Summary
Lacertilian species display a remarkable diversity in the organization of the neural apparatus of their pineal organ (epiphysis cerebri). The occurrence of immunoreactive S-antigen and opsin was investigated in the retina and pineal organ of adult lizards, Uromastix hardwicki. In this species, numerous retinal photoreceptors displayed S-antigen-like immunoreactivity, whereas only very few pinealocytes were labeled. Immunoreactive opsin was found neither in retinal photoreceptors nor in pinealocytes. Electron microscopy showed that all pinealocytes of Uromastix hardwicki resemble modified pineal photoreceptors. A peculiar observation is the existence of a previously undescribed membrane system in the inner segments of these cells. It is evidently derived from the rough endoplasmic reticulum but consists of smooth membranes. The modified pineal photoreceptor cells of Uromastix hardwicki were never seen to establish synaptic contacts with somata or dendrites of intrapineal neurons, which are extremely rare. Vesiclecrowned ribbons are prominent in the basal processes of the receptor cells, facing the basal lamina or establishing receptor-receptor and receptor-interstitial type synaptoid contacts. Dense-core granules (60–250 nm in diameter) speak in favor of a secretory activity of the pinealocytes. Attention is drawn to the existence of receptor-receptor and receptor-interstitial cell contacts indicating intramural cellular relationships that deserve further study.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Collin JP (1967) Structure, nature secrétoire, dégénérescence partielle des photorécepteurs rudimentaires épiphysaires chez Lacerta viridis (Laurenti). C R Acad Sci (Paris) Série D 264:647–650
Collin JP (1969) Contribution à l'étude de l'organe pinéal. De l'épiphyse sensorielle à la glande pinéale: modalités de transformation et implications fonctionelles. Ann Stn Biol Besse [Suppl] 1:1–359
Collin JP (1971) Differentiation and regression of the cells of the sensory line in the epiphysis cerebri. In: Wolstenholme GEW, Knight J (eds) The pineal gland. Churchill Livingstone, Edinburgh, London, pp 79–125
Collin JP, Kappers JA (1971) Synapses of the ribbon type in the pineal organ of Lacerta vivipara (Reptiles, Lacertilians). Experientia 27:1456–1457
Collin JP, Oksche A (1981) Structural and functional relationships in the nonmammalian pineal gland. In: Reiter RJ (ed) The pineal gland. Vol. 1. Anatomy and biochemistry. CRC Press, Boca Raton, pp 27–67
Dodt E (1973) The parietal eye (pineal and parietal organs) of lower vertebrates. In: Jung R (ed) Handbook of sensory physiology. Vol. VII/3 B. Springer, Berlin Heidelberg New York, pp 113–140
Gundy GC, Wurst GZ (1976) Parietal eye-pineal morphology in lizards and its functional implications. Anat Rec 185:419–432
Hafeez MA, Wagner H, Quay WB (1978) Mediation of light-induced changes in pineal receptor and supporting cell nuclei and nucleoli in steelhead trout (Salmo gairdneri). Photochem Photobiol 28:213–218
Haldar C, Thapliyal JP (1979) Pineal of Calotes versicolor Daud.: A light and electron microscopic study. J Anim Morphol Physiol 26:307–313
Hamasaki DI, Eder DJ (1977) Adaptive radiation of the pineal system. In: Jung R (ed) Handbook of sensory physiology. Vol III. Springer, Berlin Heidelberg New York, pp 497–548
Hartwig HG (1984) Cyclic renewal of whole pineal photoreceptor outer segments. Ophthalmic Res 16:102–106
Kappers JA (1967) The sensory innervation of the pineal organ in the lizard, Lacerta viridis, with remarks on its position in the trend of pineal phylogenetic structural and functional evolution. Z Zellforsch 81:581–618
Korf HW (1986) Zur Frage photoneuroendokriner Zellen und Systeme. Vergleichende Untersuchungen am Pinealkomplex. Thesis, Faculty of Medicine, Giessen
Korf HW, Oksche A (1986) The pineal organ. In: Pang PKT, Schreibman M (eds) Vertebrate Endocrinology. Fundamentals and biomedical implications. Vol. 1 Morphological considerations. Academic Press, Orlando, pp 104–145
Korf HW, Møller M, Gery I, Zigler JS, Klein DC (1985a) Immunocytochemical demonstration of retinal S-antigen in the pineal organ of four mammalian species. Cell Tissue Res 239:81–85
Korf HW, Foster RG, Ekström P, Schalken JJ (1985b) Opsin-like immunoreaction in the retinae and pineal organs of four mammalian species. Cell Tissue Res 242:645–648
Korf HW, Oksche A, Ekström P, van Veen T, Zigler JS, Gery I, Stein P, Klein DC (1986) S-antigen immunocytochemistry. In: O'Brien P, Klein DC (eds) Pineal and retinal relationships. Academic Press, Orlando, pp 343–355
Kummer-Trost E (1956) Die Bildungen des Zwischenhirndaches der Agamidae, nebst Bemerkungen über die Lagebeziehungen des Vorderhirns. Morph Jb 97:143–192
Lierse W (1965) Elektronenmikroskopische Untersuchungen zur Cytologie und Angiologie des Epiphysenstiels von Anolis carolinensis. Z Zellforsch 65:397–408
Mirshahi M, Boucheix C, Collenot G, Thillaye B, Faure JP (1985) Retinal S-antigen epitopes in vertebrate and invertebrate photoreceptors. Invest Ophthalmol Vis Sci 26:1016–1021
Oksche A (1971) Sensory and glandular elements of the pineal organ. In: Wolstenholme GEW, Knight J (eds) The pineal gland. Churchill Livingstone, Edinburgh, London, pp 127–146
Oksche A, Kirschstein H (1966) Zur Frage der Sinneszellen im Pinealorgan der Reptilien. Naturwissenschaften 53:46
Oksche A, Kirschstein H (1968) Unterschiedlicher elektronenmikroskopischer Feinbau der Sinneszellen im Parietalauge und im Pinealorgan (Epiphysis cerebri) der Lacertilia. Ein Beitrag zum Epiphysenproblem. Z Zellforsch 87:159–192
Petit A (1969) Ultrastructure, innervation et fonction de l'épiphyse de l'orvet (Anguis fragilis L.). Z Zellforsch 96:437–465
Petit A (1976) Contribution à l'étude de l'épiphyse des Reptiles: le complexe épiphysaire des Lacertiliens et l'épiphyse des ophidiens. Étude embryologique, structurale, ultrastructurale; analyse qualitative et quantitative de la sérotonine dans des conditions normales et expérimentales. Thesis, University of Strasbourg
Quay WB (1979) The parietal-pineal complex. In: Gans C, Northcult RG, Ulinski P (eds) Biology of the Reptilia. Vol. 9. Neurology A. Academic Press, London, pp 245–406
Steyn W (1960) Electron microscopic observations on the epiphysial sensory cell problem. Z Zellforsch 51:735–747
van Veen T, Elofsson R, Hartwig HG, Gery I, Mochizuki M, Cena V, Klein DC (1986) Retinal S-antigen: immunocytochemical and immunochemical studies on distribution in animal photoreceptors and pineal organs. Exp Biol 45:15–25
Vigh B, Vigh-Teichmann I (1981) Light and electron microscopic demonstration of immunoreactive opsin in the pinealocytes of various vertebrates. Cell Tissue Res 221:451–463
Vollrath L (1981) The pineal organ. In: Oksche A, Vollrath L (eds) Handbuch mikrosk Anat Mensch. Vol. VI/7. Springer, Berlin Heidelberg New York, pp 1–665
Wartenberg H, Baumgarten HG (1968) Elektronenmikroskopische Untersuchungen zur Frage der photosensorischen und sekretorischen Funktion des Pinealorgans von Lacerta viridis und Lacerta muralis. Z Anat Entw-Gesch 127:99–120
Author information
Authors and Affiliations
Additional information
Supported by the Deutsche Forschungsgemeinschaft (Ko 758/31) and the Deutscher Akademischer Austauschdienst (Senior DAAD Research Fellowship to M.A.H.)
Rights and permissions
About this article
Cite this article
Hafeez, M.A., Korf, H.W. & Oksche, A. Immunocytochemical and electron-microscopic investigations of the pineal organ in adult agamid lizards, Uromastix hardwicki . Cell Tissue Res. 250, 571–578 (1987). https://doi.org/10.1007/BF00218948
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00218948