The optic lobe projection pattern of polarization-sensitive photoreceptor cells in Drosophila melanogaster

SummaryHistological staining of wild-type and sevenless transgenic Drosophila melanogaster bearing Rh3-lacZ fusion genes permits the selective visualization of polarization-sensitive R7 and R8 photoreceptor cells located along the dorsal anterior eye margin. Diffusion of β-galactosidase throughout these cells reveals that they project long axons to the two most peripheral synaptic target rows of the dorsal posterior medulla, defining a specialized marginal zone of this optic lobe. Comparison of the staining patterns of marginal and nonmarginal Rh3-lacZ-expressing photoreceptor cells in the same histological preparations suggests that the marginal cells possess morphologically specialized axons and synaptic terminals. These findings are discussed with reference to the neuroanatomy of the corresponding dorsal marginal eye and optic lobe regions of the larger dipterans Musca and Calliphora, and in relation to the ability of Drosophila to orient to polarized light.

[1]  G. Rubin,et al.  Analysis of cis-acting requirements of the Rh3 and Rh4 genes reveals a bipartite organization to rhodopsin promoters in Drosophila melanogaster. , 1990, Genes & development.

[2]  K. Frisch Orientierungsvermögen und Sprache der Bienen , 2004, Naturwissenschaften.

[3]  N. Franceschini,et al.  Etude optique in vivo des éléments photorécepteurs dans l'œil composé de Drosophila , 2004, Kybernetik.

[4]  G. Rubin,et al.  Analysis of the promoter of the Rh2 opsin gene in Drosophila melanogaster. , 1987, Genetics.

[5]  K. Fent,et al.  Polarized skylight orientation in the desert antCataglyphis , 1986, Journal of Comparative Physiology A.

[6]  B. Hämmerle,et al.  Structure of the dorsal eye region of the moth, Adoxophyes reticulana Hb. (Lepidoptera : Tortricidae) , 1987 .

[7]  R. Hardie,et al.  Properties of photoreceptors R7 and R8 in dorsal marginal ommatidia in the compound eyes ofMusca andCalliphora , 1984, Journal of Comparative Physiology A.

[8]  K. Fischbach,et al.  The optic lobe of Drosophila melanogaster , 2004, Cell and Tissue Research.

[9]  H. Wunderer,et al.  Fine structure of ommatidia at the dorsal eye margin of Calliphora erythrocephala meigen (Diptera: Calliphoridae): An eye region specialised for the detection of polarized light , 1982 .

[10]  Rüdiger Wehner,et al.  Polarization vision in bees , 1986, Nature.

[11]  R. Hardie,et al.  Histamine-like immunoreactivity in photoreceptors of the compound eyes and ocelli of the flies Calliphora erythrocephala and Musca domestica , 1988, Cell and Tissue Research.

[12]  S. Benzer,et al.  Molecular characterization and expression of sevenless, a gene involved in neuronal pattern formation in the Drosophila eye , 1987, Cell.

[13]  Thomas Labhart,et al.  Specialized photoreceptors at the dorsal rim of the honeybee's compound eye: Polarizational and angular sensitivity , 1980, Journal of comparative physiology.

[14]  Rüdiger Wehner,et al.  Neurobiology of polarization vision , 1989, Trends in Neurosciences.

[15]  T. Labhart The electrophysiology of photoreceptors in different eye regions of the desert ant,Cataglyphis bicolor , 2004, Journal of Comparative Physiology A.

[16]  W. Harris,et al.  Genetic dissection of the photoreceptor system in the compound eye of Drosophila melanogaster , 1976, The Journal of physiology.

[17]  C. Meinecke The fine structure of the compound eye of the African armyworm moth, Spodoptera exempta walk. (Lepidoptera, Noctuidae) , 2004, Cell and Tissue Research.

[18]  G. Rubin,et al.  A rhodopsin gene expressed in photoreceptor cell R7 of the Drosophila eye: homologies with other signal-transducing molecules , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  Reinhard Wolf,et al.  Polarization sensitivity of course control inDrosophila melanogaster , 1980, Journal of comparative physiology.

[20]  S. Wada,et al.  Spezielle randzonale ommatidien der fliegen (diptera : brachycera): architektur und verteilung in den komplexauaen , 1974, Zeitschrift für Morphologie der Tiere.

[21]  K. Fischbach,et al.  The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure , 1989, Cell and Tissue Research.

[22]  R. Wehner,et al.  Does interocular transfer occur in visual navigation by ants? , 1985, Nature.

[23]  M. Dambach,et al.  Giant rhabdomes in a specialized region of the compound eye of a cricket: Cycloptiloides canariensis (Insecta, Gryllidae) , 1983, Zoomorphology.

[24]  N. Franceschini,et al.  Les phénomènes de pseudopupille dans l'œil composé deDrosophila , 1971, Kybernetik.

[25]  Rüdiger Wehner,et al.  The POL area of the honey bee's eye: behavioural evidence , 1985 .

[26]  S. Wada Ein spezieller Rhabdomerentyp im Fliegenauge , 1971, Experientia.

[27]  Jaroslav Král,et al.  A note on grammars with regular restrictions , 1973, Kybernetika.

[28]  S. Wada Spezielle randzonale ommatidien von Calliphora Erythrocephala meig. (diptera calliphoridae): Architektur der zentralen rhabdomeren-kolumne und topographie im komplexauge , 1974 .

[29]  G. Rubin,et al.  Analysis of the promoter of the ninaE opsin gene in Drosophila melanogaster. , 1987, Genetics.

[30]  D. Ready,et al.  Sevenless: A Cell-Specific Homeotic Mutation of the Drosophila Eye , 1986, Science.

[31]  N. Strausfeld,et al.  Optic lobe projections of marginal ommatidia in Calliphora erythrocephala specialized for detecting polarized light , 1985, Cell and Tissue Research.

[32]  J. L. Gould,et al.  Skylight Polarization patterns and Animal Orientation , 1982 .

[33]  K. Fischbach Neural cell types surviving congenital sensory deprivation in the optic lobes of Drosophila melanogaster. , 1983, Developmental biology.

[34]  S. Benzer,et al.  Development of the Drosophila retina, a neurocrystalline lattice. , 1976, Developmental biology.

[35]  M. Fingerman,et al.  The Orientation of Drosophila to Plane Polarized Light , 1953 .

[36]  K. Frisch,et al.  Die Polarisation des Himmelslichtes als orientierender Faktor bei den Tänzen der Bienen , 1949, Experientia.

[37]  Gertrud Kolb Retinal ultrastructure in the dorsal rim and large dorsal area of the eye of Aglais urticae (Lepidoptera) , 1986, Zoomorphology.

[38]  R. Wehner Himmelsnavigation bei Insekten : Neurophysiologie und Verhalten , 1982 .