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Photoreceptor projections and receptive fields in the dorsal rim area and main retina of the locust eye

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Abstract

In many insect species, photoreceptors of a small dorsal rim area of the eye are specialized for sensitivity to the oscillation plane of polarized skylight and, thus, serve a role in sky compass orientation. To further understand peripheral mechanisms of polarized-light processing in the optic lobe, we have studied the projections of photoreceptors and their receptive fields in the main eye and dorsal rim area of the desert locust, a model system for polarization vision analysis. In both eye regions, one photoreceptor per ommatidium, R7, has a long visual fiber projecting through the lamina to the medulla. Axonal fibers from R7 receptors of the dorsal rim area have short side branches throughout the depth of the dorsal lamina and maintain retinotopic projections to the dorsal medulla following the first optic chiasma. Receptive fields of dorsal rim photoreceptors are considerably larger (average acceptance angle 33°) than those of the main eye (average acceptance angle 2.04°) and, taken together, cover almost the entire sky. The data challenge previous reports of two long visual fibers per ommatidium in the main eye of the locust and provide data for future analysis of peripheral networks underlying polarization opponency in the locust brain.

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References

  • Armett-Kibel C, Meinertzhagen IA (1985) The long visual fibers of the dragonfly optic lobe: their cells of origin and lamina connections. J Comp Neurol 242:459–474

    Article  CAS  PubMed  Google Scholar 

  • Bech M, Homberg U, Pfeiffer K (2014) Receptive fields of locust brain neurons are matched to polarization patterns of the sky. Curr Biol 24:2124–2129

    Article  CAS  PubMed  Google Scholar 

  • Blum M, Labhart T (2000) Photoreceptor visual fields, ommatidial array, and receptor axon projections in the polarisation-sensitive dorsal rim area of the cricket compound eye. J Comp Physiol A 186:119–128

    Article  CAS  PubMed  Google Scholar 

  • Briscoe AD, Bernard GD, Szeto AS, Nagy LM, White RH (2003) Not all butterfly eyes are created equal: rhodopsin absorption spectra, molecular identification, and localization of ultraviolet-, blue-, and green-sensitive rhodopsin-encoding mRNAs in the retina of Vanessa cardui. J Comp Neurol 458:334–349

    Article  CAS  PubMed  Google Scholar 

  • Brunner D, Labhart T (1987) Behavioural evidence for polarization vision in crickets. Physiol Entomol 12:1–10

    Article  Google Scholar 

  • Burkhardt D, Streck P (1965) Das Sehfeld einzelner Sehzellen: Eine Richtigstellung. Z Vgl Physiol 51:151–152

    Google Scholar 

  • Buschbeck EK, Ehmer B, Hoy RR (2003) The unusual visual system of the Strepsiptera: external eye and neuropils. J Comp Physiol A 189:617–630

    Article  CAS  Google Scholar 

  • Dacke M, Nordström P, Scholtz C (2003) Twilight orientation to polarized light in the crepuscular dung beetle Scarabaeus zambesianus. J Exp Biol 206:1535–1543

    Article  PubMed  Google Scholar 

  • el Jundi B, Homberg U (2010) Evidence for the possible existence of a second polarization-vision pathway in the locust brain. J Insect Physiol 56:971–979

    Article  PubMed  Google Scholar 

  • el Jundi B, Homberg U (2012) Receptive field properties and intensity-response functions of polarization-sensitive neurons of the optic tubercle in gregarious and solitarious locusts. J Neurophysiol 108:1695–1710

    Article  PubMed  Google Scholar 

  • el Jundi B, Pfeiffer K, Homberg U (2011) A distinct layer of the medulla integrates sky compass signals in the brain of an insect. PLoS One 6:e27855

    Article  PubMed Central  PubMed  Google Scholar 

  • Fischbach KF, Dittrich APM (1989) The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res 258:441–475

    Article  Google Scholar 

  • Gebhardt S, Homberg U (2004) Immunocytochemistry of histamine in the brain of the locust Schistocerca gregaria. Cell Tissue Res 317:195–205

    Article  CAS  PubMed  Google Scholar 

  • Greiner B, Ribi WA, Wcislo WT, Warrant EJ (2004) Neural organization in the first optic ganglion of the nocturnal bee Megalopta genalis. Cell Tissue Res 318:429–437

    Article  PubMed  Google Scholar 

  • Hamanaka Y, Shibasaki H, Kinoshita M, Arikawa K (2013) Neurons innervating the lamina in the butterfly, Papilio xuthus. J Comp Physiol A 199:341–351

    Article  CAS  Google Scholar 

  • Hardie RC (1987) Is histamine a neurotransmitter in insect photoreceptors? J Comp Physiol A 161:201–213

    Article  CAS  PubMed  Google Scholar 

  • Hardie RC (1989) A histamine-activated chloride channel involved in neurotransmission at a photoreceptor synapse. Nature 339:704–706

    Article  CAS  PubMed  Google Scholar 

  • Hardie RC, Franceschini N, Ribi W, Kirschfeld K (1981) Distribution and properties of sex-specific photoreceptors in the fly Musca domestica. J Comp Physiol A 145:139–152

    Article  Google Scholar 

  • Heinze S, Homberg U (2008) Neuroarchitecture of the central complex of the desert locust: intrinsic and columnar neurons. J Comp Neurol 511:454–478

    Article  PubMed  Google Scholar 

  • Homberg U, el Jundi B (2013) Polarization vision in arthropods. In: Werner JS, Chalupa LM (eds) The new visual neurosciences. MIT Press, Cambridge, pp 1207–1217

    Google Scholar 

  • Homberg U, Paech A (2002) Ultrastructure and orientation of ommatidia in the dorsal rim of the locust compound eye. Arthropod Struct Dev 30:271–280

    Article  PubMed  Google Scholar 

  • Homberg U, Würden S (1997) Movement-sensitive, polarization-sensitive, and light-sensitive neurons of the medulla and accessory medulla of the locust, Schistocerca gregaria. J Comp Neurol 386:329–346

    Article  CAS  PubMed  Google Scholar 

  • Homberg U, Hofer S, Pfeiffer K, Gebhardt S (2003) Organization and neural connections of the anterior optic tubercle in the brain of the desert locust, Schistocerca gregaria. J Comp Neurol 462:415–430

    Article  PubMed  Google Scholar 

  • Homberg U, Heinze S, Pfeiffer K, Kinoshita M, el Jundi B (2011) Central neural coding of sky polarization in insects. Philos Trans R Soc B 366:680–687

    Article  Google Scholar 

  • Horridge GA, Meinertzhagen IA (1970) The exact neural projection of the visual fields upon first and second ganglia of the insect eye. Z Vgl Physiol 66:369–378

    Article  Google Scholar 

  • Horváth G, Varjú D (2004) Polarized light in animal vision: Polarization patterns in nature. Springer, Heidelberg

    Book  Google Scholar 

  • Klagges BR, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E (1996) Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16:3154–3165

    CAS  PubMed  Google Scholar 

  • Kurylas AE, Rohlfing T, Krofczik S, Jenett A, Homberg U (2008) Standardized atlas of the brain of the desert locust, Schistocerca gregaria. Cell Tissue Res 333:125–145

    Article  PubMed  Google Scholar 

  • Labhart T (1980) Specialized photoreceptors at the dorsal rim of the honeybee’s compound eye: polarizational and angular sensitivity. J Comp Physiol A 141:19–30

    Article  Google Scholar 

  • Labhart T (1986) The electrophysiology of photoreceptors in different eye regions of the desert ant Cataglyphis bicolor. J Comp Physiol A 158:1–7

    Article  Google Scholar 

  • Labhart T (1988) Polarization-opponent interneurons in the insect visual system. Nature 331:435–437

    Article  Google Scholar 

  • Labhart T (1999) How polarization-sensitive interneurons of crickets see the polarization pattern of the sky: a field study with an opto-electronic model neuron. J Exp Biol 202:757–770

    PubMed  Google Scholar 

  • Labhart T, Meyer E (1999) Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc Res Tech 47:368–379

    Article  CAS  PubMed  Google Scholar 

  • Labhart T, Meyer E (2002) Neural mechanism in insect navigation: polarization compass and odometer. Curr Opin Neurobiol 12:707–714

    Article  CAS  PubMed  Google Scholar 

  • Labhart T, Petzold J (1993) Processing of polarized light information in the visual system of crickets. In: Wiese K, Gribakin FG, Popov AV, Renninger G (eds) Sensory systems of arthropods. Birkhäuser, Basel, pp 158–169

    Google Scholar 

  • Labhart T, Hodel B, Valenzuela I (1984) The physiology of the cricket’s compound eye with particular references to the anatomically specialized dorsal rim area. J Comp Physiol A 155:289–296

    Article  Google Scholar 

  • Lillywhite PG (1978) Coupling between locust photoreceptors revealed by study of quantum bumps. J Comp Physiol A 125:13–27

    Article  Google Scholar 

  • Mappes M, Homberg U (2004) Behavioral analysis of polarization vision in tethered flying locusts. J Comp Physiol A 190:61–68

    Article  CAS  Google Scholar 

  • Meyer EP (1984) Retrograde labeling of photoreceptors in different eye regions of the compound eye of bees and ants. J Neurocytol 13:825–836

    Article  CAS  PubMed  Google Scholar 

  • Mouritsen H, Derbyshire R, Stalleicken J, Mouritsen OØ, Frost BJ, Norris DR (2013) An experimental displacement and over 50 years of tag-recoveries show that monarch butterflies are not true navigators. Proc Natl Acad Sci 110:7348–7353

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nässel DR (1999) Histamine in the brain of insects: a review. Microsc Res Tech 44:121–136

    Article  PubMed  Google Scholar 

  • Nowel MS, Shelton PMJ (1981) A Golgi-electron-microscopical study of the structure and developement of the lamina ganglionaris of the locust optic lobe. Cell Tissue Res 216:377–401

    Article  CAS  PubMed  Google Scholar 

  • Oberhauser KS, Taylor OR, Reppert SM, Dingle H, Nail KR, Pyle RM, Stenoien C (2013) Are monarch butterflies true navigators? The jury is still out. Proc Natl Acad Sci 110:E3680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paulk AC, Dacks AM, Gronenberg W (2009) Color processing in the medulla of the bumblebee (Apidae: Bombus impatiens). J Comp Neurol 513:441–456

    Article  PubMed  Google Scholar 

  • Pollack I, Hofbauer A (1991) Histamine-like immunoreactivity in the visual system and brain of Drosophila melanogaster. Cell Tissue Res 226:391–398

    Article  Google Scholar 

  • Reppert SM, Zhu H, White RH (2004) Polarized light helps monarch butterflies navigate. Curr Biol 14:155–158

    Article  CAS  PubMed  Google Scholar 

  • Ribi WA (1975a) Golgi studies of the first optic ganglion of the ant, Cataglyphis bicolor. Cell Tissue Res 160:207–217

    Article  CAS  PubMed  Google Scholar 

  • Ribi WA (1975b) The first optic ganglion of the bee. Cell Tissue Res 165:103–111

    Article  CAS  PubMed  Google Scholar 

  • Ribi WA, Scheel M (1981) The second and third optic ganglia of the worker bee. Cell Tissue Res 221:17–43

    Article  CAS  PubMed  Google Scholar 

  • Schmeling F, Wakakuwa M, Tegtmeier J, Kinoshita M, Bockhorst T, Arikawa K, Homberg U (2014) Opsin expression, physiological characterization and identification of photoreceptor cells in the dorsal rim area and main retina of the desert locust, Schistocerca gregaria. J Exp Biol 217:3557–3568

    Article  PubMed  Google Scholar 

  • Shashar N, Sabbah S, Aharoni N (2005) Migratory locusts can detect polarized reflections to avoid flying over the sea. Biol Lett 1:472–475

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shaw SR (1967) Simultaneous recording from two cells in the locust retina. Z Vgl Physiol 55:183–194

    Article  Google Scholar 

  • Shaw SR (1969) Interreceptor coupling in ommatidia of drone honeybee and locust compound eyes. Vis Res 9:999–1029

    Article  CAS  PubMed  Google Scholar 

  • Shimohigashi M, Tominaga Y (1991) Identification of UV, green and red receptors, and their projection to lamina in the cabbage butterfly, Pieris rapae. Cell Tissue Res 263:49–59

    Article  Google Scholar 

  • Simpson S, McCaffery A, Hägele BF (1999) A behavioural analysis of phase change in the desert locust. Biol Rev 74:461–480

    Article  Google Scholar 

  • Spaethe J, Briscoe AD (2005) Molecular characterization and expression of the UV opsin in bumblebees: three ommatidial subtypes in the retina and a new photoreceptor organ in the lamina. J Exp Biol 208:2347–2361

    Article  CAS  PubMed  Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  CAS  PubMed  Google Scholar 

  • Stalleicken J, Labhart T, Mouritsen H (2006) Physiological characterization of the compound eye in monarch butterflies with focus on the dorsal rim area. J Comp Physiol A 192:321–331

    Article  Google Scholar 

  • Strausfeld NJ (1971) The organization of the insect visual system (light microscopy) - I. Projections and arrangements of neurons in the lamina ganglionaris of Diptera. Z Zellforsch 121:377–441

    Article  Google Scholar 

  • Takemura S-Y, Kinoshita M, Arikawa K (2005) Photoreceptor projection reveals heterogeneity of lamina cartridges in the visual system of the Japanese yellow swallowtail butterfly, Papilio xuthus. J Comp Neurol 483:341–350

    Article  PubMed  Google Scholar 

  • Takemura S-Y, Lu Z, Meinertzhagen IA (2008) Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. J Comp Neurol 509:493–513

    Article  PubMed Central  PubMed  Google Scholar 

  • von Frisch K (1949) Die Polarisation des Himmelslichts als orientierender Faktor bei den Tänzen der Biene. Experientia 5:142–148

    Article  CAS  PubMed  Google Scholar 

  • von Philipsborn A, Labhart T (1990) A behavioural study of polarization vision in the fly, Musca domestica. J Comp Physiol A 167:737–743

    Article  Google Scholar 

  • Wakakuwa M, Kurasawa M, Giurfa M, Arikawa K (2005) Spectral heterogeneity of honeybee ommatidia. Naturwissenschaften 92:464–467

    Article  CAS  PubMed  Google Scholar 

  • Wehner R (1982) Himmelsnavigation bei Insekten: Neurophysiologie und Verhalten. Neujahrsblatt Naturforsch Ges Zürich 184:1–132

    Google Scholar 

  • Wehner R, Labhart T (2006) Polarization vision. In: Warrant E, Nilsson D-E (eds) Invertebrate Vision. Cambridge University Press, Cambridge, pp 291–348

    Google Scholar 

  • Wehner R, Müller M (2006) The significance of direct sunlight and polarized skylight in the ant’s celestial system of navigation. Proc Natl Acad Sci 103:12575–12579

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Weir PT, Dickinson MH (2012) Flying Drosophila orient to sky polarization. Curr Biol 22:21–27

    Article  CAS  PubMed  Google Scholar 

  • Wendt B, Homberg U (1992) Immunocytochemistry of dopamine in the brain of the locust Schistocerca gregaria. J Comp Neurol 321:387–403

    Article  CAS  PubMed  Google Scholar 

  • Wernet MF, Desplan C (2004) Building a retinal mosaic: cell-fate decision in the fly eye. Trends Cell Biol 14:576–584

    Article  CAS  PubMed  Google Scholar 

  • Wernet MF, Velez MM, Clark DA, Baumann-Klausener F, Brown JR, Klovstad M, Labhart T, Clandinin TR (2012) Genetic dissection reveals two separate retinal substrates for polarization vision in Drosophila. Curr Biol 22:12–20

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • White RH, Xu H, Münch TA, Bennett RR, Grable EA (2003) The retina of Manduca sexta: rhodopsin expression, the mosaic of green-, blue- and UV-sensitive photoreceptors, and regional specialization. J Exp Biol 206:3337–3348

    Article  CAS  PubMed  Google Scholar 

  • Williams DS (1983) Changes of photoreceptor performance associated with the daily turnover of photoreceptor membrane in locusts. J Comp Physiol 150:509–519

    Article  Google Scholar 

  • Wilson M, Garrard P, McGinness S (1978) The unit structure of the locust compound eye. Cell Tissue Res 195:205–226

    Article  CAS  PubMed  Google Scholar 

  • Wolburg-Buchholz K (1979) The organization of the lamina ganglionaris of the hemipteran insects, Notonecta glauca, Corixa punctata and Gerris lacustris. Cell Tissue Res 197:39–59

    Article  CAS  PubMed  Google Scholar 

  • Zufall F (1984) Physiologische und morphologische Charakterisierung der Retinulazellen im Komplexauge der Grillen (Gryllus bimaculatus). Diploma thesis, Freie Universität Berlin

  • Zufall F, Schmitt M, Menzel R (1989) Spectral and polarized light sensitivity of photoreceptors in the compound eye of the cricket (Gryllus bimaculatus). J Comp Physiol A 164:597–608

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Dr. Erich Buchner (University of Würzburg) for donation of the anti-synapsin antibody. We thank Matthias Schön for technical assistance and Martina Kern, Jerome Beetz, and Johannes Schuh for maintaining the locust cultures. This work was supported by grants from Deutsche Forschungsgemeinschaft (HO 950/20-1) to UH and the Japan Society for the Promotion of Science (#24570084) to MK.

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Schmeling, F., Tegtmeier, J., Kinoshita, M. et al. Photoreceptor projections and receptive fields in the dorsal rim area and main retina of the locust eye. J Comp Physiol A 201, 427–440 (2015). https://doi.org/10.1007/s00359-015-0990-y

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