1980.Google Scholar
  8. Cauna, N. Nerve supply and nerve endings in Meissner’s corpuscles. Am. J. Anat. 99:315–350, 1956.PubMedCrossRefGoogle Scholar
  9. Cauna, N. The effect of ageing on the receptor organs of human dermis, in: Aging, Vol. 6, Advances in Biology of Skin (W. Montagna, ed.), Permagon Press, New York, 1964, pp. 63–96.Google Scholar
  10. Cauna, N. Fine structure of the receptor organs and its probable functional significance, in: Touch, Heat and Pain (A. V. S. Rougk and J. Knight eds.), J and A Churchill, London, 1966, pp. 117–127.Google Scholar
  11. Cauna, N. The free penicillate nerve endings of the human hairy skin. J. Anat. 115:277–288, 1973.PubMedGoogle Scholar
  12. Cauna, N. Morphological basis of sensation in hairy skin. Prog. Brain Res. 43:35–45, 1976.PubMedCrossRefGoogle Scholar
  13. Cauna, N. Fine morphological characteristics and microtopography of the free nerve endings of human digital skin. Anat. Res. 198:643–656, 1980.CrossRefGoogle Scholar
  14. Chambers, M. R., Andres, K. H., von During, M., and Iggo, A. Structure and function of the slowly adapting type III mechanoreceptor in hairy skin. Q. J. Exp. Physiol. 57:417–445, 1972.PubMedGoogle Scholar
  15. Chouchkov, C. N. Cutaneous receptors. Adv. Anat. Embryol. Cell Biol. 54:1–62, 1978.Google Scholar
  16. Desjardins, R. P., Winkelmann, R. K., and Gonsalez, D. W. Comparison of nerve endings in normal gingiva with those in mucosa covering edentulous ridges. J. Dent. Res. 50:867–879, 1971.PubMedCrossRefGoogle Scholar
  17. Dickens, W. M., Winkelmann, R. K., and Mulder, D. W. Cholinesterase demonstration of dermal nerve endings in patients with impaired sensation. Neurology, (Minneap.) 13:91–100, 1963.CrossRefGoogle Scholar
  18. Dyck, P. J., Winkelmann, R. K., and Bolton, C. F. Quantitation of Meissner corpuscles in hereditary sensory disorders. Neurology (Minneap.) 16:10–17, 1966.CrossRefGoogle Scholar
  19. English, K. B. Cell types in cutaneous type I mechanoreceptors (Haarscheiben) and their alterations with injury. Am. J. Anat. 141:105–126, 1974.PubMedCrossRefGoogle Scholar
  20. Fitzgerald, M. J. T. The innervation of the epidermis, in: Skin Senses (D. R. Kenshalo, ed.), Charles C. Thomas, Springfield, IL, 1968, pp. 61–80.Google Scholar
  21. Fortman, G. J., and Winkelmann, R. K. A Merkel cell nuclear inclusion. J. Invest. Dermatol. 61:334–338, 1973.PubMedCrossRefGoogle Scholar
  22. Fortman, G. J., and Winkelmann, R. K. The Merkel cell in human oral mucosa. J. Dent. Res. 11:1303–1312, 1977.Google Scholar
  23. Giacometti, L. The anatomy of the human scalp, in: Aging, Vol. 6, Advances in Biology of the Skin (W. Montagna, ed.), Pergamon Press, New York, 1965, pp. 97–118.Google Scholar
  24. Giacometti, L., and Montagna, W. Innervation of the hair follicle, in: Advances in Biology of the Skin, Vol. IX, Hair Growth (W. Montagna and R. L. Dobson, eds.), Pergamon Press, New York, 1969, pp. 392–398.Google Scholar
  25. Gu, J., Polck, J. M., Tafia, F. J., Marangos, P. J., and Pearse, A. G. E. Neuron specific enolase in the Merkel cells of mammalian skin. Am. J. Pathol. 104:63–68, 1981.PubMedGoogle Scholar
  26. Halata, Z. The mechanoreceptors of mammalian skin. Adv. Anat. Embryol. Cell Biol. 50:3–77, 1975.PubMedGoogle Scholar
  27. Halata, Z. and Munger, B. L. Identification of the Ruffini corpuscle in human hairy skin. Cell Tissue Res. 219:437–440, 1981.PubMedCrossRefGoogle Scholar
  28. Hartschuh, W., Weihe, E., Buchler, M., Helmstaedter, V., Feurle, G. E., and Forrssmann, W. G. Metenkephalin-like immunoreactivity in Merkel cells, Cell Tissue Res. 201:343–348, 1983a.Google Scholar
  29. Hartschuh, W., Weihe, E., Yanaihara, N., and Reinecke, M. Immunohistochemical localization of vasoactive intestinal polypeptide (VIP) in Merkel cells of various mammals. J. Invest. Dermatol. 81:361–364, 1983b.PubMedCrossRefGoogle Scholar
  30. Horch, K. V., Tuckett, R. P., and Burgess, P. R. A key to the classification of cutaneous mechanoreceptors. J. Invest. Dermatol. 69:75–82, 1977.PubMedCrossRefGoogle Scholar
  31. Hromada, J., and Polacek, P. A. Contribution to the morphology of encapsulated nerve endings in the joint capsule and in the periarticular tissue. Acta Anat. 33:187–202, 1958.PubMedCrossRefGoogle Scholar
  32. Iggo, A. Cutaneous receptors, in: The Peripheral Nervous System (J. I. Hubbard, ed.), Plenum Press, New York, 1974, pp. 347–404.CrossRefGoogle Scholar
  33. Iggo, A., and Gottschaldt, K. M. Cutaneous mechanoreceptors in simple and in complex sensory structures, in: Mechanoreception (J. Schwarzkopf, ed.), Westdeutsch Verlag, Opladen, 1974, pp. 153–176.Google Scholar
  34. Iggo, A., and Muir, A. R. The structure and function of a slowly adapting touch corpuscle in hairy skin. J. Physiol (Lond.) 200:763–796, 1969.Google Scholar
  35. Iggo, A., and Ogawa, H. Correlative physiological and morphological studies of rapidly adapting mechanoreceptors in cat’s glabrous skin. J. Physiol. (Lond.) 266:275–296, 1977.Google Scholar
  36. Jackson, H. C, Winkelmann, R. K. and Bickel, W. H. Nerve endings in the human spinal column. J. Bone Joint Surg. 48A: 1272–1281, 1966.Google Scholar
  37. Janig, W. Morphology of rapidly and slowly adapting mechanoreceptors in the hairless skin of the cat. Brain Res. 28:217–231, 1971.PubMedCrossRefGoogle Scholar
  38. Krause, W. Die terminalen Korperchen der Einfach sensiblen Nerven, Hahn, Hanover, 1860.Google Scholar
  39. Lipscomb, P. R., and Winkelmann, R. K. A whole-mount cholinesterase technic for study of innervation of the deep structures of the limbs. J. Invest. Dermatol. 37:481–483, 1961.PubMedCrossRefGoogle Scholar
  40. Loewenstein, W. R. Mechano-electric transduction in the Pacinian corpuscle, in: Principles of Receptor Physiology (W. R. Loewenstein, ed.), Springer, Berlin, 1971, pp. 362–374.Google Scholar
  41. Mahrle, G. and Orfanos, C. E. Merkel cells as human cutaneous neuroreceptors. Arch. Dermatol. Forsch. 251:19–26, 1974.PubMedCrossRefGoogle Scholar
  42. Malinovsky, L. Sensory innervation in the hedgehog snout epidermis, Erinaceus europaeus. Scripta Med, 54:113–126, 1981.Google Scholar
  43. Malinovsky, L., and Pac, L. Morphology of Sensory Corpuscles in Mammals. Opuscular Morphologia 74, University of Brno, 1982.Google Scholar
  44. Malinovsky, L., and Sommerova, J. Sensory nerve endings in the human labia minora pudendi and their variability. Folia Morphol (Praha) 21:351–354, 1973.Google Scholar
  45. Malinovsky, L., and Sommerova, J. Sensory nerve endings in the penis of the green monkey (Cercopithecus aethiops). Z. Mikrosk. Anat. Forsch. 91:94–104, 1977.PubMedGoogle Scholar
  46. Merkel, F. Tastzellen und Tastkorperchen bei den Hauttieren und beim Menschen. Arch. Mikrosk. Anat, Entwickl. 11:636–652, 1875.CrossRefGoogle Scholar
  47. Miller, M. R., Ralston, H. J., and Kasahara, M. The pattern of cutaneous innervation of the human hand, foot and breast, in: Advances in Biology of Skin, Vol. 1, Cutaneous Innervation (W. Montagna, ed.), Pergamon Press, New York, 1960, pp. 1–16.Google Scholar
  48. Mitchell, J. C. Distribution of dehydrogenases in the skin of the rhesus monkey. J. Histochem. Cytochem. 13:668–676, 1965.CrossRefGoogle Scholar
  49. Montagna, W., and Brookhart, J. M. Cutaneous innervation and modalities of cutaneous sensibility. J. Invest. Dermatol. 69:1–189, 1977.Google Scholar
  50. Montagna, W., and Yun, J. S. The skin of primates VII. The skin of the great bush baby (Galago grassicaudaticus). Am J. Phys. Anthropol. 20:149–165, 1962.PubMedCrossRefGoogle Scholar
  51. Muller, S. A., and Winkelmann, R. K. Cutaneous nerve changes in zoster. J. Invest. Dermatol. 52:71–77, 1969.PubMedGoogle Scholar
  52. Munger, B. L. Patterns of organization of peripheral sensory receptors, in: Handbook of Sensory Physiology, Vol. I, Principles of Receptor Physiology (W. R. Loewenstein, ed.), Springer, Berlin, 1971, pp. 523–569.CrossRefGoogle Scholar
  53. Munger, B. L. Multiple afferent innervation of primate facial hairs: Henry Head and Max von Frey revisited. Brain Res. Rev. 4:1–43, 1982.CrossRefGoogle Scholar
  54. Munger, B. L., and Halata, Z. The sensory innervation of primate facial skin. I. Hairy Skin. Brain Res. Rev. 5(l):45–80, 1983.CrossRefGoogle Scholar
  55. Pease, D. C., and Quilliam, T. A. Electron microscopy of the Pacinian corpuscle. J. Biophys. Biochem. Cytol. 3:331–342, 1957.PubMedCrossRefGoogle Scholar
  56. Peterson, H. A., Winkelmann, R. K., and Coventry, M. B. Nerve endings in the hip joint of the cat: Their morphology distribution and density. J. Bone Joint Surg. 54:333–343, 1972.PubMedGoogle Scholar
  57. Pinkus, F. Ueber einen Eisher unbekannten Nebenapparat am Haarsystem des Menschen. Haarscheiben. Dermatol Z. 9:465–469, 1902.CrossRefGoogle Scholar
  58. Ranvier, L. Nouvelles recherches sur les organes du tact C. R. Acad. Sci. [D] (Paris) 91:1087–1089, 1880.Google Scholar
  59. Robertson, D. M., and Winkelmann, R. K. A whole-mount cholinesterase technique for demonstrating corneal nerves: Observations in the albino rabbit. Invest. Ophthalmol. 9:710–715, 1970.PubMedGoogle Scholar
  60. Rowden, G., Connelly, E. M., and Winkelmann, R. K. Cutaneous histiocytosis X: The presence of S-100 protein and its use in diagnosis. Arch Dermatol. 119:553–559, 1983.PubMedCrossRefGoogle Scholar
  61. Saurat, S. H., Chavez, P., Carraux, P., and Didier, J., L. A human monoclonal antibody reacting with Merkel cells: Immunofluorescence, immunoperoxidase and immunoelectron microscopy. J. Invest Dermatol. 81:249–252, 1983.PubMedCrossRefGoogle Scholar
  62. Saxod, R. Activite cholinesterasique des corpuscles sensorials cutanes de Herbst et de Grandry. Histochemie 34:43–63, 1973.PubMedGoogle Scholar
  63. Saxod, R. Combination of cholinesterase staining of nerves and stereoscopic viewing for three dimensional study of skin innervation in whole mounts. J. Invest. Dermatol. 70:95–97, 1978a.PubMedCrossRefGoogle Scholar
  64. Saxod, R. Development of cutaneous sensory receptors in birds, in: Handbook of Sensory Physiology, Vol. IX, Development of Sensory Systems (W. R. Loewenstein, ed.), Springer, Berlin, 1978b, pp. 338–410.Google Scholar
  65. Sinclair, D. C. Mechanisms of Cutaneous Sensation. Oxford University Press, New York, 1981.Google Scholar
  66. Steigleder, G. K., and Schultis, K. Zur Histochemie der Meissnerchen Tastkorperchen. Acta Neuroveg. 18:335–343, 1968.CrossRefGoogle Scholar
  67. Weddell, G., and Pallie, W. Studies on the innervation of skin II. The number, size and distribution of hairs, hair follicles, and orifices of the rabbit ear. J. Anat. 89:175–188, 1955.PubMedGoogle Scholar
  68. Weddell, G., Palmer, E., and Pallie, W. The morphology of peripheral nerve terminations in the skin. Q. J. Micra. Sci. 95:483–501, 1954.Google Scholar
  69. Winkelmann, R. K. The mucocutaneous endorgan. A.M.A. Arch. Dermatol. 76:225–235, 1957.CrossRefGoogle Scholar
  70. Winkelmann, R. K. The endorgan of feline skin. A morphological and histochemical study. Am. J. Anat. 107:281–290, 1960a.PubMedCrossRefGoogle Scholar
  71. Winkelmann, R. K. Nerve Endings in Normal and Pathologic Skin. Charles C Thomas, Springfield, IL, 1960b.Google Scholar
  72. Winkelmann, R. K. Nerve endings in the skin of the gorilla. J. Comp. Neurol. 116:145–155, 1961.PubMedCrossRefGoogle Scholar
  73. Winkelmann, R. K. The mammalian endorgan in oral tissue of the cat. J. Dent. Res. 41:207–212, 1962a.CrossRefGoogle Scholar
  74. Winkelmann, R. K. Cutaneous sensory endorgans of some anthropoid apes. Science 136:384–386, 1962b.PubMedCrossRefGoogle Scholar
  75. Winkelmann, R. K. Cholinesterases. Ann. N.Y. Acad. Sci. 100:224–34, 1963a.Google Scholar
  76. Winkelmann, R. K. Nerve endings in the skin of primates, in: Evolutionary and Genetic Biology of Primates, Vol. 1 (J. Bueitner-Janush, ed.), Academic Press, New York, 1963b, pp. 229–259.CrossRefGoogle Scholar
  77. Winkelmann, R. K. Nerve endings of the North American oppossum (Didelphis virginiana). A comparison with nerve endings of primates. Am. J. Phys. Anthropol. 22:253–258, 1964.PubMedCrossRefGoogle Scholar
  78. Winkelmann, R. K. Innervation of the skin: Notes on a comparison of primate and marsupial nerve endings, in: Biology of the Skin and Hair Growth (A. G. Lyne and B. F. Short, eds.), Elsevier, New York, 1965, pp. 171–182.Google Scholar
  79. Winkelmann, R. K. Some unusual histochemical properties of kangaroo. J. Invest. Dermatol. 46:446–452, 1966.Google Scholar
  80. Winkelmann, R. K. New methods for the study of nerve endings, in: The Skin (E. Helwig, ed.), Williams & Wilkins, Baltimore, 1971, pp. 112–126.Google Scholar
  81. Winkelmann, R. K. The Merkel cell system and comparison with the neurosecretory or Apud system. J. Invest. Dermatol. 69:44–46, 1977.CrossRefGoogle Scholar
  82. Winkelmann, R. K. The histochemistry of the Merkel cell neuroepithelial endings of cat and rabbit skin and oral mucosa. Acta Dermatol. Wen. 62:383–387, 1982.Google Scholar
  83. Winkelmann, R. K. and Breathnach, A. The Merkel cell. J. Invest. Dermatol. 60:2–15, 1973.PubMedCrossRefGoogle Scholar
  84. Winkelmann, R. K., and Myers, T. T. The histochemistry and morphology of the cutaneous sensory endorgans of the chicken. J. Comp. Neurol. 117:27–35, 1961.PubMedCrossRefGoogle Scholar
  85. Winkelmann, R. K. and Osment, L. O. The Vater-Pacini corpuscle in the skin of the human fingertip. Arch. Dermatol. 73:116–122, 1956.CrossRefGoogle Scholar
  86. Winkelmann, R. K, Wolef, K., and Pierce, J. Removal of epidermis with sodium bromide for cholinesterase staining of dermal nerve. Stain Technol. 42:214–215, 1967.PubMedGoogle Scholar
  87. Zollman, P. E., and Winkelmann, R. K. The sensory innervation of the common North American raccoon (Procyon lotor). J Comp. Neurol. 119:149–157, 1962.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1986

Authors and Affiliations

  • Richard K. Winkelmann
    • 1
  1. 1.Department of DermatologyMayo ClinicRochesterUSA

Personalised recommendations