Skip to main content
Cellular and Molecular Neurobiology logoLink to Cellular and Molecular Neurobiology
. 2002 Feb;22(1):57–85. doi: 10.1023/A:1015393729005

A Cytological Study on the Development of the Different Types of Visual Cells in the Chicken (Gallus domesticus)

Sen Mun Wai 1, David T Yew 1
PMCID: PMC11533763  PMID: 12064518

Abstract

The formation of visual cells and their intracellular organelles was studied in the embryonic chicken (Gallus domesticus) between stage 36 and hatching. Cilia formation was observed at stage 30 and by stage 42, outer segment formation from the cilia was evident. The inner segments appeared as buddings at stage 36. By stage 37, the buddings of double cones were observed clearly and such buddings elongated by stage 42. Both the single cones and rods appeared as buddings by stage 38 and elongation of the buddings was seen by stage 42. Oil droplets initially appeared by stage 39 in accessory cones and were observed in other cones by stage 42. Glycogen bodies were demonstrated firstly in rods and accessory cones at stage 43 and their development was completed by stage 45. In essence, all the essential elements of the visual cells were fully developed by hatching.

Keywords: embryos, chicken, visual cells, cones, rod, oil droplet, glycogen bodies

REFERENCES

  1. Bodega, J. E., Marcí, J. J., and Rebollo, M. A. (1967). ´ Etude histochimique des cellules visuelles chez le poulet. Acta Histochem.26:36–45. [PubMed] [Google Scholar]
  2. Bok,D. (1968). An electron microscopic analysis of migration, division and differentiation of presumptive rat photoreceptors. Anat. Rec.160:319. [Google Scholar]
  3. Bruhn, S. L., and Cepko, C. L. (1996). Development of the pattern of photoreceptors in the chick retina. J. Neurosci. 16:1430–1439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cameron, J. (1905a). The development of the retina in amphibian:Anembryological and cytological study. J. Anat. 39:332–348. [PMC free article] [PubMed] [Google Scholar]
  5. Cameron, J. (1905b). The development of the retina in amphibian: An embryological and cytological study. J. Anat.39:471–488. [PMC free article] [PubMed] [Google Scholar]
  6. Campenhausen, M. V., and Kirschfeld, K. (1998). Spectral sensitivity of the accessory optic system of the pigeon. J. Comp. Physiol. A183:1–6. [Google Scholar]
  7. Carasso, N. (1960). Rôle de l'ergastoplasme dans l' élaboration du glycogéne au cours de la formation du “parabol öide” des cellules visuelles. C.R. Acad. Sci. (Paris) 250:600–602.13807601 [Google Scholar]
  8. Chen, C. M., and Cepko, C. L. (2000). Expression of Chx10 and Chx 10-1 in the developing chicken retina. Mech. Dev. 90:293–297. [DOI] [PubMed] [Google Scholar]
  9. Cooper, T. G., and Meyer, D. B. (1968). Ontogeny of retinal oil droplets in the chick embryo. Exp. Eye Res.7:434–442. [DOI] [PubMed] [Google Scholar]
  10. Coulombre, A. J. (1955). Correlations of structural and biochemical changes in the developing retina of the chick. Am. J. Anat.90:153–190. [DOI] [PubMed] [Google Scholar]
  11. Coulombre, A. J. (1961). Cytology of the developing eye. Int. Rev. Cytol.11:161–190. [DOI] [PubMed] [Google Scholar]
  12. Craig, E., and Eglitis, J. (1963). Observations on the photoreceptor of the frog. Anat. Rec.145:314. [Google Scholar]
  13. DeRobertis,E. (1956). Morphogenesis of retinal rods:Anelectron microscopic study. J. Biophys. Biochem. Cytol. Suppl.2:209–218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. DeRobertis, E., and Lasansky, A. (1958). Comparative submicroscopic morphology of rods and cones. J. Biophys. Biochem. Cytol. 4:743–746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Detwiler, S. S., and Laurens, H. (1921). Histogenesis of the visual cells in Amblystoma. J. Comp. Neurol.33:493–508. [Google Scholar]
  16. Donner, K. O. (1960). On the effect of the colored oil droplets on the spectral sensitivity of the avian retina. In Proc. XIIth Internat. Ornithol. Cong. Helsinki, 1958, pp. 167–172.
  17. Francis, C. M. (1955). Lipids in the retina. J. Comp. Neurol.103:355–384. [DOI] [PubMed] [Google Scholar]
  18. Franz, V. (1913). Die Spirale in den Netzhautstäbchen. Naturwiss21:578–579. [Google Scholar]
  19. Govardovsky, V. I., and Kharkeevitch, T. A. (1966). Electron microscopic investigation of development of photoreceptor outer segments in the chick. J. Evol. Biochem. Physiol. (Russian) 2:37–44. [Google Scholar]
  20. Govardovsky, V. I., and Kharkeevitch, T. A. (1967). Electron microscopic study of the retina in birds (Gallus bankiva domestica). Arkh. Anat. Gistol. Embriol. 52:53–61. [PubMed] [Google Scholar]
  21. Hart, N. S., Partridge, J. C., and Cuthill, I. C. (1999). Visual pigments, cone oil droplets, ocular media and predicted spectral sensitivity in the domestic turkey (Meleagris gallopavo) Vision Res.39:3321–3328. [DOI] [PubMed] [Google Scholar]
  22. Hart, N. S., Partridge, J. C., and Cuthill, I. C. (2000). Retinal asymmetry in birds. Curr. Biol.10:115–117. [DOI] [PubMed] [Google Scholar]
  23. Hudson, R. A., Johnston, D., and Meyer, D. B. (1971). The chemical composition of retinal oil droplets. I. Ophthalmic Res.2:217–222. [Google Scholar]
  24. Keefe, J. R., Ordy, J. M., and Samorajski, T. (1966). Prenatal development of the retina in a diurnal primate (Macaca mulatta). Anat. Rec.154:759–783. [DOI] [PubMed] [Google Scholar]
  25. Klug, H., and Lommatzsch, P. (1967). Vergleichende elektronenmikroskopische Untersuchingen am Innenglied von Stäbchen und Zapfen normaler menschlicher Retina. DeZ. Mikr. Anat. Forsch.77:596–610. [PubMed] [Google Scholar]
  26. Leplat, G. (1913). Les plastosomes des cellules viselles et leur role dans la differentiation des cones et des bâtonnets. Anat. Anz.45:215–221. [Google Scholar]
  27. Lerche,W. (1963). Elektronenmikroskopische untersuchungen zur. Differenzierung des Pigmentepithels und der ausseren Kornerzellen (Sinneszellen) in menschliche Auge. DeZ. Zellforsch.58:953–970. [Google Scholar]
  28. Lerche, W., and Wulle, K. G. (1967). ¨ Uber die Genese der Cilien und der späteren Receptoren-Aussenglieder im embryonalen menschlichen Augenbecher, Albrecht v. DeGraefes Arch. Klin. Exp. Ophthalmol.172:286–292. [DOI] [PubMed] [Google Scholar]
  29. Lowry, O. H., Roberts, N. R., and Lewis, C. (1956). The quantitative histochemistry of the retina. J. Biol. Chem.220:879–892. [PubMed] [Google Scholar]
  30. Magitot, M. A. (1910). ´ FrEtude sur le development de la rétine humaine. Ann. d'Oculist. 143:241–282. [Google Scholar]
  31. Maier, E. J., and Bowmaker, J. K. (1993). Colour vision in the passiform bird, Leothris lutea: Correlation of visual pigment absorbance and oil droplet transmission with spectral sensitivity. J. Comp. Physiol. A172:295–301. [Google Scholar]
  32. Mann, I. (1950). The Development of the Human Eye, Grune & Stratton Inc., New York. [Google Scholar]
  33. Matsusaka, T. (1962). Electron microscopic observations on the cytology and cytochemistry of the paraboloid glycogen in the chick retina. Jpn. J. Ophthalmol.7:238–253. [Google Scholar]
  34. Matsusaka, T. (1966). Some observations on the inner segments of the accessory cone in the chick retina as revealed by the electron microscope. Jpn. J. Ophthalmol.10:72–87. [Google Scholar]
  35. Meller, K., and Breipohl, W. (1965). DeDie Feinstruktur und Differenzierung des inneren Segmentes und des Paraboloids der Photorezeptoren in der Retina von H¨ uhnerembryonen. Z. Zellforsch. 66:673–684. [PubMed] [Google Scholar]
  36. Meyer, D. B., and Cooper, T. G. (1966). The visual cells of the chicken as revealed by phase contrast microscopy. Am. J. Anat.118:723–734. [DOI] [PubMed] [Google Scholar]
  37. Meyer, D. B., Cooper, T. G., and Gernez, C. (1965). Retinal oil droplets. In Rohen, J. W. (ed.), Structure of the Eye. II. Symposium, Schattauer-Verlag, Stuttgt. 8th International Congress of Anatomy.
  38. Meyer, D. B., and May, H. C., Jr. (1973). The topographical distribution of rods and cones in the adult chicken retina. Exp. Eye Res. 17:347–356. [DOI] [PubMed] [Google Scholar]
  39. Moog, F. (1958). Embryogenesis of neural retina. In Rudmek, D. (ed.), Embryonic Nutrition, University of Chicago Press, Chicago. [Google Scholar]
  40. Morris, V. B., and Shorey, C. D. (1967). An electronmicroscopic study of types of receptors in the chick retina. J. Comp. Neurol.129:313–340. [DOI] [PubMed] [Google Scholar]
  41. Müller, C. (1926). Das glycogen der Retina des Frosches. Z. Anat. U. Entw.81:220–238. [Google Scholar]
  42. Nguyen, H., and Anh, J. (1970). Aspects de la synthese du glycogène dans le parabolöide des cellules visuelles de la retine. Bull. Assoc. Anat.148:468-474. [PubMed] [Google Scholar]
  43. Ohashi, Y. (1924). Development of rods and cones of chicken and Anura species. Jpn. Med.World4:257–260. [Google Scholar]
  44. Olson, M. D. (1972). Fine structural development of the chick retina: Early morphogenesis of photoreceptors. Anat. Rec. 172:441. [Google Scholar]
  45. O'Rahilly, R., and Meyer, D. B. (1963). Etude histologie et histochimique des cellules visuelles de la rétine du poulet. Ann. Histochim. 8:281–282. [PubMed] [Google Scholar]
  46. Osorio, D., Vorobyer, M., and Jones, C. D. (1999). Color vision of domestic chicks. J. Exp. Biol.201:2951–2959. [DOI] [PubMed] [Google Scholar]
  47. Piddington, R. (1967). Hormonal effects on the development of glutamine synthetase in the embryonic chick retina. Dev. Biol.16:168–188. [DOI] [PubMed] [Google Scholar]
  48. Prada, J. A., Verastegui, C., Perez-Rios, N., Gonzalez-Moreno, M., and Fdez-Trujillo, F. J. (2000). Thyrotropin-like immunoreactivity in the developing chicken retina. Eur. J. Morphol.38:34–40. [DOI] [PubMed] [Google Scholar]
  49. Rabinovitch, M., Mota, I., and Yoneda, S. (1954). Note on the histochemical localization of glycogen and pentopolynucleotides in the visual cells of the chick (Gallus gallus). Q. J. Microsc. Sci.95:5–10. [Google Scholar]
  50. Rios, H., Lopez-Costa, J. J., Fosser, N. S., Brusco, A., and Saavedra, J. P. (2000). Development of nitric oxide neurons in the chick embryo retina. Dev. Brain Res.120:17–25. [DOI] [PubMed] [Google Scholar]
  51. Sáxen, L. (1955). The glycogen inclusion of the visual cells and its hypothetical role in the photomechanical responses. Acta Anat.25:319–330. [PubMed] [Google Scholar]
  52. Sáxen, L. (1956). Double vision cell formation in amphibian. J. Embryol. Exp. Morphol.4:57–65. [Google Scholar]
  53. Schlosshauer, B., Bauch, H., and Stier, H. (1997). Photoreceptor differentiation analyzed by the novel monoclonal antibody 1G1. Eur. J. Cell Biol.73:150–157. [PubMed] [Google Scholar]
  54. Schultze, M. (1866). FrZür Anatomie und Physiologie der Retina. Arch. Mikr. Anat.2:175–286. [Google Scholar]
  55. Sidman, R., and Wislocki, G. B. (1954). Histochemical observations on rods and cones in the retinas of vertebrates. J. Histochem. Cytochem.2:413–433. [DOI] [PubMed] [Google Scholar]
  56. Smith, R. L., Nishimura, Y., and Raviola, G. (1985). Interreceptor junction in the double cone of the chicken retina. J. Submicro. Cyto. Path.17:183–186. [PubMed] [Google Scholar]
  57. Strother, G. K., and Wolken, J. J. (1960). Microspectrophotometry. I absorption spectra of colored oil globules in the chicken retina. Exptl. Cell. Res.21:504–512. [Google Scholar]
  58. Szel, A., Takacs, L., Monostori, E., Vigh-Teichmann, I., and Rohlich, P. (1985). Heterogeneity of chicken photoreceptors as defined by hybridoma supernatants. An immunocytochemical study. Cell Tissues Res.240:735–741. [DOI] [PubMed] [Google Scholar]
  59. Szel, A., van Veen T., and Rohhch, P. (1994). Retinal cone differentiation. Nature370:336. [DOI] [PubMed] [Google Scholar]
  60. Tokayama, T. (1960). Comparative anatomy of vertebrate visual cells by electron microscopy. Acta Soc. Ophthal. Jpn.64:1310–1319. [Google Scholar]
  61. Tokuyasu, K., and Yamada, E. (1959). The fine structure of the retina studies with the electron microscope. IV. Morphogenesis of outer segments of retinal rods. J. Biophys. Biochem. Cytol.6:225–230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Ueno, K. (1960). Morphogenesis of the retinal cone studies with electron microscope. Acta Soc. Ophathal. Jpn.64:260–277. [Google Scholar]
  63. Vorobyer, M., and Osorio, D. (1998). Receptor noise as a determinant of colour thresholds. Proc. R. Soc. London B. Biol. Sci.265:351–359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Wada, H. (1965). The fine structure of the retinal visual cells with the electron microscope. Part I. Electrton microscopic observations of visual cells of normal chick embryo. Nagoya Med. J.11:11–18. [PubMed] [Google Scholar]
  65. Wald, G. (1948). Galloxanthin: A carotenoid from the chicken retina. J. Gen. Physiol.31:377–383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Walls, G. C., and Judd, H. D. (1933). The intracellular filters of vertebrates. Brit. J. Ophthalmol.17: 641–675,703–723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Weidman, T. A., and Kuwabara, T. (1969). Development of the rat retina. Invest. Ophthalmol.8:60–69. [PubMed] [Google Scholar]
  68. Wislocki,G., and Sidman, R. (1954). The chemical morphology of the retina. J. Comp. Neurol.101:53–100. [DOI] [PubMed] [Google Scholar]
  69. Yamada, E., Tokuyasu, K., and Iwaki, S. (1958). The fine structure of the retina studied with electron microscope. III. Human retina. J. Kurume Med. Assoc.21:1979–2027. [Google Scholar]
  70. Yoshizawa, T., and Kuwata, O. (1991). Iodopsin, a red sensitive cone visual pigment in the chicken retina. Photochem. Photobiol. 54:1061–1070. [DOI] [PubMed] [Google Scholar]
  71. Young, R.W. (1965). Renewal of photoreceptor outer segments. Anat. Rec.151:484. [Google Scholar]

Articles from Cellular and Molecular Neurobiology are provided here courtesy of Springer

RESOURCES