Skip to main content
Log in

Ultrastructure of Merkel corpuscles in the tongue of the finch, Lonchura striata

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Merkel corpuscles in the lingual mucosa of the finch, Lonchura striata, were examined by means of the argyrophilic reaction and electron microscopy. These corpuscles are composed of 12 to 20 flattened Merkel cells and enclosed nerve terminals. The present study demonstrated for the first time argyrophilia in avian subepithelial Merkel cells with the use of Grimelius silver stain. Electron-microscopically, the Merkel cell was characterized by the presence of numerous densecore granules, approximately 80 to 140 nm in diameter, as well as specialized contacts with nerve terminals. The granules showed a tendency to accumulate in the cytoplasm in close association with both nerve terminals and basal lamina. This study also provided unequivocal evidence for exocytotic discharge of Merkel-cell granules at the plasma membrane facing not only the nerve terminals but also the basal lamina. The exocytotic figures toward the nerve terminals can be regarded as synaptic discharge of Merkel-cell granules, but the possibility also exists that the Merkel-cell granules may exert a trophic effect on the nerve terminals. The exocytotic release of Merkel-cell granules toward the basal lamina with no relation to nerve terminals may suggest an endocrine (paracrine) function for the Merkel cell. The avian subepithelial Merkel cells qualify as paraneurons, but their exact nature and function remain enigmatic as is the case of intraepithelial Merkel cells in other vertebrates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alvarez FJ, Cervantes C, Villalba R, Blasco I, Martinez-Murillo R, Polak JM, Rodrigo J (1988) Immunocytochemical analysis of calcitonin gene-related peptide and vasoactive intestinal polypeptide in Merkel cells and cutaneous free nerve endings of cats. Cell Tissue Res 254:429–437

    Google Scholar 

  • Andersen AE, Nafstad PHJ (1968) An electron microscopic investigation of the sensory organs in the hard palate region of the hen (Gallus domesticus). Z Zellforsch 91:391–401

    Google Scholar 

  • Andres KH (1969) Zur Ultrastruktur verschiedener Mechanorezeptoren von höheren Wirbeltieren. Anat Anz 124:551–565

    Google Scholar 

  • Berkhoudt H (1980) The morphology and distribution of cutaneous mechanoreceptors (Herbst and Grandry corpuscles) in bill and tongue of the mallard (Anas platyrhynchos L). Neth J Zool 30:1–34

    Google Scholar 

  • Breathnach AS,(1980) The mammalian and avian Merkel cell. In: Spearman RIC, Riley PA (eds) The skin of vertebrates. Linn Soc Symp Ser 9:283–292

  • Breathnach AS, Robins J (1970) Ultrastructural observations on Merkel cells in human foetal skin. J Anat 106:411A

    Google Scholar 

  • Diamond J, Holmes M, Nurse CA (1986) Are Merkel cell-neurite reciprocal synapses involved in the initiation of tactile responses in salamander skin? J Physiol (London) 376:101–120

    Google Scholar 

  • Diamond J, Mills LR, Mearow KM (1988) Evidence that the Merkel cell is not the transducer in the mechanosensory Merkel cell-neurite complex. Progr Brain Res 74:51–56

    Google Scholar 

  • Düring M von (1975) The ultrastructure of cutaneous receptors in the skin of Caiman crocodilus. Abh Rhein-Westf Akad Wiss 53:123–134

    Google Scholar 

  • Findlater GS, Cooksey EJ, Anand A, Paintal AS, Iggo A (1987) The effect of hypoxia on slowly adapting type I(STI) cutaneous mechanoreceptors in the cat and rat. Somatosens Mot Res 5:1–17

    Google Scholar 

  • Fujita T (1977) Concept of paraneurons. Arch Histol Jpn 40 [Suppl]:1–12

    Google Scholar 

  • Fujita T, Kanno T, Kobayashi S (1988) The paraneuron. Springer, Tokyo Berlin Heidelberg

    Google Scholar 

  • Garcia-Caballero T, Gallego R, Rosón E, Basanta D, Morel G, Beiras A (1989a) Localization of serotonin-like immunoreactivity in the Merkel cells of pig snout skin. Anat Rec 225:267–271

    Google Scholar 

  • Garcia-Caballero T, Gallego R, Rosón E, Fraga M, Beiras A (1989b) Calcitonin gene-related peptide (CGRP) immunoreactivity in the neuroendocrine Merkel cells and nerve fibres of pig and human skin. Histochemistry 92:127–132

    Google Scholar 

  • Gauweiler B, Weihe E, Hartschuh W, Yanaihara N (1988) Presence and coexistence of chromogranin A and multiple neuropeptides in Merkel cells of mammalian oral mucosa. Neurosci Lett 89:121–126

    Google Scholar 

  • Gottschaldt K-M, Vahle-Hinz C (1981) Merkel cell receptors: tructure and transducer function. Science 214:183–186

    Google Scholar 

  • Gottschaldt K-M, Vahle-Hinz C (1982) Evidence against transmitter function of met-enkephalin and chemosynaptic impulse generation in “Merkel cell” mechanoreceptors. Exp Brain Res 45:459–463

    Google Scholar 

  • Grimelius L (1968) A silver nitrate stain for α2 cells in human pancreatic islets. Acta Soc Med Upsal 73:243–270

    Google Scholar 

  • Gu J, Polak JM, Tapia FJ, Marangos PJ, Pearse AGE (1981) Neuron-specific enolase in the Merkel cells of mammalian skin. The use of specific antibody as a simple and reliable histologic marker. Am J Pathol 104:63–68

    Google Scholar 

  • Halata Z (1971) Ultrastructure of Grandry nerve endings in the beak skin of some aquatic birds. Folia Morphol 19:225–232

    Google Scholar 

  • Hartschuh W, Weihe E (1988) Multiple messenger candidates and marker substances in the mammalian Merkel cell-axon complex: a light and electron microscopic immunohistochemical study. Progr Brain Res 74:181–187

    Google Scholar 

  • Hartschuh W, Weihe E, Buchler M, Helmstaedter GE, Feurle GE, Forssmann WG (1979) Met-enkephalin-like immunoreactivity in Merkel cells. Cell Tissue Res 201:343–348

    Google Scholar 

  • Hartschuh W, Weihe E, Yanaihara N, Reinecke M (1983) Immunohistochemical localization of vasoactive intestinal polypeptide (VIP) in Merkel cells of various mammals: evidence for a neuromodulator function of the Merkel cell, J Invest Dermatol 81:361–364

    Google Scholar 

  • Hartschuh W, Weihe E, Reincke M (1986) The Merkel cell. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument, vol 2. Vertebrates. Springer, Berlin Heidelberg New York, pp 605–620

    Google Scholar 

  • Hartschuh W, Weihe E, Yanaihara N (1989) Immunohistochemical analysis of chromogranin A and multiple peptides in the mammalian Merkel cell: Further evidence for its paraneuronal function? Arch Histol Cytol 52 [Suppl]:423–431

    Google Scholar 

  • Hashimoto K (1972) The ultrastructure of the skin of human embryos. X. Merkel tactile cells in the finger and nail. J Anat 111:99–120

    Google Scholar 

  • Horch KW, Whitehorn D, Burgess PR (1974) Impulse generation in type I cutaneous mechanoreceptors. J Neurophysiol 37:267–281

    Google Scholar 

  • Ide C, Munger BL (1978) A cytologic study of Grandry corpuscle development in chicken toe skin. J Comp Neurol 179:301–324

    Google Scholar 

  • Kalt MR, Tandler B (1971) A study of fixation of early amphibian embryos for electron microscopy. J Ultrastruct Res 36:633–645

    Google Scholar 

  • Louweryns JM, Van Ranst L, Lloid RV, O'Connor DT (1987) Chromogranin in bronchopulmonary neuroendocrine cells. Immunohistochemical detection in human, monkey, and pig respiratory mucosa. J Histochem Cytochem 35:113–118

    Google Scholar 

  • Malinovský L, Páč L (1985) Is the Merkel cell a secondary sensory cell? (A contribution to the classification of Merkel cell neurite complexes). Z Mikrosk Anat Forsch 99:119–128

    Google Scholar 

  • Marangos PJ, Polak JM, Pearse AGE (1982) Neuron-specific enolase: a probe for neurons and neuroendocrine cells. Trends Neurosci 5:193–196

    Google Scholar 

  • Mearow KW, Diamond J (1983) The development of mechanosensory function and synaptic morphology when regenerating axons arrive at nerve-free Merkel cells in Xenopus skin. Soc Neurosci Abstr 9:228.12

    Google Scholar 

  • Mearow KM, Diamond J (1988) Merkel cells and the mechanosensitivity of normal and regenerating nerves in Xenopus skin. Neurosciences 26:695–708

    Google Scholar 

  • Merkel F (1880) Über die Endigungen der sensiblen Nerven in der Haut der Wirbelthiere. Schmidt, Rostock

    Google Scholar 

  • Moll R, Moll I, Franke WW (1986) Formation of epidermal and dermal Merkel cells during human fetal skin development. J Invest Dermatol 87:779–787

    Google Scholar 

  • Munger BL (1965) The intraepidermal innervation of the snout skin of the opossum. A light and electron microscopic study with observation on the nature of Merkel's Tastzellen. J Cell Biol 26:79–97

    Google Scholar 

  • Munger BL (1971) Patterns of organization of peripheral sensory receptors. In: Loewenstein WR (eds) Handbook of sensory physiology, vol I. Principles of receptor physiology. Springer, Berlin Heidelberg New York, pp 523–556

    Google Scholar 

  • Munger BL, Halata Z (1984) The sensorineural apparatus of the human eyelid. Am J Anat 170:181–204

    Google Scholar 

  • Munger BL, Ide C (1988) The structure and function of cutaneous sensory receptors. Arch Histol Cytol 51:1–34

    Google Scholar 

  • Nafstad PHJ (1971) Comparative ultrastructural study on Merkel cells and dermal basal cells in poultry (Gallus domesticus). Z Zellforsch 116:342–348

    Google Scholar 

  • Nafstad PHJ (1986) On the avian Merkel cells. J Anat 145:25–33

    Google Scholar 

  • Nafstad PHJ (1987) Evidence of turnover of mammalian Merkel cells. J Anat 151:57–64

    Google Scholar 

  • Páč L (1982) Contribution to the study of Merkel corpuscles in the domestic fowl. Folia Morphol 30:340–345

    Google Scholar 

  • Sato T (1968) A modified method for lead staining of thin sections. J Electron Microsc 17:158–159

    Google Scholar 

  • Saxod R (1970) Etude au microscope électronique de l'histogenèse du corpuscle sensoriel cutané de Grandry chez le canard. J Ultrastruct Res 32:477–496

    Google Scholar 

  • Saxod R (1978) Ultrastructure of Merkel corpuscles and so-called ‘transitional’ cells in the White Leghorn chicken. Am J Anat 151:453–474

    Google Scholar 

  • Saxod R (1980) Development of Merkel corpuscles in the chicken beak. The problem of their origin and identity. Biol Cellulaire 37:61–66

    Google Scholar 

  • Scott SA, Cooper E, Diamond J (1981) Merkel cells as targets of the mechanosensory nerves in salamander skin. Proc R Soc Lond [Biol] 211:453–470

    Google Scholar 

  • Sevier AC, Munger BL (1965) A silver method applicable to paraffin sections of formol-fixed tissue. J Neuropathol Exp Neurol 24:130–135

    Google Scholar 

  • Tachibana T, Ishizeki K, Sakakura Y, Nawa T (1984) Ultrastructural evidence for a possible secretory function of Merkel cells in the barbels of a teleost fish, Cyprinus carpio. Cell Tissue Res 235:695–697

    Google Scholar 

  • Tandler B, Walter R (1977) Epon-Maraglas embedment for electron microscopy. Stain Technol 52:238–239

    Google Scholar 

  • Toyoshima K (1989) Chemoreceptive and mechanoreceptive paraneurons in the tongue. Arch Histol Cytol 52[Suppl]:383–388

    Google Scholar 

  • Watanabe I, Usukura J, Yamada E (1985) Electron microscope study of the Grandry and Herbst corpuscles in the palatine mucosa, gingival mucosa and beak skin of the duck. Arch Histol Jpn 48:89–108

    Google Scholar 

  • Whitear M (1989) Merkel cells in lower vertebrates. Arch Histol Cytol 52[Suppl]:415–422

    Google Scholar 

  • Zaccone G (1986) Neuron-specific enolase and serotonin in the Merkel cells of conger-eel (Conger conger) epidermis. An immunohistochemical study. Histochemistry 85:29–34

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Toyoshima, K., Shimamura, A. Ultrastructure of Merkel corpuscles in the tongue of the finch, Lonchura striata . Cell Tissue Res 264, 427–436 (1991). https://doi.org/10.1007/BF00319033

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00319033

Key words

Navigation