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Chronobiology International
The Journal of Biological and Medical Rhythm Research
Volume 21, 2004 - Issue 4-5
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REVIEW

Extraocular Photoreception and Circadian Entrainment in Nonmammalian Vertebrates

& , Ph.D.
Pages 501-519 | Published online: 07 Jul 2009

References

  • Adler K. Pineal end organ: role in extraoptic entrainment of circadian locomotor rhythms in frogs. Biochronometry, M. Menaker. U.S. National Academy of Science, Washington, DC 1993; 342–350
  • Aschoff J., Daan S., Homna K. I. Zeitgeber, entrainment, and masking: some unsettled questions. Vertebrate Circadian System (Structure and Physiology), J. Aschoff, S. Daan, G. A. Groos. Springer-Verlag, Berlin, Heidelberg, New York 1982; 13–24
  • Aspengren S., Skold H. N., Quiroga G., Martensson L., Wallin M. Noradrenaline- and melatonin-mediated regulation of pigment aggregation in fish melanophores. Pigment Cell Res. 2003; 16(1)59–64, [CSA]
  • Beinot J. Stimulation par la lumiére artificielle du développement testiculaire chez des canards aveugles per section du nerf optique. CR Soc. Biol. (Paris). 1935; 120: 133–136, [CSA]
  • Bellingham J., Foster R. G. Opsin and mammalian photoentrainment. Cell Tissue Res. 2002; 309(1)57–71, [CROSSREF], [CSA]
  • Bellingham J., Whitmore D., Philp A. R., Wells D. J., Foster R. G. Zebrafish melanopsin: isolation, tissue localization and phylogenetic position. Mol. Brain Res. 2002; 107(2)128–136, [CROSSREF], [CSA]
  • Bertolucci C., Wagner G., Foa A., Gwinner E., Brandstätter R. Photoperiod affects amplitude but not duration of in vitro melatonin production in the ruin lizard (Podarcis sicula). J. Biol. Rhythms 2003; 18: 63–70, [CROSSREF], [CSA]
  • Bissinger B. E. Role of the parietal eye in the homing behavior of lizards. American Zoologist 1980; 20: 842
  • Blackshaw S., Snyder S. H. Parapinopsin, a novel catfish opsin localized to the parapineal organ, defines a new gene family. J. Neurosci. 1997; 17: 8083–8092
  • Bolliet V., Ali M. A., Anctil M., Zachmann A. Melatonin secretion in vitro from the pineal complex of the lamprey Petromyzon marinus. Gen. Comp. Endocrinol. 1993; 89(1)101–106, [CROSSREF]
  • Bolliet V., Ali M. A., Lapointe F. J., Falcon J. Rhythmic melatonin secretion in different teleost species: an in vitro study. J. Comp. Physiol. B 1996; 165(8)677–683, [CROSSREF], [CSA]
  • Brandstätter R. Encoding time of day and time of year by the avian circadian system. J. Neuroendocrinol. 2003; 15(4)398–404, [CROSSREF], [CSA]
  • Brandstätter R., Kumar V., Van’t Hof T. J., Gwinner E. Photoperiodic information acquired and stored in vivo is retained in vitro by a circadian oscillator, the avian pineal gland. Proc. Natl. Acad. Sci. USA 2000; 97(22)12324–12328, [CROSSREF], [CSA]
  • Cahill G. Circadian organization in fish and Amphibians. Biological Rhythms, V. Kumar. Narosa Publishing House, New Delhi 2002; 120–128
  • Cole W. C., Youson J. H. The effect of pinealectomy, continuous light, and continuous darkness on metamorphosis of anadromous sea lampreys, Petromyzon marinus L. J. Exp. Zool. 1981; 218(3)397–404
  • Coon S. L., Begay V., Falcon J., Klein D. C. Expression of melatonin synthesis genes is controlled by a circadian clock in the pike pineal organ but not in the trout. Biol. Cell 1998; 90(5)399–405, [CROSSREF], [CSA]
  • Daniolos A., Lerner A. B., Lerner M. R. Action of light on frog pigment cells in culture. Pigment Cell Res. 1990; 3(1)38–43
  • de Miguel E., Rodicio M. C., Anadon R. Organization of the visual system in larval lampreys: an HRP study. J. Comp. Neurol. 1990; 302(3)529–542, [CSA]
  • Deutschlander M. E., Borland S. C., Phillips J. B. Extraocular magnetic compass in newts. Nature 1999; 400(6742)324–325, [CROSSREF]
  • Drivenes O., Soviknes A. M., Ebbesson L. O., Fjose A., Seo H. C., Helvik J. V. Isolation and characterization of two teleost melanopsin genes and their differential expression within the inner retina and brain. J. Comp. Neurol. 2003; 456(1)84–93, [CROSSREF], [CSA]
  • Ellis-Quinn B. A., Simon C. A. Lizard homing behavior: the role of the parietal eye during displacement and radio-tracking, and time-compensated celestial orientation in the lizard Sceloporus jarrovi. Behav. Ecol. Sociobiol. 1991; 28: 397–407, [CROSSREF], [CSA]
  • Engbretson A. Neurobiology of the lacertilian parietal eye system. Ethol. Ecol. Evol. 1992; 4: 89–107, [CSA]
  • Foà A. The role of the pineal and the retinae in the expression of circadian locomotor rhythmicity in the ruin lizard, Podarcis sicula. J. Comp. Physiol. A 1991; 169: 201–207, [CROSSREF]
  • Foà A., Flamini M., Innocenti A., Minutini L., Monteforti G. The role of the extraretinal photoreception in the circadian system of the ruin lizards Podarcis sicula. Comp. Bioch. Physiol. 1993; 105A: 223–230
  • Forsell J., Holmqvist B., Ekstrom P. Molecular identification and developmental expression of UV and green opsin mRNAs in the pineal organ of the Atlantic halibut. Dev. Brain Res. 2002; 136(1)51–62, [CROSSREF], [CSA]
  • Foster R. G., Follett B. K. The involvement of a rhodopsin-like photopigment in the photoperiodic response of the japanese quail. J. Comp. Physiol. A 1985; 157: 519–528, [CROSSREF], [CSA]
  • Foster R. G., Hankins M. W. Non-rod, noncone photoreception in the vertebrates. Prog. Retin. Eye Res. 2002; 21(6)507–527, [CROSSREF], [CSA]
  • Foster R. G., Garcia-Fernandez J. M., Provencio I., De Grip W.J. Opsin localization and chromophore retinoids identified within the basal brain of the lizard Anolis carolinensis. J. Comp. Physiol. A 1993; 172: 33–45, [CROSSREF]
  • Foster R. G., Grace M. S., Provencio I., DeGrip W. J., Garcia-Fernandez J. M. Identification of vertebrate deep brain photoreceptors. Neurosci. Biobehav. Rev. 1994; 18: 541–546, [CROSSREF], [CSA]
  • Fraenkel G., Gunn D. L. The Orientation of Animals. Dove Publ, New York 1940
  • Freake M. J. Homing behaviour in the sleepy lizard (Tiliqua rugosa): the role of cues and the parietal eye. Behav. Ecol. Sociobiol. 2001; 50(6)563–569, [CSA]
  • Gamse J. T., Shen Y. C., Thisse C., Thisse B., Raymond P. A., Halpern M. E., Liang J. O. Otx5 regulates genes that show circadian expression in the zebrafish pineal complex. Nat. Genet. 2002; 30(1)117–121, [CROSSREF]
  • Garcia-Fernandez J. M., Jimenez A. J., Gonzalez B., Pombal M. A., Foster R. G. An immunocytochemical study of encephalic photoreceptors in three species of lamprey. Cell Tissue Res. 1997; 288(2)267–278, [CROSSREF], [CSA]
  • Garg S. K., Sundararaj B. I. Role of pineal in the regulation of some aspects of circadian rhythmicity in the catfish, Heteropneustes fossilis (Bloch). Chronobiologia 1986; 13(1)1–11
  • Grace M. S., Alones V., Menaker M., Foster R. G. Light perception in the vertebrate brain: an ultrastructural analysis of opsin- and vasoactive intestinal polypeptide-immunoreactive neurons in iguanid lizards. J. Comp. Neurol. 1996; 367: 575–594, [CSA]
  • Green C. B., Liang M. Y., Steenhard B. M., Besharse J. C. Ontogeny of circadian and light regulation of melatonin release in Xenopus laevis embryos. Dev. Brain Res. 1999; 117(1)109–116, [CROSSREF], [CSA]
  • Guglielmotti V., Vota-Pinardi U., Fiorino L., Sada E. Seasonal variations in the frontal organ of the frog: structural evidence and physiological correlates. Comp. Biochem. Physilo. A 1997; 116(2)137–141, [CROSSREF], [CSA]
  • Gundy G. C., Ralph C. L., Wurst G. Z. Parietal eyes in lizards: zoogeographical correlates. Science 1975; 190(4215)671–673
  • Gwinner E., Brandstatter R. Complex bird clocks. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2001; 356(1415)1801–1810, [CROSSREF], [CSA]
  • Harada Y., Goto M., Ebihara S., Fujisawa H., Kegasawa K., Oishi T. Circadian locomotor activity rhythms in the African clawed frog, Xenopus laevis: the role of the eye and the hypothalamus. Biol. Rhythm Res. 1998; 29(1)30–48, [CROSSREF], [CSA]
  • Innocenti A., Minutini L., Foà A. The pineal and circadian rhythms of temperature selection and locomotion in lizards. Physiol. Behav. 1993; 53(5)911–915, [CROSSREF], [CSA]
  • Jamieson D., Roberts A. Responses of young Xenopus laevis tadpoles to light dimming: possible roles for the pineal eye. J. Exp. Biol. 2000; 203(12)1857–1867
  • Joss J. M. The pineal complex, melatonin, and colour change in the lamprey Lampetra fluviatilis. Gen. Comp. Endocrinol. 1973a; 21(1)188–195, [CROSSREF], [CSA]
  • Joss J. M. Pineal-gonad relationships in the lamprey Lampetra fluviatilis. Gen. Comp. Endocrinol. 1973b; 21(1)118–122, [CROSSREF], [CSA]
  • Justis C. S., Taylor D. H. Extraocular photoreception and compass orientation in larval bullfrogs, Rana catesbeiana. Copeia 1976; 1976: 98–105, [CSA]
  • Kawamura S., Yokoyama S. Molecular characterization of the pigeon P-opsin gene. Gene 1996; 182(1–2)213–214, [CROSSREF]
  • Kawamura S., Yokoyama S. Expression of visual and nonvisual opsins in American chameleon. Vision Res. 1997; 37: 1867–1871, [CROSSREF], [CSA]
  • Kojima D., Mano H., Fukada Y. Vertebrate ancient long opsin: a green-sensitive photoreceptive molecule present in zebrafish deep brain and retinal horizontal cells. J. Neurosci. 2000; 20: 2845–2851
  • Korf H. W., Schomerus C., Stehle J. H. The pineal organ, its hormone melatonin, and the photoneuroendocrine system. Adv. Anat. Embryol. Cell Biol. 1998; 146: 1–100, [CSA]
  • Kusakabe T., Kusakabe R., Kawakami I., Satou Y., Satoh N., Tsuda M. Ci-opsin1, a vertebrate-type opsin gene, expressed in the larval ocellus of the ascidian Ciona intestinalis. FEBS Lett. 2001; 506(1)69–72, [CROSSREF], [CSA]
  • Mano H., Kojima D., Fukada Y. Exo-rhodopsin: a novel rhodopsin expressed in the zebrafish pineal gland. Mol. Brain Res. 1999; 73(1–2)110–108, [CROSSREF], [CSA]
  • Masuda T., Iigo M., Mizusawa K., Aida K. Retina-type rhodopsin gene expressed in the brain of a teleost, ayu (Plecoglossus altivelis). Zoolog. Sci. 2003; 20(8)989–997, [CROSSREF], [CSA]
  • Masuda H., Oishi T., Ohtani M., Michinomae M., Fukada Y., Shichida Y., Yoshizawa T. Visual pigments in the pineal complex of the Japanese quail, Japanese grass lizard and bullfrog: immunocytochemistry and HPLC analysis. Tissue Cell 1994; 26(1)101–113, [CROSSREF], [CSA]
  • Max M., Menaker M. Regulation of melatonin production by light, darkness, and temperature in the trout pineal. J. Comp. Physiol. A 1992; 170(4)479–489, [CROSSREF]
  • Menaker M. Extraretinal light perception in the sparrow. I. Entrainment of the biological clock. Proc. Natl. Acad. Sci. USA 1968; 59(2)414–421
  • Menaker M. Nonvisual light reception. Sci. Am. 1972; 226(3)22–29
  • Menaker M. Eyes—the second (and third) pineal glands?. Ciba Found. Symp. 1985; 117: 78–92
  • Menaker M., Keatts H. Extraretinal light perception in the sparrow. II. Photoperiodic stimulation of testis growth. Proc. Natl. Acad. Sci. USA 1968; 60(1)146–151
  • Menaker M., Wisner S. Temperature-compensated circadian clock in the pineal of Anolis. Proc. Natl. Acad. Sci. USA 1983; 80: 6119–6121, [CSA]
  • Miller W. H., Wolbarsht M. L. Neural activity in the parietal eye of lizard. Science 1962; 35: 316–317
  • Minamoto T., Shimizu I. A novel isoform of vertebrate ancient opsin in a smelt fish, Plecoglossus altivelis. Biochem. Biophys. Res. Commun. 2002; 290(1)280–286, [CROSSREF], [CSA]
  • Minutini L., Innocenti A., Bertolucci C., Foà A. Circadian organization in the ruin lizard Podarcis sicula: the role of the suprachiasmatic nuclei of the hypothalamus. J. Comp. Physiol. A 1995; 176: 281–288, [CROSSREF]
  • Morita Y., Tabata M., Uchida K., Samejima M. Pineal-dependent locomotor activity of lamprey, Lampetra japonica, measured in relation to LD cycle and circadian rhythmicity. J. Comp. Physiol. A 1992; 171: 555–562, [CROSSREF]
  • Moutsaki P., Bellingham J., Soni B. G., David-Gray Z. K., Foster R. G. Sequence, genomic structure and tissue expression of carp (Cyprinus carpio L.) vertebrate ancient (VA) opsin. FEBS Lett. 2000; 473(3)316–322, [CROSSREF], [CSA]
  • Moutsaki P., Whitmore D., Bellingham J., Sakamoto K., David-Gray Z. K., Foster R. G. Teleost multiple tissue (tmt) opsin: a candidate photopigment regulating the peripheral clocks of zebrafish?. Mol. Brain Res. 2003; 112(1–2)135–145, [CROSSREF], [CSA]
  • Okano T., Yoshizawa T., Fukada Y. Pinopsin is a chicken pineal photoreceptive molecule. Nature 1994; 372: 94–97, [CROSSREF]
  • Okano K., Okano T., Yoshikawa T., Masuda A., Fukada Y., Oishi T. Diversity of opsin immunoreactivities in the extraretinal tissues of four anuran amphibians. J. Exp. Zool. 2000; 286(2)136–142, [CROSSREF]
  • Okano T., Takanaka Y., Nakamura A., Hirunagi K., Adachi A., Ebihara S., Fukada Y. Immunocytochemical identification of pinopsin in pineal glands of chicken and pigeon. Mol. Brain Res. 1997; 50(1–2)190–196, [CROSSREF], [CSA]
  • Pasqualetti M., Bertolucci C., Ori M., Innocenti A., Magnone M. C., De Grip W. J., Nardi I., Foà A. Identification of circadian brain photoreceptors mediating photic entrainment of behavioural rhythms in lizards. Eur. J. Neurosci. 2003; 18(2)364–372, [CROSSREF], [CSA]
  • Phillips J. B., Deutschlander M. E., Freake M. J., Borland S. C. The role of extraocular photoreceptors in newt magnetic compass orientation: parallels between light-dependent magnetoreception and polarized light detection in vertebrates. J. Exp. Biol. 2001; 204(14)2543–2552
  • Philp A. R., Bellingham J., Garcia-Fernandez J., Foster R. G. A novel rod-like opsin isolated from the extra-retinal photoreceptors of teleost fish. FEBS Lett. 2000a; 468(2–3)181–188, [CROSSREF], [CSA]
  • Philp A. R., Garcia-Fernandez J. M., Soni B. G., Lucas R. J., Bellingham J., Foster R. G. Vertebrate ancient (VA) opsin and extraretinal photoreception in the Atlantic salmon (Salmo salar). J. Exp. Biol. 2000b; 203: 1925–1936
  • Provencio I., Jhang G., DeGrip W. J., Hayes W. P., Rollag M. D. Melanopsin: an opsin in melanophores, brain and eye. Proc. Natl. Acad. Sci. USA 1998; 95: 340–345, [CROSSREF], [CSA]
  • Quay W. B. The parietal eye-pineal complex. Biology of the Reptilia, C. Glans, R. G. Northcutt, P. Ulinski. Academic Press, New York 1979; 245–406
  • Roenneberg T., Foster R. G. Twilight times: light and the circadian system. Photochem. Photobiol. 1997; 66: 549–561, [CSA]
  • Roth J. J., Gern W. A., Roth E. C., Ralph C. L., Jacobson E. Nonpineal melatonin in the alligator (Alligator mississippiensis). Science 1980; 210(4469)548–550
  • Scharrer E. Die Lichtempfindlichkeit blinder Elritzen. I. Untersuchungen über das Zwischenhirn der Fische. Z. Vergl. Physiol. 1928; 7: 1–38, [CROSSREF]
  • Shand J., Foster R. G. The extraretinal photoreceptors of nonmammalian vertebrates. Adaptive Mechanisms in the Ecology of Vision, S. Archer, J. Djamgoz, E. Loew. Kluwer Academic Publishers, Dordrecht, Boston, London 1999; 197–222
  • Silver R., Witkovsky P., Horvath P., Alones V., Barnstable C. J., Lehman M. N. Coexpression of opsin- and VIP-like-immunoreactivity in CSF-contacting neurons of the avian brain. Cell Tissue Res. 1988; 253: 189–198, [CROSSREF]
  • Sinsch U. Migration and orientation in anuran amphibians. Ethol. Ecol. Evol. 1990; 2: 65–79, [CSA]
  • Solessio E., Engbretson G. A. Antagonistic chromatic mechanisms in photoreceptors of the parietal eye of lizards. Nature 1993; 364(6436)442–445, [CROSSREF]
  • Solessio E., Engbretson G. A. Electroretinogram of the parietal eye of lizards: photoreceptor, glial, and lens cell contributions. Vis. Neurosci. 1999; 16(5)895–907, [CROSSREF], [CSA]
  • Taniguchi Y., Hisatomi O., Yoshida M., Tokunaga F. Pinopsin expressed in the retinal photoreceptors of a diurnal gecko. FEBS Lett. 2001; 496(2–3)69–74, [CROSSREF], [CSA]
  • Taniguchi M., Murakami N., Nakamura H., Nasu T., Shinohara S., Etoh T. Melatonin release from pineal cells of diurnal and nocturnal birds. Brain Res. 1993; 620(2)297–300, [CROSSREF]
  • Taylor D. H., Adler K. Spatial orientation by Salamanders using plane-polarized light. Science 1973; 181(96)285–287
  • Taylor D. H., Adler K. The pineal body: site of extraocular perception of celestial cues for orientation in the tiger salamander (Ambystoma tigrinum). J. Comp. Physiol. A 1978; 124: 357–361, [CROSSREF]
  • Taylor D. H., Ferguson D. E. Extraoptic celestial orientation in the southern cricket frog Acris gryllus. Science 1970; 168(929)390–392
  • Tosini G., Menaker M. The pineal complex and melatonin affects the daily rhythm of temperature selection in the green iguana. J. Comp. Physiol. A 1996; 179: 135–142, [CROSSREF]
  • Tosini G., Menaker M. Multioscillatory circadian organization in a vertebrate, Iguana iguana. J. Neurosci. 1998; 18(3)1105–1114
  • Tosini G., Bertolucci C., Foà A. The circadian system of reptiles: a true multioscillatory and multiphotoreceptive system. Physiol. Behav. 2001; 72: 461–471, [CROSSREF], [CSA]
  • Underwood H. Retinal and extraretinal photoreceptor mediate entrainment of the circadian locomotor rhythms in lizard. J. Comp. Physiol. 1973; 83: 187–222, [CROSSREF]
  • Underwood H. Circadian organization in the lizard Anolis carolinensis: a multioscillator system. J. Comp. Physiol. 1983; 152: 265–274, [CROSSREF]
  • Underwood H. The pineal and melatonin: regulators of circadian function in lower vertebrates. Experentia 1990; 46: 120–128
  • Underwood H., Groos G. Vertebrate circadian rhythms: retinal and extraretinal photoreception. Experientia 1982; 38: 1013–1021
  • Underwood H., Menaker M. Extraretinal photoreception in lizard. Photochem. Photobiol 1976; 24: 277–241
  • Vigh B., Manzano M. J., Zadori A., Frank C. L., Lukats A., Rohlich P., Szel A., David C. Nonvisual photoreceptors of the deep brain, pineal organs and retina. Histol. Histopathol. 2002; 17(2)555–590, [CSA]
  • Vigh-Teichmann I., Vigh B., Olsson R., van Veen T. Opsin-immunoreactive outer segments of photoreceptors in the eye and in the lumen of the optic nerve of the hagfish, Myxine glutinosa. Cell Tissue Res. 1984; 238(3)515–522, [CROSSREF]
  • Vollrath L. The Pineal Organ. Hanbuch der mikroskopischen Anatomie des Menschen, VI/7, A. Oksche, L. Vollrath. Springer, Berlin, Heidelberg, New York 1981
  • von Frisch K. Beitrage zur Physiologie der Pigmentzellen inder Fischhaut. Pflügers Arch. 1911; 138: 319–387
  • Wada Y., Okano T., Adachi A., Ebihara S., Fukada Y. Identification of rhodopsin in the pigeon deep brain. FEBS Lett. 1998; 424: 53–56, [CROSSREF], [CSA]
  • Xiong W. H., Solessio E. C., Yau K. W. An unusual cGMP pathway underlying depolarizing light response of the vertebrate parietal-eye photoreceptor. Nat. Neurosci. 1998; 1(5)359–365, [CROSSREF]

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