The eyes of Limulus polyphemus (Xiphosura, Chelicerata) and their afferent and efferent projections

Arthropod Structure and Development

Volumn 35, Issue 4, 2006, Pages 261-274

  Battelle, B A ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Circadian rhythms; Horseshoe crab; Myosin III; Photoreceptors; Visual system; Xiphosuran

Indexed keywords

ARTHROPOD; BRAIN; CELL TYPE; COMPOUND EYE; DEFENSE MECHANISM; EFFERENT NERVE; INNERVATION; LIMULUS; NERVE CELL; NERVE CONDUCTION; NONHUMAN; PHOTORECEPTOR; REVIEW; VISUAL SYSTEM;

ARTHROPODA; CHELICERATA; LIMULUS POLYPHEMUS; MEROSTOMATA; XIPHOSURA;

EID: 33845303990     PISSN: 14678039     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.asd.2006.07.002     Document Type: Review

References (89)

1. Arikawa K., Uchiumi K., and Eguchi E. Extraocular photoreceptors in the last abdominal ganglion of a swallowtail butterfly, Pspilio xuthus. Naturwissenschaften 78 (1991) 82-84
2. Barlow Jr. R.B. Circadian rhythms in the Limulus visual system. Journal of Neuroscience 3 (1983) 856-870
3. Barlow Jr. R.B., and Kaplan E. Properties of visual cells in the lateral eye of Limulus in situ. Intracellular recordings. Journal of General Physiology 69 (1977) 203-220
4. Barlow Jr. R.B., Bolanowski Jr. S.J., and Brachman M.L. Efferent optic nerve fibers mediate circadian rhythms in the Limulus eye. Science 197 (1977) 86-89
5. Barlow Jr. R.B., Chamberlain S.C., and Levinson J.Z. Limulus brain modulates the structure and function of the lateral eyes. Science 210 (1980) 1037-1039
6. Barlow Jr. R.B., Ireland L.C., and Kass L. Vision has a role in Limulus mating behavior. Nature 296 (1982) 65-66
7. Barlow R.B., Hitt J.A., and Dodge F.A. Limulus vision in the marine environment. Biological Bulletin 200 (2001) 169-176
8. Batra R., and Chamberlain S.C. Central connections of Limulus ventral photoreceptors revealed by intracellular staining. Journal of Neurobiology 16 (1985) 435-441
9. Battelle B.-A. Neurotransmitter candidates in the visual system of Limulus polyphemus: synthesis and distribution of octopamine. Vision Research 20 (1980) 911-922
10. Battelle B.-A. Circadian efferent input to Limulus eyes: anatomy, circuitry and impact. Microscopic Research and Technique 58 (2002) 345-355
11. Battelle B.-A., and Evans J.A. Octopamine release from centrifugal fibers in the Limulus peripheral visual system. Journal of Neurochemistry 46 (1984) 1464-1472
12. Battelle B.-A., and Hart M.K. Histamine metabolism in the visual system of the horseshoe crab Limulus polyphemus. Comparative Biochemistry and Physiology A 133 (2002) 135-142
13. Battelle B.-A., Evans J.A., and Chamberlain S.C. Efferent fibers to Limulus eyes synthesize and release octopamine. Science 216 (1982) 1250-1252
14. Battelle B.-A., Calman B.G., Andrews A.W., Grieco F.D., Meleziva M.B., Callaway J.C., and Stuart A.E. Histamine: a putative afferent neurotransmitter in Limulus eyes. Journal of Comparative Neurology 305 (1991) 527-542
15. Battelle B.-A., Calman B.G., and Hart M.K. Cellular distributions and functions of histamine, octopamine and serotonin in the peripheral visual system, brain and circumesophageal ring of the horseshoe crab Limulus polyphemus. Microscopic Research and Technique 44 (1999) 70-80
16. Battelle B.-A., Dabdoub A., Malone M.A., Andrews A.W., Cacciatore C., Calman B.G., Smith W.C., and Payne R. Immunocytochemical localization of opsin, visual arrestin. myosinIII and calmodulin in Limulus lateral eye retinular cells and ventral photoreceptors. Journal of Comparative Neurology 435 (2001) 211-225
17. Behrens M.E., and Fahy J.L. Slow potentials in non-spiking optic nerve fibers in the peripheral visual system of Limulus. Journal of Comparative Physiology 141 (1981) 239-247
18. Calman B.G., and Battelle B.-A. Central origin of the efferent neurons projecting to the eyes of Limulus polyphemus. Visual Neuroscience 6 (1991) 481-495
19. Calman B.G., and Chamberlain S.C. Distinct lobes of Limulus ventral photoreceptors. II. Structure and ultrastructure. Journal of General Physiology 80 (1982) 839-862
20. Calman B.G., Lauerman M.A., Andrews A.W., Schmidt M., and Battelle B.-A. Central projections of Limulus photoreceptor cells revealed by a photoreceptor-specific monoclonal antibody. Journal of Comparative Neurology 313 (1991) 553-562
21. Chamberlain S.C., and Barlow Jr. R.B. Innervation patterns of single optic nerve fibers in the Limulus brain: a modification of the cobalt staining technique for cut axons. Vision Research 18 (1978) 1427-1433
22. Chamberlain S.C., and Barlow Jr. R.B. Neuroanatomy of the visual afferents in the horseshoe crab (Limulus polyphemus). Journal of Comparative Neurology 192 (1980) 387-400
23. Chamberlain S.C., and Barlow Jr. R.B. Retinotopic organization of lateral eye inputs to Limulus brain. Journal of Neurophysiology 48 (1982) 505-520
24. Chapman R.M., and Lall A.B. Electroretinogram characteristics and the spectral mechanisms of the median ocellus and the lateral eye in Limulus polyphemus. Journal of General Physiology 50 (1967) 2267-2287
25. Clark A.W., Mellecchia R., and Mauro A. The ventral photoreceptor cells of Limulus. Journal of General Physiology 54 (1969) 289-309
26. Conley K.W., Blackburn D.C., Plachetzki D., Kempler K., Currie J., Battelle B.A., and Brown N.L. Pax6 and Atonal expression during embryonic eye formation in the American Horseshoe crab, Limulus polyphemus. Developmental Biology 295 (2006) 255
27. Dalal J.S., Jinks R.N., Cacciatore C., Greenberg R.M., and Battelle B.-A. Limulus opsins: diurnal regulation of expression. Visual Neuroscience 20 (2003) 523-534
28. Eakin R.M., and Brandenburger J.L. Fine structure of the eyes of jumping spiders. Journal of Ultrastructure Research 37 (1971) 618-663
29. Evans J.A., Chamberlain S.C., and Battelle B.-A. Autoradiographic localization of newly synthesized octopamine in the retinal efferents in the Limulus visual system. Journal of Comparative Neurology 219 (1983) 369-383
30. Fahrenbach W.H. The morphology of the eyes of Limulus II. Ommatidia of the compound eye. Zeitschrift für Zellforschung und Mikroskopische Anatomie 93 (1969) 451-483
31. Fahrenbach W.H. The morphology of the Limulus visual system. III. The lateral rudimentary eye. Zeitschrift für Zellforschung und Mikroskopische Anatomie 105 (1970) 303-316
32. Fahrenbach W.H. The morphology of the Limulus visual system. IV. The lateral optic nerve. Zeitschrift für Zellforschung und Mikroskopische Anatomie 114 (1971) 532-545
33. Fahrenbach W.H. The morphology of the Limulus visual system. V. Protocerebral neurosecretion and occular innervation. Zeitschrift für Zellforschung und Mikroskopische Anatomie 144 (1973) 153-166
34. Fahrenbach W.H. The visual system of the horseshoe crab Limulus polyphemus. International Review of Cytology 41 (1975) 285-349
35. Fahrenbach W.H. The morphology of the horseshoe crab (Limulus polyphemus) visual system. VII. Innervation of photoreceptor neurons by neurosecretory efferents. Cell and Tissue Research 216 (1981) 655-659
36. Fahrenbach W.H. Anatomical circuitry of lateral inhibition in the eye of the horseshoe crab, Limulus polyphemus. Proceedings of the Royal Society of London B225 (1985) 219-249
37. Fahrenbach W.H., and Griffin A.J. The morphology of the Limulus visual system VI. Connectivity in the ocellus. Cell and Tissue Research 159 (1975) 39-47
38. Fleissner G. Efferent neurosecretory fibers and pathways for circadian clock signals in the scorpion. Naturwissenshaften 70 (1983) 366
39. Fleissner G.U., and Fleissner G. Efferent control of the visual sensitivity in arthropod eyes: with emphasis on circadian rhythms. In: Lindauer M. (Ed). Information Processing in Animals 5 (1988), Akademie der Wissenshaften und der Literature, Mainz
40. Fleissner G.E., and Fleissner G.U. Non-visual photoreceptors in arthropods with emphasis on their putative role as receptors for natural zeitgeber stimuli. Chronobiology. International 20 (2003) 593-616
41. Fleissner G., and Heinrichs S. Neurosecretory cells in the circadian-clock system of the scorpion, Androctonus australis. Cell and Tissue Research 224 (1982) 233-238
42. Fleissner G.E., Loesel R., Fleissner G.U., Waterkamp M., Kleiner O., Batschauer A., and Homberg U. Candidates for extraocular photoreceptors in the cockroach suggest homology to the lamina and lobula organs in beetles. Journal of Comparative Neurology 433 (2001) 401-414
43. French K.A., 1980. The development of photoreception in Limulus polyphemus: morphology, electrophysiology and behavior. PhD thesis, Boston University Graduate School, 1-168.
44. Fuortes M.G.F., and Yeandel S. Probability of occurrence of discrete potential waves in the eye of Limulus. Journal of General Physiology 47 (1964) 443-463
45. 2+ release and the opening of cGMP-gated channels. BMC Neuroscience 5, 7. Published online 2004 February 26. doi: 10.1186/1471-2202-5-7.
46. Geethabali, and Rao K.P. A metasomatic neural photoreceptor in the scorpion. Journal of Experimental Biology 58 (1973) 189-196
47. Grahm C.H., and Hartline H.K. The response of single visual sense cells to lights of different wavelengths. Journal of General Physiology 18 (1935) 917-931
48. Hanna W.J.B., Horne J.A., and Renninger G.H. Circadian photoreceptor organs in Limulus. II The telson. Journal of Comparative Physiology A 162 (1988) 133-140
49. Hartline, H.K., Wagner, H.G., MacNichol, E.F., Jr., 1952. The peripheral origin of nervous activity in the visual system. Cold Spring Harbor Symposium for Quantitative Biology 17, 124-141.
50. Hartline H.K., Wagner H.G., and Ratliff F. Inhibition in the eye of Limulus. Journal of General Physiology 39 (1956) 651-673
51. Harzsch S. The phylogenetic significance of crustancean optic neuropils and chiasmata: a re-examination. Journal of Comparative Neurology 453 (2002) 10-21
52. Harzsch S., Wildt M., Battelle B., and Waloszek D. Immunohistochemical localization of neurotransmitters in the nervous system of the larval Limulus polyphemus Linnaeus, 1758 (Chelicerata, Xiphosura): evidence for a conserved architecture of the protocerebrum in Euarthropoda. Arthropod Structure and Development 34 (2005) 327-342
53. Harzsch, S., Vilpoux, K., Blackburn, D.C., Platchetzki, D., Brown, N.L., Meizer, R., Kempler, K.E., Battelle, B.-A., 2006. Evolution of arthropod visual systems: development of the eyes and central visual pathways in the horseshoe crab Limulus polyphemus Linnaeus, 1758 (Chelicerata, Xiphosura). Developmental Dynamics, June [Epub].
54. Heinrichs S., and Fleissner G. Neuronal components of the circadian clock in the scorpion, Androctonus australis: central origin of the efferent neurosecretory elements projecting to the median eyes. Cell and Tissue Research 250 (1987) 277-285
55. Herman K. Two classes of Limulus ventral photoreceptors. Journal of Comparative Neurology 303 (1991) 1-10
56. Herman K. Light-stimulated rhabdom turnover in Limulus ventral photoreceptors maintained in vitro. Journal of Comparative Neurology 303 (1991) 11-21
57. Herzog E.D., and Barlow Jr. R.B. Ultraviolet light from the nighttime sky enhances retinal sensitivity of Limulus. Biological Bulletin 181 (1991) 321-322
58. Horne J.A., and Renninger G.H. Circadian photoreceptor organs in Limulus, I. Ventral, median and lateral eyes. Journal of Comparative Physiology A 162 (1988) 127-132
59. Hubbard R., and Wald G. Visual pigment of the horseshoe crab, Limulus polyphemus. Nature 186 (1960) 212
60. Ichikawa T. Brain photoreceptors in the pupal and adult butterfly: fate of the larval ocelli. Zoological Science 8 (1991) 327-330
61. Jones C., Nolte J., and Brown J.E. The anatomy of the median ocellus of Limulus. Zeitschrift für Zellforschung und Mikroskopische Anatomie 118 (1971) 297-309
62. Kaplan E., and Barlow Jr. R.B. Circadian clock in Limulus brain increases response and decreases noise of retinal photoreceptors. Nature 286 (1980) 393-395
63. Kass L., and Barlow Jr. R.B. A circadian clock in the Limulus brain transmits synchronous efferent signals to all eyes. Visual Neuroscience 9 (1992) 493-504
64. Kass L., and Renninger G. Circadian changes in function of Limulus ventral photoreceptors. Visual Neuroscience 1 (1988) 3-11
65. Kennedy D. Physiology of photoreceptor neurons in the abdominal nerve cord of the crayfish. Journal of General Physiology 46 (1963) 551-572
66. Land M.F., and Nilsson D.-E. Animals Eyes (2002), Oxford University Press, New York
67. Lee H.M., and Wyse G.A. Immunocytochemical localization of octopamine in the central nervous system of Limulus polyphemus: a light- and electron-microscopic study. Journal of Comparative Neurology 307 (1991) 683-694
68. 2+ in excitation and adaptation of Limulus ventral photoreceptors. Advances in Experimental Medical Biology 514 (2002) 507-538
69. Millecchia R., Bradbury J., and Mauro A. Simple photoreceptors in Limulus polyphemus. Science 154 (1966) 1199-1201
70. Mori K., and Kuramoto T. Photosensitivity of the central nervous system of Limulus polyphemus. Zoological Science 21 (2004) 731-737
71. Mori K., Saito T., and Kuramoto T. Physiological and morphological identification of photosensitive neurons in the opisthosomal ganglia of Limulus polyphemus. Biological Bulletin 207 (2004) 209-216
72. Nolte J., and Brown J.E. The spectral sensitivities of single cells in the median ocellus of Limulus. Journal of General Physiology 54 (1969) 636-649
73. Nolte J., and Brown J.E. Electrophysiological properties of cells in the median ocellus of Limulus. Journal of General Physiology 59 (1972) 167-185
74. Oberdorfer M.D. The neural organization of the first optic ganglion of the principal eyes of jumping spiders (Salticidae). Journal of Comparative Neurology 174 (1977) 95-118
75. Renninger G.H., Lajolie C., Hanna W.J.B., Fong D., House C., and Zelin J. Phase shifting and entrainment of a circadian rhythm in Limulus polyphemus by ocular and extraocular photoreceptors. Biological Rhythms Research 28 (1997) 50-68
76. Sandeman D.C., Sandeman R.E., and deCouet H.G. Extraretinal photoreceptors in the brain of the crayfish Cherax destructor. Journal of Neurobiology 21 (1990) 619-629
77. Samie F.H., Jinks R.N., Weiner W.W., and Chamberlain S.C. The morphology and physiology of a mini-ommatidium in the median optic nerve of Limulus polyphemus. Visual Neuroscience 12 (1995) 69-76
78. Seifert P., Smola U., and Schinko I. Internal extraocular photoreceptors in a dipteran insect. Cell and Tissue Research 19 (1987) 111-118
79. Shultz J.W., and Regier J.C. Phylogenetic analysis of arthropods using two nuclear protein encoding genes supports a crustacean + hexapod clade. Proceedings of the Royal Society of London B 267 (2000) 1011-1019
80. Smith W.C., Price D.A., Greenberg R.M., and Battelle B.-A. Opsins from the lateral eyes and ocelli of the horseshoe crab, Limulus polyphemus. Proceedings of the National Academy of Science, U.S.A. 90 (1993) 6150-6154
81. Snodderly Jr. D.M. Processing of visual inputs by brain of Limulus. Journal of Neurophysiology 34 (1971) 588-611
82. Strausfeld N.J. The evolution of crustacean and insect lobes and the origins of chiasmata. Arthropod Structure and Development 34 (2005) 235-256
83. Strausfeld N.J., and Barth F.G. Two visual systems in one brain: neuropils serving the secondary eyes of the spider Cupiennius salei. Journal of Comparative Neurology 328 (1993) 43-62
84. Strausfeld N.J., Weltzien P., and Barth F.G. Two visual systems in one brain: neuropils serving the principal eyes of the spider Cupiennius salei. Journal of Comparative Neurology 328 (1993) 63-75
85. Weiner W.W., and Chamberlain S.C. The visual field of American horseshoe crabs: two different eye shapes in Limulus polyphemus. Visual Neuroscience 11 (1994) 333-346
86. Wilkens L.A., and Larimer J.L. Photosensitivity in the sixth abdominal ganglion of Decapod Crustaceans: a comparative study. Journal of Comparative Physiology A 106 (1976) 69-75
87. Yamashita S. Efferent innervation of photoreceptors in spiders. Microscopic Research and Technique 58 (2002) 356-364
88. Yamashita S., and Tateda H. Cerebral photosensitive neurons in the orb weaving spiders, Argiope bruennichii and A. amoena. Journal of Comparative Physiology A 150 (1983) 467-472
89. Zwicky K.T. A light response in the tail of Urodacus, a scorpion. Life Science 7 (1968) 257-262