Understanding the dermal light sense in the context of integrative photoreceptor cell biology

Visual Neuroscience

Volumn 28, Issue 4, 2011, Pages 265-279

  Desmond Ramirez, M ^a   Speiser, Daniel I ^a   Sabrina Pankey, M ^a   Oakley, Todd H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Evolution; Extraocular photoreceptors; Invertebrates; Non visual photoreception; Phototransduction

Indexed keywords

ANNELID WORM; ARTHROPOD; CELL AGGREGATION; CELL FUNCTION; CELL STRUCTURE; CELL TYPE; CEPHALOCHORDATA; CNIDARIA; CYTOLOGY; ECHINODERM; EVOLUTION; METAZOON; MOLLUSC; NEMATODE; NERVE CELL NETWORK; NEUROPHYSIOLOGY; NONHUMAN; PHOTORECEPTOR CELL; PHOTOTRANSDUCTION; PLATYHELMINTH; PRIORITY JOURNAL; REVIEW; UROCHORDATA; VERTEBRATE; VISION;

ANIMALS; BEHAVIOR, ANIMAL; CNIDARIA; ECHINODERMATA; INVERTEBRATES; LIGHT; PHOTORECEPTOR CELLS, INVERTEBRATE; SENSATION; SKIN PHYSIOLOGICAL PHENOMENA;

EID: 80053162827     PISSN: 09525238     EISSN: 14698714     Source Type: Journal    
DOI: 10.1017/S0952523811000150     Document Type: Review

References (145)

1. Adler, K. (1976). Extraocular photoreception in amphibians. Photochemistry and Photobiology 23, 275-298.
2. Aizenberg, J., Tkachenko, A., Weiner, S., Addadi, L. & Hendler, G. (2001). Calcitic microlenses as part of the photoreceptor system in brittlestars. Nature 412, 819-822. (Pubitemid 32801463)
3. Arendt, D. (2003). Evolution of eyes and photoreceptor cell types. International Journal of Developmental Biology 47, 563-572.
4. Arendt, D., Tessmar-Raible, K., Snyman, H., Dorresteijn, A.W. & Wittbrodt, J. (2004). Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 306, 869-871. (Pubitemid 39446995)
5. Arendt, D. & Wittbrodt, J. (2001). Reconstructing the eyes of Urbilateria. Philosophical Transactions of the Royal Society B: Biological Sciences 356, 1545-1563. (Pubitemid 33001680)
6. Arey, L. & Crozier, W. (1919). The sensory responses of Chiton. Journal of Experimental Zoology 29, 157-260.
7. Arikawa, K. & Aoki, K. (1982). Response characteristics and occurrence of extraocular photoreceptors on lepidopteran genitalia. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 148, 483-489.
8. Arikawa, K., Eguchi, E., Yoshida, A. & Aoki, K. (1980). Multiple extraocular photoreceptive areas on genitalia of butterfly Papilio xuthus. Nature 288, 700-702.
9. Arikawa, K. & Miyako-Shimazaki, Y. (1996). Combination of physiological and anatomical methods for studying extraocular photoreceptors on the genitalia of the butterfly, Papilio xuthus. Journal of Neuroscience Methods 69, 75-82. (Pubitemid 26354466)
10. Arikawa, K., Suyama, D. & Fujii, T. (1997). Hindsight by genitalia: Photo-guided copulation in butterflies. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 180, 295-299. (Pubitemid 27161753)
11. Arikawa, K. & Takagi, N. (2001). Genital photoreceptors have crucial role in oviposition in Japanese yellow swallowtail butterfly, Papilio xuthus. Zoological Science 18, 175-179. (Pubitemid 33397558)
12. Arvanitaki, A. & Chalazonitis, N. (1961). Excitatory and inhibitory processes initiated by light and infra-red radiations in single identifiable nerve cells. In Nervous Inhibition, ed. Florey, E. New York: Pergamon Press, 194-231.
13. Bagnara, J. & Obika, M. (1967). Light sensitivity of melanophores in neural crest explants. Experimentia 23, 155-157.
14. Barber, V. & Wright, D. (1969). The fine structure of the eye and optic tentacle of themollusc Cardiumedule. Journal ofUltrastructure Research 26, 515-528.
15. Bellingham, J., Morris, A. & Hunt, D. (1998). The rhodopsin gene of the cuttlefish Sepia officinalis: Sequence and spectral tuning. The Journal of Experimental Biology 201, 2299-2306. (Pubitemid 28407617)
16. Blevins, E. & Johnsen, S. (2004). Spatial vision in the echinoid genus Echinometra. Journal of Experimental Biology 207, 4249-4253. (Pubitemid 40099375)
17. Bolwig, N. (1946). Senses and sense organs of the anterior end of the house fly larvae. Dansk Naturhist for Kobenhavn Vidensk Meddel 109, 81-217.
18. Boyle, P. (1969). Rhabdomeric ocellus in a chiton. Nature 222, 895-896.
19. Boyle, P. (1972). The aesthetes of chitons. Marine and Freshwater Behaviour and Physiology 1, 171-184.
20. Brown, P. & Brown, P. (1958). Visual pigments of the octopus and cuttlefish. Nature 182, 1288-1290.
21. Burke, R., Angerer, L., Elphick, M., Humphrey, G., Yaguchi, S., Kiyama, T., Liang, S., Mu, X., Agca, C. & Klein, W. (2006). A genomic view of the sea urchin nervous system. Developmental Biology 300, 434-460. (Pubitemid 44834382)
22. Cashmore, A.R., Jarillo, J.A., Wu, Y. & Liu, D. (1999). Cryptochromes: Blue light receptors for plants and animals. Science 284, 760-765. (Pubitemid 29291333)
23. Chono, K., Fujito, Y. & Ito, E. (2002). Non-ocular dermal photoreception in the pond snail Lymnaea stagnalis. Brain Research 951, 107-112. (Pubitemid 35253903)
24. Chrachri, A. & Nelson, L. (2005). Whole-cell recording of light-evoked photoreceptor responses in a slice preparation of the cuttlefish retina. Visual Neuroscience 22, 359-370. (Pubitemid 41329351)
25. Clark, E.D. & Kimeldorf, D.J. (1971). Behavioral reactions of the sea anemone, Anthopleura xanthogrammica, to ultraviolet and visible radiations. Radiation Research 45, 166-175.
26. Cobb, J. & Hendler, G. (1990). Neurophysiological characterization of the photoreceptor system in a brittlestar, Ophiocoma wendtii (Echinodermata, Ophiuroidea). Comparative Biochemistry and Physiology A: Physiology 97, 329-333.
27. Cobb, J. & Moore, A. (1986). Comparative studies on receptor structure in the brittlestar Ophiura ophiura. Journal of Neurocytology 15, 97-108. (Pubitemid 16138127)
28. Cobb, C. & Williamson, R. (1998a). Electrophysiology and innervation of the photosensitive epistellar body in the lesser octopus Eledone cirrhosa. The Biological Bulletin 195, 78-87. (Pubitemid 28424147)
29. Cobb, C. & Williamson, R. (1998b). Electrophysiology of extraocular photoreceptors in the squid Loligo forbesi (Cephalopoda: Loliginidae). Journal of Molluscan Studies 64, 111-117. (Pubitemid 28132103)
30. Cobb, C.S., Williamson, R. & Pope, S.K. (1995). The responses of the epistellar photoreceptors to light and their effect on circadian rhythms in the lesser octopus, Eledone cirrhosa. Marine and Freshwater Behaviour and Physiology 26, 59-69.
31. Cook, A. (1975). The withdrawal response of a freshwater snail (Lymnaea stagnalis L.). Journal of Experimental Biology 62, 783-796.
32. Cowles, R. (1910). Stimuli produced by light and by contact with solid walls as factors in the behavior of ophiuroids. Journal of Experimental Biology 9, 387-416.
33. Crisp, M. (1972). Photoreceptive function of an epithelial receptor in Nassarius reticulatus [Gastropoda, Prosobranchia]. Journal of the Marine Biological Association of the United Kingdom 52, 437-442.
34. Diggle, P. (2003). Statistical Analysis of Spatial Point Patterns. Arnold, London.
35. Dilly, P. & Wolken, J. (1973). Studies on the receptors in Ciona intestinalis. IV. The ocellus in the adult. Micron 4, 11-29.
36. Dörjes, J. (1968). Die Acoela (Turbellaria) der deutschen Nordseeküste und ein neues System der Ordnung. Zeitschrift fuer Zoologische Systematik und Evolutionsforschung 6, 56-452.
37. Duivenboden, Y. (1982). Non-ocular photoreceptors and photo-orientation in the pond snail Lymnaea stagnalis (L.). Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 149, 363-368. (Pubitemid 13129896)
38. Eakin, R. (1961). Photoreceptors in the amphibian frontal organ. Proceedings of the National Academy of Sciences 47, 1084-1088.
39. Eakin, R. (1968). Evolution of photoreceptors. In Evolutionary Biology, Vol 2, eds. Dobzhansky, T., Hecht, M., and Steere, W., pp. 194-242. Appleton-Century-Crofts: New York.
40. Eakin, R. (1972). Structure in invertebrate photoreceptors. In Handbook of Sensory Physiology, Vol. 7, ed. Dartnell, H.J., pp. 635-684. New York: Springer New York.
41. Eakin, R. & Brandenburger, J. (1967). Differentiation in eye of a pulmonate snail Helix aspersa. Journal of Ultrastructure Research 18, 391-421.
42. Eakin, R. & Westfall, J.A. (1962). Fine structure of photoreceptors in Amphioxus. Journal of Ultrastructure Research 6, 531-539.
43. Edwards, S., Charlie, N., Milfort, M., Brown, B., Gravlin, C., Knecht, J. & Miller, K. (2008). A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans. PLoS Biology 6, 1715-1729.
44. Fu, Y. & Yau, K.W. (2007). Phototransduction in mouse rods and cones. Pflügers Archiv: European Journal of Physiology 454, 805-819. (Pubitemid 46976598)
45. Gabel, C.V., Gabel, H., Pavlichin, D., Kao, A., Clark, D.A. & Samuel, A.D.T. (2007). Neural circuits mediate electrosensory behavior in Caenorhabditis elegans. Journal of Neuroscience 27, 7586-7596. (Pubitemid 47066580)
46. Gomez, M.P. & Nasi, E. (2000). Light Transduction in Invertebrate Hyperpolarizing Photoreceptors: Possible Involvement of a Go- Regulated Guanylate Cyclase. Journal of Neuroscience 20, 5254-5263. (Pubitemid 30457722)
47. Gotow, T. (1975). Morphology and function of the photoexcitable neurones in the central ganglia of Onchidium verruculatum. Journal of Comparative Physiology A: Neuroethology 99, 139-152.
48. Gotow, T. & Nishi, T. (2002). Light-dependent K channels in the mollusc Onchidium simple photoreceptors are opened by cGMP. Journal of General Physiology 120 (4): 581-597. doi:10.1085/jgp.20028619. (Pubitemid 35155098)
49. Gotow, T. & Nishi, T. (2008). Simple photoreceptors in some invertebrates: Physiological properties of a new photosensory modality. Brain Research 1225, 3-16.
50. Grancher, J. (1920). Note on the photic sensitivity of the chitons. The American Naturalist 54, 376-380.
51. Grueber, W., Jan, L. & Jan, Y. (2002). Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129, 2867-2878. (Pubitemid 34874266)
52. Hara, T. & Hara, R. (1980). Retinochrome and rhodopsin in the extraocular photoreceptor of the squid, Todarodes. The Journal of General Physiology 75, 1.
53. Hardie, R. & Raghu, P. (2001). Visual Transduction in Drosophila. Nature. 413, 186-193. (Pubitemid 32867883)
54. Hattar, S., Lucas, R.J., Mrosovsky, N., Thompson, S., Douglas, R., Hankins, M.W., Lem, J., Biel, M., Hofmann, F. & Foster, R.G. (2003). Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424, 75-81.
55. Haug, G. (1933). Die Lichtreaktionen der Hydren (Chlorohydra viridissima und Pelmatohydra oligactis). Zeitschrift für Vergleichende Physiologie 19, 354-355.
56. Heath, H. (1904). The larval eye of chitons. Proceedings of the Academy of Natural Sciences of Philadelphia 56, 257-259.
57. Hecht, S. (1919). Sensory equilibrium and dark adaptation in Mya arenaria. The Journal of General Physiology 1, 545-558.
58. Hegemann, P. (2008). Algal sensory photoreceptors. Annual Review of Plant Biology 59, 167-189. (Pubitemid 351813028)
59. Hendler, G. (1984). Brittlestar color-change and phototaxis (Echinodermata: Ophiuroidea: Ophiocomidae). Marine Ecology 5, 379-401. (Pubitemid 16273165)
60. Hendler, G. & Byrne, M. (1987). Fine structure of the dorsal arm plate of Ophiocoma wendtii: Evidence for a photoreceptor system (Echinodermata, Ophiuroidea). Zoomorphology 107, 261-272.
61. Hisano, N., Tateda, H. & Kuwabara, M. (1972a). An electrophysiological study of the photo-excitative neurones of Onchidium verruculatum in situ. Journal of Experimental Biology 57, 661-671.
62. Hisano, N., Tateda, H. & Kuwabara, M. (1972b). Photosensitive neurones in the marine pulmonate mollusc Onchidium verruculatum. Journal of Experimental Biology 57, 651.
63. Howard, L. (2008). Drosophilidae compound eye edit. Photo. http://commons. wikimedia.org/wiki/File:Drosophilidae-compound-eye-edit1.jpg.
64. Hyman, L. (1951). The Invertebrates: Acanthocephala, Aschelminthes, and Entoprocta, the Pseudocoelomate Bilateria, Vol. 3. McGraw-Hill, New York: London.
65. Hyman, L. (1967). The Invertebrates. Vol. VI. Mollusca I. Aplacophora, Polyplacophora, Monoplacophora, Gastropoda. The Coelomate Bilateria. McGraw-Hill, New York: London.
66. Jekely, G. (2009). Evolution of phototaxis. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 2795-2808.
67. Johnsen, S. (1997). Identification and localization of a possible rhodopsin in the echinoderms Asterias forbesi (Asteroidea) and Ophioderma brevispinum (Ophiuroidea). The Biological Bulletin 193, 97-105. (Pubitemid 27370062)
68. Kennedy, D. (1960). Neural photoreception in a lamellibranch mollusc. Journal of General Physiology 44, 277-299.
69. Kennedy, D. (1963). Physiology of photoreceptor neurons in the abdominal nerve cord of the crayfish. The Journal of General Physiology 46, 551.
70. Kojima, D., Terakita, A. & Ishikawa, T. (1997). A novel Go-mediated phototransduction cascade in scallop visual cells. Journal of Biological Chemistry 272, 22979-22982. (Pubitemid 27392418)
71. Koyanagi, M., Kubokawa, K. & Tsukamoto, H. (2005). Cephalochordate melanopsin: Evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Current Biology 15, 1065-1069. (Pubitemid 40772156)
72. Koyanagi, M., Takano, K., Tsukamoto, H. & Ohtsu, K. (2008). Jellyfish vision starts with cAMP signaling mediated by opsin-Gs cascade. Proceedings of the National Academy of Sciences 105, 15576-15580.
73. Koyanagi, M., Terakita, A., Kubokawa, K. & Shichida, Y. (2002). Amphioxus homologs of Go-coupled rhodopsin and peropsin having 11-cis-and all-trans-retinals as their chromophores. FEBS Letters 531, 525-528. (Pubitemid 35336080)
74. Kozmik, Z., Ruzickova, J. & Jonasova, K. (2008). Assembly of the cnidarian camera-type eye from vertebrate-like components. Proceedings of the National Academy of Sciences 105, 8989-8993.
75. Kusakabe, T., Kusakabe, R., Kawakami, I., Satou, Y., Satoh, N. & Tsuda, M. (2001). Ci-opsin1, a vertebrate-type opsin gene, expressed in the larval ocellus of the ascidian Ciona intestinalis. FEBS Letters 506, 69-72. (Pubitemid 32925234)
76. Kusakabe, T. & Tsuda, M. (2007). Photoreceptive systems in ascidians. Photochemistry and Photobiology 83, 248-252. (Pubitemid 46623046)
77. Lacalli, T. (2004). Sensory systems in amphioxus: A window on the ancestral chordate condition. Brain Behavior and Evolution 64, 148-162. (Pubitemid 39279348)
78. Land, M.F. & Nilsson, D.-E. (2002). Animal Eyes. Oxford University Press Oxford; Toronto.
79. Lesser, M.P., Carleton, K.L., Bottger, S.A., Barry, T.M. & Walker, C.W. (2011). Sea urchin tube feet are photosensory organs that express a rhabdomeric-like opsin and PAX6. Proceedings of the Royal Society B: Biological Sciences. doi:10.1098/rspb.2011.0336.
80. Light, V. (1930). Photoreceptors in Mya arenaria, with special reference to their distribution, structure, and function. Journal of Morphology 49, 1-43.
81. Liu, J., Ward, A., Gao, J., Dong, Y., Nishio, N., Inada, H., Kang, L., Yu, Y., Ma, D., Xu, T., Mori, I., Xie, Z. & Xu, X.Z. (2010). C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog. Nature Neuroscience 13, 715-722.
82. Lukowiak, K. & Jacklet, J. (1972). Habituation and dishabituation: Interactions between peripheral and central nervous systems in Aplysia. Science 178, 1306-1308.
83. Mano, H. & Fukada, Y. (2007). A median third eye: Pineal gland retraces evolution of vertebrate photoreceptive organs. Photochemistry and Photobiology 83, 11-18. (Pubitemid 46697218)
84. Marks, P. (1976). Nervous control of light responses in the sea anemone, Calamactis praelongus. Journal of Experimental Biology 65, 85-96.
85. Martin, V. (2002). Photoreceptors of cnidarians. Canadian Journal of Zoology 80, 1703-1722.
86. Mathger, L.M., Roberts, S.B. & Hanlon, R.T. (2010). Evidence for distributed light sensing in the skin of cuttlefish, Sepia officinalis. Biology Letters 6, 600-603.
87. Mauro, A. (1977). Extra-ocular photoreceptors in cephalopods. Symposium of the Zoological Society of London 38, 287-308.
88. Millott, N. (1968). The dermal light sense. Symposia of the Zoological Society of London 23, 1-36.
89. Millott, N. (1975). The photosensitivity of echinoids. Advances in Marine Biology 13, 1-52.
90. Milne, L. & Milne, M. (1956). Invertebrate photoreceptors. In Radiation Biology, Vol. 3. ed. Hollaender, A. McGraw-Hill New York 621-692.
91. Miyako, Y., Arikawa, K. & Eguchi, E. (1993). Ultrastructure of the extraocular photoreceptor in the genitalia of a butterfly, Papilio xuthus. The Journal of Comparative Neurology 327, 458-468. (Pubitemid 23031947)
92. Morton, J. (1960). The responses and orientation of the bivalve Lasaea rubra Montagu. Journal of the Marine Biological Association of the United Kingdom 39, 5-26.
93. Mrabet, Y. (2008). Drosophila XY sex-chromosomes. Drawing. http:// commons.wikimedia.org/wiki/File:Drosophila-XY-sex-determination.svg.
94. Nasi, E. & Del Pilar Gomez, M. (2009). Melanopsin-mediated lightsensing in amphioxus: A glimpse of the microvillar photoreceptor lineage within the deuterostomia. Communicative and Integrative Biology 2, 441-443.
95. Nilsson, D. (1994). Eyes as optical alarm systems in fan worms and ark clams. Philosophical Transactions: Biological Sciences 346, 195-212. (Pubitemid 2163293)
96. Nilsson, D. (2009). The evolution of eyes and visually guided behaviour. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 2833-2847.
97. Nishioka, R., Hagadorn, I. & Bern, H. (1962). Ultrastructure of the epistellar body of the octopus. Cell and Tissue Research 57, 406-421.
98. Nishioka, R., Yasumasu, I., Packard, A., Bern, H. & Young, J. (1966). Nature of vesicles associated with the nervous system of cephalopods. Cell and Tissue Research 75, 301-316.
99. Nordstrom, K., Wallen, R., Seymour, J. & Nilsson, D. (2003). A simple visual system without neurons in jellyfish larvae. Proceedings of the Royal Society B: Biological Sciences 270, 2349-2354. (Pubitemid 37464018)
100. North, W.J. (1957). Sensitivity to light in the sea anemone Metridium senile (L.). The Journal of General Physiology 40, 715-733.
101. North, W. & Pantin, C. (1958). Sensitivity to light in the sea-anemone Metridium senile (L): Adaptation and action spectra. Proceedings of the Royal Society of London 148, 385-396.
102. Ooka, S., Katow, T., Yaguchi, S., Yaguchi, J. & Katow, H. (2010). Spatiotemporal expression pattern of an encephalopsin orthologue of the sea urchin Hemicentrotus pulcherrimus during early development, and its potential role in larval vertical migration. Development, Growth & Differentiation 52, 195-207.
103. Oshima, N. (2001). Direct reception of light by chromatophores of lower vertebrates. Pigment Cell Research 14, 312-319. (Pubitemid 32956356)
104. Packard, A. & Brancato, D. (1993). Some responses of Octopus chromatophores to light. Journal of Physiology 459, 429.
105. Panda, S., Sato, T., Castrucci, A., Rollag, M., Degrip, W., Hogenesch, J., Provencio, I. & Kay, S. (2002). Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298, 2213-2216. (Pubitemid 35471251)
106. Pankey, S., Sunada, H., Horikoshi, T. & Sakakibara, M. (2010). Cyclic nucleotide-gated channels are involved in phototransduction of dermal photoreceptors in Lymnaea stagnalis. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 180, 1205-1211.
107. Passano, L. & Mccullough, C. (1962). The light response and the rhythmic potentials of Hydra. Proceedings of the National Academy of Sciences of the United States of America 48, 1376-1382.
108. Pearse, V.B. (1974). Modification of sea anemone behavior by symbiotic zooxanthellae: Expansion and contraction. Biological Bulletin 147, 641-651.
109. Plachetzki, D.C., Fong, C.R. & Oakley, T.H. (2010). The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway. Proceedings of the Royal Society B: Biological Sciences 277, 1963-1969.
110. Plachetzki, D.C., Degnan, BM. & Oakley, TH. (2007). The Origins of Novel Protein Interactions during Animal Opsin Evolution. PLoS ONE 2(10): e1054. doi:10.1371/journal.pone.0001054. (Pubitemid 351559261)
111. Provencio, I., Rodriguez, I. & Jiang, G. (2000). A novel human opsin in the inner retina. Journal of Neuroscience 20, 600-605. (Pubitemid 30225562)
112. Raible, F., Tessmar-Raible, K., Arboleda, E., Kaller, T., Bork, P., Arendt, D. & Arnone, M. (2006). Opsins and clusters of sensory G-protein-coupled receptors in the sea urchin genome. Developmental Biology 300, 461-475. (Pubitemid 44834389)
113. Richter, S., Loesel, R., Purschke, G., Schmidt-Rhaesa, A., Scholtz, G., Stach, T., Vogt, L., Wanninger, A., Brenneis, G., Doering, C., Faller, S., Fritsch, M., Grobe, P., Heuer, C.M., Kaul, S., Moller, O.S., Mueller, C.H.G., Rieger, V., Rothe, B.H., Stegner, M.E.J. & Harzsch, S. (2010). Invertebrate neurophylogeny: Suggested terms and definitions for a neuroanatomical glossary. Frontiers in Zoology 7, 29.
114. Röhlich, P., Aros, B. & Viragh, S. (1970). Fine structure of photoreceptor cells in the earthworm, Lumbricus terrestris. Cell and Tissue Research 104, 345-357.
115. Rubin, E.B., Shemesh, Y., Cohen, M., Elgavish, S., Robertson, H.M. & Bloch, G. (2006). Molecular and phylogenetic analyses reveal mammalian- like clockwork in the honey bee (Apis mellifera) and shed new light on the molecular evolution of the circadian clock. Genome Research 16, 1352-1365. (Pubitemid 44664678)
116. Ruiz, M. & Anadon, R. (1991). Some considerations on the fine structure of rhabdomeric photoreceptors in the amphioxus, Branchiostoma lanceolatum (Cephalochordata). Journal für Hirnforschung 32, 159-164.
117. Rushforth, N., Burnett, A. & Maynard, R. (1963). Behavior in hydra: Contraction responses of Hydra pirardi to mechanical and light stimuli. Science 139, 760-761.
118. Sakakibara, M., Aritaka, T., Iizuka, A., Suzuki, H., Horikoshi, T. & Lukowiak, K. (2005). Electrophysiological responses to light of neurons in the eye and statocyst of Lymnaea stagnalis. Journal of Neurophysiology 93, 493-507. (Pubitemid 40626856)
119. Salvini-Plawen, L. & Mayr, E. (1977). On the evolution of photoreceptors and eyes. Evolutionary Biology 10, 207-253.
120. Sawyer, S., Dowse, H. & Shick, J. (1994). Neurophysiological correlates of the behavioral response to light in the sea anemone Anthopleura elegantissima. Biological Bulletin 186, 195-201. (Pubitemid 2087017)
121. Shick, J. & Dykens, J.A. (1984). Photobiology of the symbiotic sea anemone Anthopleura elegantissima: Photosynthesis, respiration, and behavior under intertidal conditions. The Biological Bulletin 166, 608-619.
122. Siddiqui, I. & Viglierchio, D. (1970). Ultrastructure of photoreceptors in the marine nematode Deontostoma californicum. Journal of Ultrastructure Research 32, 558-571.
123. Singla, C. (1974). Ocelli of hydromedusae. Cell and Tissue Research 149, 413-429.
124. Speiser, D.I., Eernisse, D.J. & Johnsen, S. (2011). A chiton uses aragonite lenses to form images. Current Biology 21, 665-670.
125. Steven, D. (1963). The dermal light sense. Biological Reviews 38, 204-240.
126. Stoll, C. (1972). Sensory systems involved in shadow response of Lymnaea stagnalis (L) as studied with use of habituation phenomena. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen Series C: Biological and Medical Sciences 75, 342-351.
127. Stoll, C. (1976). Extraocular photoreception in Lymnaea Stagnalis L. In Neurobiology of Invertebrates, Gastropoda Brain. ed. Salánki, J. Akadémiai Kiadó, location: Budapest pp 487-495
128. Su, C., Luo, D., Terakita, A., Shichida, Y., Liao, H., Kazmi, M., Sakmar, T. & Yau,K. (2006). Parietal-eye phototransduction components and their potential evolutionary implications. Science 311, 1617-1621.
129. Suga, H., Schmid, V. & Gehring, W. (2008). Evolution and functional diversity of jellyfish opsins. Current Biology 18, 51-55.
130. Tardent, P. & Frei, E. (1969). Reaction patterns of dark and light adapted Hydra to light stimuli. Cellular andMolecular Life Sciences 25, 265-267.
131. Tarttelin, E., Bellingham, J., Hankins, M., Foster, R. & Lucas, R.J. (2003). Neuropsin (Opn5): A novel opsin identified in mammalian neural tissue. FEBS Letters 554, 410-416. (Pubitemid 37412523)
132. Tong, D., Rozas, N., Oakley, T., Mitchell, J., Colley, N.J. & Mc Fall- Ngai, M.J. (2009). Evidence for light perception in a bioluminescent organ. Proceedings of the National Academy of Sciences 106, 9836-9841.
133. Ullrich-Lüter, E.M., Dupont, S., Arboleda, E., Hausen, H., Arnone, MI. (2011). Unique system of photoreceptors in sea urchin tube feet. Proceedings of the National Academy of Sciences of the United States of America, 10.1073/pnas.1018495108.
134. Ward, A., Liu, J., Feng, Z. & Xu, X. (2008). Light-sensitive neurons and channels mediate phototaxis in C. elegans. Nature Neuroscience 11, 916-922.
135. Watson, G. & Hessinger, D. (1989). Cnidocyte mechanoreceptors are tuned to the movements of swimming prey by chemoreceptors. Science 243, 1589-1591. (Pubitemid 19090507)
136. Watson, G. & Hessinger, D. (1994). Evidence for calcium channels involved in regulating nematocyst discharge. Comparative Biochemistry and Physiology 107, 473-481. (Pubitemid 24094295)
137. Wiederhold, M., JR, E.M. & Bell, A. (1973). Photoreceptor spike responses in the hardshell clam, Mercenaria mercenaria. Journal of General Physiology 61, 24-55.
138. Wilkens, L. & Larimer, J. (1972). The CNS photoreceptor of crayfish: Morphology and synaptic activity. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 80, 389-407.
139. Woodley, J. (1982). Photosensitivity in Diadema antillarum: Does it show scototaxisIn Echinoderms, Proceedings of the International Conference, Tampa Bay. ed. Lawrence, J.M., pp. 61: CRC Press A.A. Balkema, Rotterdam.
140. Xiang, Y., Yuan, Q., Vogt, N., Looger, L.L., Jan, L.Y. & Jan, Y.N. (2010). Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468, 921-926.
141. Yamasu, T. & Yoshida, M. (1973). Electron microscopy on the photoreceptors of the anthomedusae and a scyphomedusa. Publications. Seto Marine Biological Laboratory, Kyoto University 20, 757-778.
142. Yanase, T. & Sakamoto, S. (1965). Fine structure of the visual cells of the dorsal eye in molluscan Onchidium verruculatum. Zoological Magazine 74, 238-242.
143. Yerramilli, D. & Johnsen, S. (2010). Spatial vision in the purple sea urchin Strongylocentrotus purpuratus (Echinoidea). Journal of Experimental Biology 213, 249-255.
144. Yoshida, M. (1979). Extraocular photoreception. In Handbook of Sensory Physiology, vol. 7, ed. Autrum, H., pp. 581-640. Berlin: Springer.
145. Zylstra, U. (1971). Distribution and ultrastructure of epidermal sensory cells in the freshwater snails Lymnaea stagnalis and Biomphalaria pfeifferi. Netherlands Journal of Zoology 22, 283-298.