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Ontogenetic development of the pineal organ, parapineal organ, and retina of the three-spined stickleback, Gasterosteus aculeatus L. (Teleostei)

Development of photoreceptors

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Summary

The ontogenetic developments of the pineal organ, parapineal organ, and retina were studied by the use of light and electron microscopy in embryos and fry of the teleost, Gasterosteus aculeatus, from 60 to 168 h after fertilization. Sixty to 66 h after fertilization, the primordium of the pineal complex is discernible in the diencephalic roofplate; the parapineal anlage is located rostral to the pineal anlage. Photoreceptor cells endowed with outer segments are present in the embryonic pineal organ already after 72 h, whereas outer segments of retinal photoreceptors could not be demonstrated before 144 h (hatching occurs between 120–144 h). Furthermore, neuropil formations with synaptic specializations are present in the rostral part of the pineal organ 108 h after fertilization. At 72 h, the embryonic parapineal parenchyma is already differentiated into parapinealocytes, which give rise to the parapineal tract, and glia-resembling elements. Although parapinealocytes carry cilia (9 × 2 + 0), only a single outer segment of the photoreceptor type could be demonstrated in the parapineal organ of one adult stickleback. Photoreceptors present in the pineal organ of unhatched embryos are hardly involved in visual functions, but may already at this early developmental stage serve as photoneuroendocrine transducers.

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References

  • Belsare DK (1974) Studies on the development of endocrine glands in fishes. II. Development of the pineal organ in Clarias batrachus L. Anat Anz 136:268–273

    Google Scholar 

  • Blaxter JHS (1975) The eyes of larval fish. In: Ali MA (ed) Vision in fishes. Plenum Press, New York London, pp 427–443

    Google Scholar 

  • Borg B (1982) Extraretinal photoreception involved in photoperiod effects on reproduction in male three-spined sticklebacks, Gasterosteus aculeatus. Gen Comp Endocrinol 47:84–87

    Google Scholar 

  • Dodt E (1963) Photosensitivity of the pineal organ in the teleost, Salmo irideus (Gibbons). Experientia 19:642–643

    Google Scholar 

  • Ekström P, van Veen Th (1983) Central connections of the pineal organ in the three-spined stickleback, Gasterosteus aculeatus L. (Teleostei). Cell Tissue Res, in press

  • Falcon J, Geffard M, Juillard M-T, Delaage M, Collin J-P (1981) Melatonin-like immunoreactivity in photoreceptor cells. A study in the teleost pineal organ and the concept of photoneuroendocrine cells. Biol Cell 42:65–68

    Google Scholar 

  • Gern WA, Ralph CL (1979) Melatonin synthesis by the retina. Science 204:183–184

    Google Scholar 

  • Gern WA, Owens DW, Ralph CL (1978 a) Persistence of the nychthemeral rhythm of melatonin secretion in pinealectomized or optic tract-sectioned trout (Salmo gairdneri). J Exp Zool 205:371–376

    Google Scholar 

  • Gern WA, Owens DW, Ralph CL (1978b) The synthesis of melatonin by the trout retina. J Exp Zool 206:263–270

    Google Scholar 

  • Goudie CA, Davis KB, Simco BA (1983) Influence of the eyes and pineal gland on locomotor activity patterns of channel catfish, Ictalurus punctatus. Physiol Zool 56:10–17

    Google Scholar 

  • Grün G (1982) The development of the vertebrate retina: a comparative survey. Adv Anat Embryol Cell Biol 78:1–85

    Google Scholar 

  • Hafeez MA, Quay WB (1969) Histochemical and experimental studies of 5-hydroxytryptamine in pineal organs of teleosts (Salmo gairdneri and Atherinopsis californiensis). Gen Comp Endocrinol 13:211–217

    Google Scholar 

  • Hafeez MA, Zerihun L (1974) Studies on central projections of the pineal nerve tract in rainbow trout, Salmo gairdneri Richardson, using cobalt chloride iontophoresis. Cell Tissue Res 154:485–510

    Google Scholar 

  • Hartwig HG, Oksche A (1982) Neurobiological aspects of extraretinal photoreceptive systems: structure and function. Experientia 38:991–996

    Google Scholar 

  • Herwig HJ (1980) Comparative ultrastructural observations on the pineal organ of the pipefish, Syngnathus acus and the seahorse, Hippocampus hudsonius. Cell Tissue Res 209:187–200

    Google Scholar 

  • Herwig HJ (1981) The pineal organ. An ultrastructural and biochemical study of Hemigrammus caudovittatus and other closely related characid fish species with special reference to the Mexican blind cave fish, Astyanax mexicanus. Thesis, Utrecht

  • Hill C (1981) Development of the epiphysis in Coregonus albus. J Morphol 5:503–510

    Google Scholar 

  • Holmgren U (1965) On the ontogeny of the pineal- and parapineal organs in teleost fishes. Prog Brain Res 10:172–182

    Google Scholar 

  • Kavaliers M (1980a) Retinal and extraretinal entrainment spectra for the activity rhythms of the lake chub, Couesius plumbeus. Behav Neural Biol 30:56–67

    Google Scholar 

  • Kavaliers M (1980b) Extraretinal mediation of responses to temperature and light in hatchling alligators. J Comp Physiol 136:243–246

    Google Scholar 

  • Kavaliers M (1980c) Circadian rhythm of extraretinal photosensitivity in hatchling alligators, Alligator mississippiensis. Photochem Photobiol 32:67–70

    Google Scholar 

  • Kavaliers M (1980d) Circadian locomotor activity rhythms of the burbot, Lota lota: Seasonal differences in period length and the effect of pinealectomy. J Comp Physiol 136:215–218

    Google Scholar 

  • Kelly DE (1965) Ultrastructure and development of amphibian pineal organs. Prog Brain Res 10:270–287

    Google Scholar 

  • Klein DC, Namboodiri MAA, Auerbach DA (1981) The melatonin rhythm generating system: developmental aspects. Life Sci 28:1975–1986

    Google Scholar 

  • Korf HW (1974) Acetylcholinesterase-positive neurons in the pineal and parapineal organs of the rainbow trout, Salmo gairdneri (with special reference to the pineal tract). Cell Tissue Res 155:475–489

    Google Scholar 

  • McNulty JA, Nafpaktitis BG (1976) The structure and development of the pineal complex in the lanternfish Triphoturus mexicanus (family Myctophidae). J Morphol 150:579–606

    Google Scholar 

  • Moore RY, Klein DC (1974) Visual pathways and the central neural control of a circadian rhythm in pineal serotonin N-acetyltransferase activity. Brain Res 71:17–33

    Google Scholar 

  • Nilsson SEG, Crescitelli F (1970) A correlation of ultrastructure and function in the developing retina of the frog tadpole. J Ultrastruct Res 30:87–102

    Google Scholar 

  • Oksche A, Kirschstein H (1971) Weitere elektronenmikroskopische Untersuchungen am Pinealorgan von Phoxinus laevis (Teleostei, Cyprinidae). Z Zellforsch 112:572–588

    Google Scholar 

  • Oksche A, Ueck M, Rüdeberg C (1971) Comparative ultrastructural studies of sensory and secretory elements in pineal organs. In: Heller H, Lederis K (eds) Subcellular organization and function in endocrine tissues. Mem Soc Endocrinol 19:7–25

  • Oliver J, Baylé JD (1982) Brain photoreceptors for the photo-induced testicular response in birds. Experientia 38:1021–1029

    Google Scholar 

  • Omura Y, Oguri M (1971) The development and degeneration of the photoreceptor outer segment of the fish pineal organ. Bull Jpn Soc Sci Fish 37:851–860

    Google Scholar 

  • Owman C, Rüdeberg C (1970) Light, fluorescence, and electron microscopic studies on the pineal organ of the pike, Esox lucius L., with special regard to 5-hydroxytryptamine. Z Zellforsch 107:522–550

    Google Scholar 

  • Pittendrigh CS (1974) Circadian oscillations in cells and the circadian organization of multicellular systems. In: Schmitt FO, Worden FG (eds) The neurosciences: third study program. MIT Press, Cambridge Mass., pp 437–458

    Google Scholar 

  • Richardson KC, Jarret L, Finke EH (1960) Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 35:313–323

    CAS  PubMed  Google Scholar 

  • Rüdeberg C (1969) Structure of the parapineal organ of the adult rainbow trout, Salmo gairdneri Richardson. Z Zellforsch 93:282–304

    Google Scholar 

  • Scharrer E (1964) Photo-neuro-endocrine systems: general concepts. Ann N Y Acad Sci 117:13–22

    Google Scholar 

  • Ueck M, Kobayashi H (1979) Neue Ergebnisse zu Fragen der vergleichenden Epiphysenforschung. Verh Anat Ges 73:961–963

    Google Scholar 

  • Underwood H, Groos G (1982) Vertebrate circadian rhythms: retinal and extraretinal photoreception. Experientia 38:1013–1021

    Google Scholar 

  • Veen Th van (1982) The parapineal and pineal organs of the elver (glass eel), Anguilla anguilla L. Cell Tissue Res 222:433–444

    Google Scholar 

  • Veen Th van, Hartwig HG, Müller K (1976) Light-dependent motor activity and photonegative behavior in the eel (Anguilla anguilla L.). Evidence for extraretinal and extrapineal photoreception. J Comp Physiol 111:209–219

    Google Scholar 

  • Veen Th van, Ekström P, Borg B, Møller M (1980) The pineal complex of the three-spined stickleback, Gasterosteus aculeatus L. A light-, electron microscopic and fluorescence histochemical investigation. Cell Tissue Res 209:11–28

    Google Scholar 

  • Veen Th van, Laxmyr L, Borg B (1982) Diurnal variation of 5-hydroxytryptamine content in the pineal organ of the yellow eel, (Anguilla anguilla (L.)). Gen Comp Endocrinol 46:322–326

    Google Scholar 

  • Vigh-Teichmann I, Röhlich P, Vigh B, Aros B (1980) Comparison of the pineal complex, retina and cerebrospinal fluid contacting neurons by immunocytochemical antirhodopsin reaction. Z mikrosk anat Forsch 94:623–640

    Google Scholar 

  • Vigh-Teichmann I, Korf H-W, Oksche A, Vigh B (1982) Opsin-immunoreactive outer segments and acetylcholinesterase-positive neurons in the pineal complex of Phoxinus phoxinus (Teleostei, Cyprinidae). Cell Tissue Res 227:351–369

    Google Scholar 

  • Vigh-Teichmann I, Korf H-W, Nürnberger F, Oksche A, Vigh B, Olsson R (1983) Opsinimmunoreactive outer segments in the pineal and parapineal organs of the lamprey (Lampettra fluviatilis), the eel (Anguilla anguilla), and the rainbow trout (Salmo gairdneri). Cell Tissue Res 230:289–307

    Google Scholar 

  • Vollrath L (1981) The pineal organ. In: Oksche A, Vollrath L (eds) Handbuch der mikroskopischen Anatomie des Menschen. Band 6/7. Springer-Verlag, Berlin Heidelberg New York

    Google Scholar 

  • Wake K (1973) Acetylcholinesterase-containing nerve cells and their distribution in the pineal organ of the goldfish, Carassius auratus. Z Zellforsch 145:287–298

    Google Scholar 

Download references

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Supported by grants from the Swedish Natural Science Research Council (4644-103), and the Royal Physiographical Society in Lund

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Ekström, P., Borg, B. & van Veen, T. Ontogenetic development of the pineal organ, parapineal organ, and retina of the three-spined stickleback, Gasterosteus aculeatus L. (Teleostei). Cell Tissue Res. 233, 593–609 (1983). https://doi.org/10.1007/BF00212227

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