Extraocular Photoreception

  • Jerome J. Wolken
  • Mary A. Mogus


We live in a world of light, which greatly affects the behavior of all life on earth. In animals, information about the external world is obtained through the eye and other sensory receptors. Animals move and orient with respect to the light stimulus, and the regularity in the light-dark periods are signals for circadian rhythms. These photobehavioral responses provide a means to find an appropriate environment, to search for food, and to escape from enemies; light also affects growth, maturation, and reproduction—all necessary for the animals’ survival.


Circadian Rhythm Spectral Sensitivity Frog Skin Pigment Granule Pineal Organ 
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. Adler, K., and Taylor, D. H., 1973, Extraocular perception of polarized light by orienting salamanders, J. Comp. Physiol. 87:203–212.CrossRefGoogle Scholar
  2. Andersen, M. C., and Brown, A. M., 1979, Photoresponses of a sensitive extraretinal photoreceptor in Aplysia, J. Physiol. 287:267–282.Google Scholar
  3. Austin, G., Yai, H., and Sato, M., 1967, Calcium ion effects on Aplysia membrane ion potentials, in: Invertebrate Nervous System (C. A. G. Wiersma, ed.), pp. 39–53, University of Chicago Press, Chicago.Google Scholar
  4. Baumann, F. A., Mauro, A., Milecchia, R., Nightingale, S., and Young, J. Z., 1970, The extraocular receptors of squids Todarodes and Illex, Brain. Res. 21:275–279.CrossRefGoogle Scholar
  5. Benjamin, P. R., and Walker, J. S., 1972, Two pigments in the brain of a freshwater pulmonate snail, Comp. Biochem. Physiol. 41B:813–821.Google Scholar
  6. Bennett, M. F., 1979, Extraocular light receptors and circadian rhythms, in: Handbook of Sensory Physiology. Vol. 7/6A, Vision in Invertebrates, A: Invertebrate Photoreceptors (H. Autrum, ed.), pp. 641–663, Springer-Verlag, Berlin.Google Scholar
  7. Block, G. D., and Lickey, M. E., 1973, Extraocular photoreceptors and oscillators can control the circadian rhythm of behavioral activity in Aplysia, J. Comp. Physiol. 86:367–374.CrossRefGoogle Scholar
  8. Brown, A. M., Baur, P. S., Jr., and Tully, F. H., Jr., 1975, Phototransduction in Aplysia neurons: Calcium release from pigmented granules is essential, Science 188:157–160.CrossRefGoogle Scholar
  9. Bruno, M. S., and Kennedy, D., 1962, Spectral sensitivity of photoreceptor neurons in the sixth ganglion of the crayfish, Comp. Biochem. Physiol. 6:41–46.CrossRefGoogle Scholar
  10. Chalazonitis, N., 1964, Light energy conversion in neuronal membranes, Photochem. Photobiol. 3:539–559.CrossRefGoogle Scholar
  11. Chase, R., 1979, Photic sensitivity of the rhinophore in Aplysia, Can. J. Zool. 57:698–701.CrossRefGoogle Scholar
  12. Croll, N. A., 1966, The phototactic response and spectral sensitivity of Chromadorina viridis (Nematoda, Chromadorida) with a note on the nature of paired pigment spots, Nematologica 12:610–614.CrossRefGoogle Scholar
  13. Croll, N. A., Evans, A. A. F., and Smith, J. M., 1975, Comparative nematode photoreceptors, Comp. Biochem. Physiol. 51A:139–143.CrossRefGoogle Scholar
  14. Deguchi, T., 1979, A circadian oscillator in cultured cells of chicken pineal gland, Nature 282:94–96.CrossRefGoogle Scholar
  15. Dilly, P. N., and Wolken, J. J., 1973, Studies on the receptors in Ciona intestinalis IV: The ocellus in the adult, Micron 4:11–29.Google Scholar
  16. Dodt, E., and Jacobson M., 1963, Photosensitivity of a localized region of the frog Diencephalon, J. Neurophysiol. 26:752–758.Google Scholar
  17. Dumortier, B., 1972, Photoreception in the circadian rhythm of stridulatory activity in Ephippiger, J. Comp. Physiol. 77:81–112.CrossRefGoogle Scholar
  18. Eakin, R. M., 1973, The Third Eye, University of California Press, Berkeley, Calif.Google Scholar
  19. Eldred, W. D., and Nolte, J., 1978, Pineal photoreceptors: Evidence for a vertebrate visual pigment with two physiologically active states, Vis. Res. 18:29–32.CrossRefGoogle Scholar
  20. Engbretson, G. A., and Lent, C. M., 1976, Parietal eye of the lizard: Neuronal photoresponses and feedback from the pineal gland, Proc. Natl. Acad. Sci. U.S.A. 73:654–657.CrossRefGoogle Scholar
  21. Erlanger, P. F., 1976, Photoregulation of biologically active macromolecules, Annu. Rev. Biochem. 45:267–283.CrossRefGoogle Scholar
  22. Geethabali, X., and Rao, K. P., 1973, A metasomatic neural photoreceptor in the scorpion, J. Exp. Biol. 58:189–196.Google Scholar
  23. Gotow, T., 1975, Morphology and function of photoexcitable neurons in the central ganglia of Onchidium verruculatum, J. Comp. Physiol. 99:139–157.CrossRefGoogle Scholar
  24. Gwilliam, G. F., 1969, Electrical responses to photo stimulation in the eyes and nervous system of nerid polychaetes, Biol. Bull. 136:385–397.CrossRefGoogle Scholar
  25. Hamasaki, D. I., and Streck, P., 1971, Properties of the epiphysis cerebri of the small spotted dogfish shark Scyliorhinus caniculus L., Vis. Res. 11:189–198.CrossRefGoogle Scholar
  26. Hara, T., and Hara, R., 1980, Retinochrome and rhodopsin in the extraocular photoreceptor of the squid Todarodes, J. Gen. Physiol. 75:1–19.CrossRefGoogle Scholar
  27. Harth, M. S., and Heaton, M. B., 1973, Nonvisual photoresponsiveness in newly hatched pigeons (Columba livid), Science 180:753–755.CrossRefGoogle Scholar
  28. Hartwig, H. G., and Baumann, C., 1974, Evidence for photosensitive pigments in the pineal complex of the frog, Vis. Res. 14:597–598.CrossRefGoogle Scholar
  29. Hisano, N., Tateda, H., and Kubara, M., 1972a, Photosensitive neurons in the marine pulmonate mollusk Onchidium verruculatum, J. Exp. Biol. 57:651–660.Google Scholar
  30. Hisano, N., Tateda, H., and Kubara, M., 1972b, An electrophysiological study of the photo-excitable neurons of Onchidium verruculatum in situ, J. Exp. Biol. 57:661–671.Google Scholar
  31. Hisano, N., Cardinalli D. P., Rosner, J. M., Nagle, C. A., and Tremezzani, J. H., 1972c, Pineal role in the duck extraretinal photoreception, Endocrinology 91:1318–1322.CrossRefGoogle Scholar
  32. Kraughs, J. M., Sordhal, L. A., and Brown, A. M., 1977, Isolation of pigment granules involved in extra-retinal photoreception in Aplysia californica neurons, Biochim. Biophys. Ada 471:25–31.CrossRefGoogle Scholar
  33. Krinsky, N. I., 1976, Cellular damage initiated by visible light, in The Survival of Vegetative Microbes (G. R. Grey and J. R. Postgate, eds.), pp. 209–239, Cambridge University Press, Cambridge.Google Scholar
  34. Justis, C. S., and Taylor, D. H., 1976, Extraocular photoreception and compass orientation in larval bullfrogs Rana catesbeinana, Copeia (1):98–125.CrossRefGoogle Scholar
  35. Larimer, J. L., Trevino, D. L., and Ashby, F. A., 1966, A comparison of spectral sensitivities of caudal photoreceptors of epigeal and cavenicolous crayfish, Comp. Biochem. Physiol. 19:409–415.CrossRefGoogle Scholar
  36. Lickey, M. E., and Zack, S., 1973, Extraocular photoreceptors can entrain the circadian rhythm in the abdominal ganglion of Aplysia, J. Comp. Physiol. 86:361–366.CrossRefGoogle Scholar
  37. Lickey, M. E., Block, G. D., Hudson, D. J., and Smith, J. T., 1976, Circadian oscillators and photoreceptors in the gastropod, Aplysia, Photochem. Photobiol. 23:253–257.CrossRefGoogle Scholar
  38. Marks, P. S., 1976, Nervous control of light responses in the sea anemone, Calamactis praelongus, J. Exp. Biol. 65:85–96.Google Scholar
  39. Mauro, A., 1977, Extraocular photoreceptiors in cephalopods, Symp. Zool. Soc. Lond. 38:287–308.Google Scholar
  40. Mauro, A., and Baumann, F., 1968, Nervous control of light responses of photoreceptors in the epistellar body of Eledone moschata, Nature 220:1332–1334.CrossRefGoogle Scholar
  41. Mauro, A., and Sten-Knudsen, A., 1972, Light-evoked impulses from extra-ocular photoreceptors in the squid Todarodes, Nature 33:342–343.CrossRefGoogle Scholar
  42. Menaker, M. (ed.), 1976, Extraretinal photoreception, Photochem. Photobiol. 23(4): 213-306.Google Scholar
  43. Menaker, M., 1977, Extra-retinal photoreceptors, in The Science of Photobiology (K. C. Smith, ed.), pp. 227–240, Plenum Press, New York.CrossRefGoogle Scholar
  44. Menaker, M., and Underwood, H., 1976, Extraretinal photoreception in birds, Photochem. Photobiol. 23:299–306.CrossRefGoogle Scholar
  45. Messenger, J. B., 1967, Parolfactory vesicles as photoreceptors in a deep sea squid, Nature 213:836–838.CrossRefGoogle Scholar
  46. Meyer, J. R., 1977, Head capsule transmission of long-wavelength light in the Curculionidae, Science 196:524–525.CrossRefGoogle Scholar
  47. McCrone, E. J., and Sokolove, P. G., 1979, Brain-gonad axis and photoperiodically-stimulated sexual maturation in the slug, Umax maximus, J. Comp. Physiol. 133:117–123.CrossRefGoogle Scholar
  48. McMillan, J. P., Elliot, J. A., and Menaker, M., 1975a, On the role of eyes and brain photoreceptors in the sparrow: Aschoff’s rule, J. Comp. Physiol. 102:257–262.CrossRefGoogle Scholar
  49. McMillan, J. P., Elliot, J. A., and Menaker, M., 1975b, On the role of eyes and brain photoreceptors in the sparrow: Arrhythmicity in constant light, J. Comp. Physiol. 102:2623–2268.Google Scholar
  50. Millott, N., 1968, The dermal light sense, in: Invertebrate Receptors (J. D. Carthy and G. E. Newell, eds.), pp. 1–36, Academic Press, New York.Google Scholar
  51. Millott, N., 1978, Extra-ocular Photosensitivity, Meadowfield Press, Burham, England.Google Scholar
  52. Ninneman, H., 1980, Blue light photoreceptors, Bioscience 30:166–170.CrossRefGoogle Scholar
  53. O’Benar, J. D., and Matsumoto, Y., 1976, Light induced neural activity and muscle contraction in the marine worm Golfingia gouldii, Comp. Biochem. Physiol. 55A:77–81.CrossRefGoogle Scholar
  54. Palmer, J., 1974, Biological Clocks in Marine Organisms, Wiley, New York.Google Scholar
  55. Ralph, C. L., Firth, B. T., Gern, W. A., and Owens, D. W., 1979, The pineal complex and thermoregulation, Biol. Rev. 54:41–72.CrossRefGoogle Scholar
  56. Rayport, S., and Wald, G., 1978, Frog skin photoreceptors, Am. Soc. Photobiol. Abstr. 6:94–95.Google Scholar
  57. Steven, D. M., 1963, The dermal light sense, Biol. Rev. 38:204–240.CrossRefGoogle Scholar
  58. Taylor, D. H., 1972, Extra-optic photoreception and compass orientation in larval and adult salamanders (C. Ambystoma tigrinum), Anim. Behav. 20:233–236.CrossRefGoogle Scholar
  59. Taylor, D. H., and Ferguson, D. E., 1970, Extraoptic celestial orientation in the southern cricket frog Acris gryllus, Science 170:390–392.CrossRefGoogle Scholar
  60. Truman, J. W., 1976, Extraretinal photoreception in insects, Photochem. Photobiol. 23:215–225.CrossRefGoogle Scholar
  61. Turek, F. W., 1975, Extraretinal photoreception during gonadal photorefractory period in the gold-crowned sparrown, J. Comp. Physiol. 96:27–36.CrossRefGoogle Scholar
  62. Underwood, H., 1977, Circadian organization in lizards: The role of the pineal organ, Science 195:587–589.CrossRefGoogle Scholar
  63. Underwood, H., and Menaker, M., 1976, Extraretinal photoreception in lizards, Photochem. Photobiol. 23:227–244.CrossRefGoogle Scholar
  64. Underwood, H., and Menaker, M., 1970, Extraretinal light perception: Entrainment of the biological clock controlling locomotor activity, Science 170:190–193.CrossRefGoogle Scholar
  65. Uchizono, K., 1962, The structure of possible photoreceptive elements in the sixth abdominal ganglion of the crayfish, J. Cell. Biol. 15:151–154.CrossRefGoogle Scholar
  66. Van Brunt, E. E., Shepherd, M. D., Wall, J. R., Ganong, W. F., and Clegg, M. T., 1964, Penetration of light into the brain of mammals, Ann. N.Y. Acad. Sci. 117:204–216.Google Scholar
  67. Van Veen, Th., Hartwig, H. G., and Muller, K., 1976, Light-dependent motor activity and photonegative behavior in the eel, J. Comp. Physiol. 11A:209–219.CrossRefGoogle Scholar
  68. Watanabe, M., 1980, An autoradiographic, biochemical and morphological study of the Harderian gland of the mouse, J. Morphol. 163:349–365.CrossRefGoogle Scholar
  69. Weiderhold, M. L., MacNichol, E. F., Jr., and Bell, A. L., 1973, Photoreceptor spike response in the hardshell clam, Mercenaria mercenaria, J. Gen. Physiol. 61:24–55.CrossRefGoogle Scholar
  70. Wetterberg, L., Geller, E., and Yuwiler, A., 1970a, Harderian gland: An extraretinal photoreceptor influencing pineal gland in neonatal rats, Science 170:194–196.CrossRefGoogle Scholar
  71. Wetterberg, L., Yuwiler, A., Ulrich, R., Geller, E., and Wallace, R., 1970b, Harderian gland: Influence on pineal hydroxyindole-O-methyltransferase activity in neonatal rats, Science 171:194–196.CrossRefGoogle Scholar
  72. Wilkins, L. A., and Larimer, J. S., 1972, The CNS photoreceptor of crayfish: Morphology and synaptic activity, J. Comp. Biol. 80:389–407.Google Scholar
  73. Wolken, J. J., 1975, Photoprocesses, Photoreceptors and Evolution, Academic Press, New York.Google Scholar
  74. Wolken J. J., 1971, Invertebrate Photoreceptors: A Comparative Analysis, Academic Press, New York.Google Scholar
  75. Wolken, J. J., and Mogus, M. A., 1979, Extra-ocular photosensitivity, Photochem. Photobiol. 29:189–196.CrossRefGoogle Scholar
  76. Wurtman, R. J., 1975, The effects of light on the human body, Sci. Am. 233:68–77.CrossRefGoogle Scholar
  77. Wurtman, R. J., Axelrod, J., and Kelly, D. E., 1968, The Pineal, Academic Press, New York.Google Scholar
  78. Yoshida, M., 1979, Extraocular photoreception, in: Handbook of Sensory Physiology, Vol. 7/6A, Vision in Invertebrates, A: Invertebrate Photoreceptors (H. Autrum, ed.), pp. 581–640, Springer-Verlag, Berlin.Google Scholar

Copyright information

© Plenum Press, New York 1981

Authors and Affiliations

  • Jerome J. Wolken
    • 1
  • Mary A. Mogus
    • 2
  1. 1.Department of Biological Sciences, Mellon College of ScienceCarnegie-Mellon UniversityPittsburghUSA
  2. 2.Department of PhysicsEast Stroudsburg State CollegeEast StroudsburgUSA

Personalised recommendations