Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-17T09:17:48.524Z Has data issue: false hasContentIssue false
  • English
  • Français

Dual controls for screening pigment movement in photoreceptors of the Limulus lateral eye: Circadian efferent input and light

Published online by Cambridge University Press:  02 June 2009

Christian K. Kier  and
Steven C. Chamberlain
Christian K. Kier
Affiliation:
Department of Bioengineering, Syracuse University, Syracuse
Steven C. Chamberlain
Affiliation:
Department of Bioengineering, Syracuse University, Syracuse Institute for Sensory Research, Syracuse University, Syracuse
Get access Rights & Permissions [Opens in a new window]

Abstract

The radial and longitudinal distribution of retinular screening pigment in the lateral eye of the horseshoe crab Limulus polyphemus was quantified under a variety of experimental conditions. Pigment position was characterized by the center and width of the radial distribution at four levels in the ommatidium.

Under diurnal lighting, intact animals show movement of pigment granules from the periphery of the retinular cell at night towards the junction of the arhabdomeral and rhabdomeral segments of the retinular cell in the day. In constant darkness, intact animals exhibit the same circadian rhythm in pigment migration. Animals with bilaterally cut optic nerves do not receive circadian efferent input from the brain and show little pigment movement in diurnal lighting. In all of these cases, pigment was either aggregated in a band just peripheral to the rays of the rhabdom or dispersed to the periphery of the retinular cell.

When dark-adapted animals are exposed to a sudden large light increment, pigment moves inward between the rays of the rhabdom. During the day, this inward response begins immediately and reverses as the ommatidial aperture begins to close. At night, the onset of the inward movement is delayed, but then occurs more rapidly than during the day. No significant longitudinal movement of photoreceptor screening pigment was detected under any of these experimental conditions.

Two opposing mechanisms control the movement of screening pigment in these cells. Release of neurotransmitters from the circadian efferents causes outward movement; large increments of light cause inward movement. In the absence of sudden changes in light intensity, circadian efferent input, not cyclic lighting, appears to be the major determinant of screening pigment position. A sudden and large increment of light triggers the rapid inward movement which appears to be a protective mechanism optimized for daytime performance.

Keywords

Retinal screening pigmentCircadian rhythmsLimulusPhotoreceptors
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 3 , March 1990 , pp. 237 - 255
Copyright
Copyright © Cambridge University Press 1990

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barlow, R.B. Jr (1969). Inhibitory fields in the Limulus lateral eye. Journal of General Physiology 54, 383–396.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr, (1983). Circadian rhythms in the Limulus visual system. Journal of Neuroscience 3, 856–870.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr & Chamberlain, S.C. (1980 a). Light and a circadian clock modulate structure and function in Limulus photoreceptors. In The Effects of Constant Light on Visual Processes, ed. Williams, T.P. & Baker, B.N., pp. 247–269. New York: Plenum.CrossRefGoogle Scholar
Barlow, R.B. Jr & Chamberlain, S.C. (1980 b). Microtubule inhibitors can increase the sensitivity of the Limulus eye. Investigative Ophthalmology and Visual Science (Suppl.) 19, 245.Google Scholar
Barlow, R.B. Jr, Bolanowski, S.J. Jr, & Brachman, M.L. (1977). Efferent optic nerve fibers mediate circadian rhythms in the Limulus eye. Science 197, 86–89.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr, & Chamberlain, S.C. & Lehman, H.K. (1989). Circadian rhythms in the invertebrate retina. In Facets of Vision, ed. Stavenga, D. & Hardie, R., pp. 257–280. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Barlow, R.B. Jr, & Chamberlain, S.C. & Levinson, J.Z. (1980). Limulus brain modulates structure and function of the lateral eyes. Science 210, 1037–1039.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr, Ireland, L.C. & Kass, L. (1982). Vision has role in Limulus mating behavior. Nature 296, 65–66.CrossRefGoogle Scholar
Barlow, R.B. Jr, Kaplan, E., Renninger, G.H. & Saito, T. (1987). Circadian rhythms in Limulus photoreceptors, I: Intracellular studies. Journal of General Physiology 89, 353–378.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr, Powers, M.-K. & Kass, L. (1986). Vision and mating behavior in Limulus. In Symposium on the Sensory Biology of Aquatic Animals, ed. Popper, A.N., Fay, R., Atema, J. & Travolga, W., pp. 419–434. Berlin: Springer-Verlag.Google Scholar
Batra, R. & Barlow, R.B. Jr (1982). Efferent control of pattern vision in Limulus. Society for Neuroscience Abstracts 8, 49.Google Scholar
Battelle, B.-A. (1980). Neurostransmitter candidates in the visual system of Limulus polyphemus: Synthesis and distribution of octopamine. Vision Research 20, 911–922.CrossRefGoogle Scholar
Battelle, B.-A. & Evans, J.A. (1984). Octopamine release from centrifugal fibers of the Limulus peripheral visual system. Journal of Neurochemistry 42, 71–79.CrossRefGoogle ScholarPubMed
Battelle, B.-A. & Evans, J.A. (1986). Veratridine-stimulated release of amine conjugates from centrifugal fibers in the Limulus peripheral visual system. Journal of Neurochemistry 46, 1464–1472.CrossRefGoogle ScholarPubMed
Battelle, B.-A., Evans, J.A. & Chamberlain, S.C. (1982). Efferent fibers to Limulus eyes synthesize and release octopamine. Science 216, 1250–1252.CrossRefGoogle Scholar
Battelle, B.-A., Edwards, S.C., Kass, L., Maresch, H.M., Pierce, S.K. & Wishart, A.C. (1988). Identification and function of octopamine and tyramine conjugates in the Limulus visual system. Journal of Neurochemistry 51, 1240–1251.CrossRefGoogle ScholarPubMed
Baur, P.S. Jr, Brown, A.M., Rogers, R.D. & Brower, M.E. (1977). Lipochondria and the light response of Aplysia giant neurons. Journal of Neurobiology 8, 19–42.CrossRefGoogle ScholarPubMed
Behrens, M.E. (1974). Photomechanical changes in the ommatidia of the Limulus lateral eye during light and dark adaptation. Journal of Comparative Physiology 89, 45–57.CrossRefGoogle Scholar
Bennitt, R. (1932). Diurnal rhythm in the proximal pigment cells of the crayfish retina. Physiological Zoology 5, 65–69.Google Scholar
Bernhard, C.G. & Ottoson, D. (1964). Quantitative studies on pigment migration and light sensitivity in the compound eye at different light intensities. Journal of General Physiology 47, 465–478.CrossRefGoogle ScholarPubMed
Boll, F. (1877). Zur Anatomic und Physiologic der Retina. Archiv für Physiologie 10, 4–36.Google Scholar
Brandenburg, J., Bobbert, A. & Eggelmeyer, F. (1981). Evidence for the existence of a retino-hypothalamo-retinal loop in rabbits. International Journal of Chronobiology 8, 13–29.Google ScholarPubMed
Brown, A.M., Baur, B.S. & Tutley, F.H. (1975). Phototransduction in Aplysia neurons: calcium release from pigmented granules is essential. Science 188, 157–160.CrossRefGoogle ScholarPubMed
Butler, R. & Horridge, G.A. (1973). The electrophysiology of the retina of Periplaneta americana, I: Changes in receptor acuity upon light/dark adaptation. Journal of Comparative Physiology 83, 263–278.Google Scholar
Calman, B.G. (1988). Neuroanatomical studies of the visual system of Limulus polyphemus. Syracuse University, Institute for Sensory Research Special Report ISR-S-26.Google Scholar
Calman, B.G. & Chamberlain, S.C. (1982). Distinct lobes of Limulus ventral photoreceptors, II: Structure and ultrastructure. Journal of General Physiology 80, 839–862.CrossRefGoogle ScholarPubMed
Chamberlain, S.C. & Barlow, R.B. Jr (1977). Morphological correlates of efferent circadian activity and light adaptation in the Limulus lateral eye. Biological Bulletin 153, 418–419.Google Scholar
Chamberlain, S.C. & Barlow, R.B. Jr (1979). Light and efferent activity control rhabdom turnover in Limulus photoreceptors. Science 206, 361–363.CrossRefGoogle ScholarPubMed
Chamberlain, S.C. & Barlow, R.B. Jr (1981). Modulation of retinal structure in Limulus lateral eye: interactions of light and efferent inputs. Investigative Ophthalmology and Visual Science (Suppl.) 20, 75.Google Scholar
Chamberlain, S.C. & Barlow, R.B. Jr (1984). Transient membrane shedding in Limulus photoreceptors: control mechanisms under natural lighting. Journal of Neuroscience 4, 2792–2810.CrossRefGoogle ScholarPubMed
Chamberlain, S.C. & Barlow, R.B. Jr (1987). Control of structural rhythms in the lateral eye of Limulus: interactions of natural lighting and circadian efferent activity. Journal of Neuroscience 7, 2135–2144.Google Scholar
Clark, A.W., Millecchia, R. & Mauro, A. (1969). The ventral photoreceptor cells of Limulus, I: The microanatomy. Journal of General Physiology 54, 289–309.CrossRefGoogle ScholarPubMed
Day, M.F. (1941). Pigment migration in the eye of the moth Ephestia kühniella Zeller. Biological Bulletin 80, 275–291.CrossRefGoogle Scholar
Demoll, R. (1911). über die Wanderung des Irispigments im Facettenauge. Zoologische Jahrbücher Abteilung für Allgemeine Zoologie und Physiologie der Tiere 30, 169–180.Google Scholar
Demoll, R. (1917). Die Sinnesorgane der Arthropoden, ihr Bau und ihre Funktion. Braunschweig: Vieweg.CrossRefGoogle Scholar
Edwards, S.C. & Battelle, B-A. (1987). Octopamine and cyclic AMP-stimulated phosphorylation of a protein in Limulus ventral and lateral eyes. Journal of Neuroscience 7, 2811–2820.CrossRefGoogle ScholarPubMed
Evans, J.A., Chamberlain, S.C. & Battelle, B.-A. (1983). Autoradiographic localization of newly synthesized octopamine in retinal efferents in the Limulus visual system. Journal of Comparative Neurology 219, 369–383.CrossRefGoogle ScholarPubMed
Exner, S. (1889). Durch Licht bedingte Verschiebungen des Pigmentes im lnsektenauge und deren physiologische Bedeutung. Ebenda 98, 143–151.Google Scholar
Exner, S. (1891). Die Physiologie der facettirlen Augen von Krebsen und Insecten. Leipzig-Wein: Franz Deuticke.Google Scholar
Fahrenbach, W.H. (1969). The morphology of the eyes of Limulus, II: Ommatidia of the compound eye. Zeitschrtft für Zellforschung 93, 451–483.Google Scholar
Fahrenbach, W.H. (1973). The morphology of the Limulus visual system, V: Protocerebral neurosecretion and ocular innervation. Zeitschrift für Zellforschung 144, 153–166.CrossRefGoogle Scholar
Fahrenbach, W.H. (1975). The visual system of the horseshoe crab Limulus polyphemus. International Review of Cytology 41, 285–349.CrossRefGoogle ScholarPubMed
Fahrenbach, W.H. (1981). The morphology of the Limulus visual system, VII: Innervation of photoreceptor neurons by neurosecretory efferents. Cell and Tissue Research 216, 655–659.Google Scholar
Fleissner, G. & Fleissner, G. (1978). The optic nerve mediates the circadian pigment migration in the median eyes of the scorpion. Comparative Biochemistry and Physiology A 61, 69–71.CrossRefGoogle Scholar
Franceschini, N. & Kirschfeld, K. (1976). Le contrâle automatique du flux lumineux dans l'oeil composé des Diptères. Propriétés spectrales, statiques et dynamiques du méchanisme. Biological Cybernetics 21, 181–203.CrossRefGoogle Scholar
Goldsmith, T.H. & Bernard, G.D. (1974). The visual system of insects. In The Physiology of Insecta, ed. Rockstein, M., pp. 165–272. New York: Academic Press.Google Scholar
Grenacher, H. (1879). Untersuchungen über das Sehorgan der Arthropoden. Göttingen: Vandenhoek und Ruprecht.Google Scholar
Hamdorf, K., Höglund, G. & Juse, A. (1986). Ultraviolet- and blue-induced migration of screening pigment in the retina of the moth Deilephila elpenor. Journal of Comparative Physiology A 159, 353–362.Google Scholar
Henkart, M. (1975). Light-induced changes in the structure of pigmented granules in Aplysia neurons. Science 188, 155–157.CrossRefGoogle ScholarPubMed
Höglund, G. (1966). Pigment migration and retinula sensitivity. In The Functional Organization of the Compound Eye, ed. Berhnard, S., pp. 77–88. New York: Pergamon Press.Google Scholar
Horridge, G.A., Marcelja, L., Jahnke, R. & McIntyre, P. (1983). Daily changes in the compound eye of a beetle (Macrogyrus). Proceedings of the Royal Society (London) 217, 265–285.Google Scholar
Horstmann, E. (1935). Die tagesperiodische Pigmentwanderung in Facettenaugen von Nachtschmetterlingen. Biologisches Zentralblatt 55: 93–97.Google Scholar
Juse, A., Höglund, G. & Hamdorf, K. (1987). Reversed light reaction of the screening pigment in a compound eye induced by noradrenaline. Zeitschrift für Naturforschung C 42, 973–976.CrossRefGoogle Scholar
Kaplan, E. & Barlow, R.B. Jr (1975). Properties of visual cells in the lateral eye of Limulus in situ: extracellular recordings. Journal of General Physiology 66, 303–326.Google Scholar
Kaplan, E. & Barlow, R.B. Jr (1980). Circadian clock in Limulus brain increases response and decreases noise of retinal photoreceptors. Nature 286, 393–395.Google Scholar
Kass, L. & Barlow, R.B. Jr (1984). Efferent neurotransmission of circadian rhythms in Limulus lateral eye, I. Octopamine-induced increases in retinal sensitivity. Journal of Neuroscience 4, 908–917.CrossRefGoogle ScholarPubMed
Kass, L., Pelletier, J.L., Renninger, G.H. & Barlow, R.B. Jr (1988). Efferent neurotransmission of circadian rhythms in Limulus lateral eye, II: Intracellular recordings in vitro. Journal of Comparative Physiology A 164, 95–105.CrossRefGoogle ScholarPubMed
Kaupp, U.B., Malbon, C.C., Battelle, B-A. & Brown, J.E. (1982). Octopamine stimulated rise of cAMP in Limulus ventral photoreceptors. Vision Research 22, 1503–1506.CrossRefGoogle ScholarPubMed
Kier, C.K. & Chamberrlain, S.C. (1988 a). Dual control of screening pigment movement in the photoreceptors of the Limulus lateral eye: effects of light and circadian efferent inputs. Investigative Ophthalmology and Visual Science (Suppl.) 29, 351.Google Scholar
Kier, C.K. & Chamberlain, S.C. (1988 b). Photoreceptor screening pigment in Limulus lateral eye: distribution, movement, and control mechanisms. Society for Neuroscience Abstracts 14, 376.Google Scholar
Kiesel, A. (1894). Untersuchungen zur Physiologie des facettierten Auges. Sitzungberichte der Akademie der Wissenschaften in Wien, Mathematisch-Naturwissenschaftliche Klasse Abteilung 3 103, 97–139.Google Scholar
Kirschfeld, K. & Franceschini, N. (1969). Em Mechanismus zur Steuerung des Lichtflusses in den Rhabdomeren des Komplexauges von Musca. Kybernetik 6, 12–22.Google Scholar
Kühne, W. (1877). Uber den Sehpurpur. Untersuchung physiol. Inst. Heidelberg 1, 15–104.Google Scholar
Kunze, P. (1979). Apposition and superposition eyes. In Handbook of Sensory Physiology, Vol. VII/6A, Vision in Invertebrates, A. Invertebrate Photoreceptors, ed. Autrum, H., pp. 442–502. Berlin: Springer-Verlag.Google Scholar
Land, M.F. (1987). Screening pigment migration in a sphingid moth is triggered by light near the cornea. Journal of Comparative Physiology A 160, 355–357.CrossRefGoogle Scholar
Lankester, E.R. & Bourne, A.B. (1883). The minute structure of the lateral and the central eyes of Scorpio and of Limulus. Quarterly Journal of Microscopical Science 23, 177–212.Google Scholar
Lehman, H.K. & Barlow, R.B. Jr (1987 a). Multiple transmitters mediate circadian rhythms in the Limulus lateral eye. Investigative Ophthalmology and Visual Science (Suppl.) 28, 186.Google Scholar
Lehman, H.K. & Barlow, R.B. Jr (1987 b). An efferent neuropeptide in the eye of Limulus. Society for Neuroscience Abstracts 13, 237.Google Scholar
Lehman, H.K., Lewandowski, T.J., Johnson, J.K. & Chamberlain, S.C. (1988). Substance P is not an efferent neurotransmitter in the Limulus eye. Society for Neuroscience Abstracts 14, 535.Google Scholar
Lewandowski, T.J., Lehman, H.K. & Chamberlain, S.C. (1989). Immunoreactivity in Limulus, III: Morphological and biochemical studies of FMRFamide-like immunoreactivity and colocalized substance P-like immunoreactivity in the brain and lateral eye. Journal of Comparative Neurology 288, 136–153.CrossRefGoogle ScholarPubMed
Mazokhin-Porshnyakov, G.A. (1969). Insect Vision. New York: Plenum Press.Google Scholar
Meyer-Rochow, V.B. & Eguchi, E. (1986). Do disintegrating microvilli in the eye of the crayfish Procambarus clarkii contribute to the synthesis of screening pigment granules? Zeitschrift für Mikroskopisch-Anatomische Forschung 100, 39–55.Google Scholar
Miller, W.H. (1957). Morphology of the ommatidia of the compound eye of Limulus. Journal of Biophysical and Biochemical Cytology 3, 421–427.Google Scholar
Miller, W.H. (1975). Mechanisms of photomechanical movement. In Photoreceptor Optics, ed. Snyder, A.W. & Menzel, R., pp. 415–428. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Miller, W.H. (1979). Ocular optical filtering. In Handbook of Sensory Physiology, Vol. VII/6A, Vision in In vertebrates, A. Invertebrate Photoreceptors, ed. Autrum, H., pp. 69–143. Berlin: Springer–Verlag.Google Scholar
Miller, W.H. & Cawthon, D.F. (1974). Pigment granule movement in Limulus photoreceptors. Investigative Ophthalmology 13, 401–405.Google Scholar
Page, T.L. & Larimer, J.L. (1975). Neural control of circadian rhythmicity in the crayfish, II: The ERG amplitude rhythm. Journal of Comparative Physiology A 97, 81–96.CrossRefGoogle Scholar
Parker, G.H. (1932). The movements of the retinal pigment. Ergebnisse der Biologie 9, 239–291.CrossRefGoogle Scholar
Rawitz, B. (1891). Zur Physiologie der Cephalopodenretina. Archiv für Physiologie 24, 367–372.Google Scholar
Renninger, G.H., Kaplan, E. & Barlow, R.B. Jr (1984). A circadian clock increases the gain of photoreceptor cells in the Limulus lateral eye. Biological Bulletin 167, 532.Google Scholar
Stavenga, D.G. (1977). Optics of compound eyes and circadian pigment movements studied by pseudopupil observations in vivo. Biological Bulletin 153, 446.Google Scholar
Stavenga, D.G. (1979). Pseudopupils of compound eyes. In Handbook of Sensory Physiology, Vol. VII/6A, Vision in Invertebrates, A. Invertebrate Photoreceptors, ed. Autrum, H., pp. 358–441. Berlin: Springer-Verlag.Google Scholar
Sugaya, E. & Onozuka, M. (1978). Intracellular calcium: its release from granules during bursting activity in snail neurons. Science 202, 1195–1197.Google Scholar
Teirstein, P.S., Goldman, A.I. & O'Brien, P.J. (1980). Evidence for both local and central regulation of rat outer segment disc shedding. Investigative Ophthalmology and Visual Science 19, 1268–1273.Google Scholar
Trump, B.F., Smuckler, E.A. & Benditt, E.P. (1961). A method for staining epoxy sections for light microscopy. Journal of Ultrastructure Research 5, 343–348.Google Scholar
Tunstall, J. & Horridge, G.A. (1967). Electrophysiological investigation of the optics of the locust retina. Zeirschrift für vergleindische Physiologie 55, 167–172.Google Scholar
Tuurala, O. (1954). Histologishe und physiologische Untersuchungen über die photomechanischen Erscheinungen in den Augen der Lepidopteren. Annales Academiae Scienliarum Fennicae, Series A 24, 1–69.Google Scholar
Walcott, B. (1975). Anatomical changes during light-adaptation in insect compound eyes. In The Compound Eye and Vision of Insects, ed. Horridge, G.A., pp. 20–33, Oxford: Clarendon Press.Google Scholar
Welsh, J.H. (1930). Diurnal rhythm of the distal pigment cells in the eyes of certain crustaceans. Proceedings of the National Academy of Sciences of the U.S.A. 16, 386–395.Google Scholar
White, R.H. & Michaud, N.A. (1980). Calcium is a component of ommochrome pigment granules in insect eyes. Comparative Biochemistry and Physiology A 65, 239–242.CrossRefGoogle Scholar
White, R.H., Banister, M.J. & Bennett, R.R. (1983). Spectral sensitivity of pigment migration in the compound eye of Manduca sexta. Journal of Comparative Physiology A 153, 59–66.Google Scholar
Yamashita, S. & Tateda, M. (1981). Efferent neural control in the eyes of orb weaving spiders. Journal of Comparative Physiology A 143, 477–483.CrossRefGoogle Scholar