Discrimination of visual motion from flicker by identified neurons in the medulla of the fleshfly Sarcophaga bullata

Summary1.Responses to moving contrast gratings and to flicker have been studied in cells in the medulla of the fleshfly Sarcophaga bullata using intracellular recordings and stainings. Medullary neurons responded periodically to flicker. Those which primarily discriminated motion had periodic responses or DC shifts in membrane potentials or increased noise. Intrinsic neurons included a T1a cell which was directionally selective (DS) and specific non-DS amacrine cells (6 types) arborizing either distal or proximal to the serpentine layer. Among the 12 types of output neurons recorded, 1 projected to the lobula plate, 6 to the lobula (Tm and T2 cells), 3 to both the lobula and lobula plate (Y cells), and 2 to the central brain.2.Irrespective of their projection, medulla neurons which arborize in the stratum of the L2 terminals respond to flicker as does L2 and have the simplest, primarily periodic, responses to motion. The responses have significant power at the second harmonic of the stimulus temporal frequency suggesting that a non-linear operation, such as multiplication, may occur in the L2 stratum. Cells with arbors coinciding with either of the two levels of L1 terminals have much more complex responses to motion. All cells projecting to the lobula plate responded periodically to movement in some direction(s).

[1]  G. Horridge The Compound eye and vision of insects , 1975 .

[2]  Matti Järvilehto,et al.  Lateral inhibition in an insect eye , 1972, Zeitschrift für vergleichende Physiologie.

[3]  S. R. Shaw,et al.  The Retina-Lamina Pathway in Insects, Particularly Diptera, Viewed from an Evolutionary Perspective , 1989 .

[4]  B. Hilbush,et al.  Lucifer yellow uptake in developing rat retina: selective staining of horizontal cells. , 1983, Brain research.

[5]  W. W. Stewart,et al.  Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer , 1978, Cell.

[6]  K. Hausen The Lobula-Complex of the Fly: Structure, Function and Significance in Visual Behaviour , 1984 .

[7]  L. N. Thibos,et al.  Vision beyond the resolution limit: Aliasing in the periphery , 1987, Vision Research.

[8]  N. Strausfeld,et al.  Cobalt-coupled neurons of a giant fibre system in Diptera , 1983, Journal of neurocytology.

[9]  Simon B. Laughlin,et al.  The Roles of Parallel Channels in Early Visual Processing by the Arthropod Compound Eye , 1984 .

[10]  Accepted June,et al.  Are the large monopolar cells of the insect lamina on the optomotor pathway , 1989 .

[11]  A. Borst,et al.  Transient and steady-state response properties of movement detectors. , 1989, Journal of the Optical Society of America. A, Optics and image science.

[12]  I. Bülthoff Deoxyglucose mapping of nervous activity induced in Drosophila brain by visual movement. 3. Outer rhabdomeres absent JK84, small optics lobes KS58 and no object fixation EB12, visual mutants. , 1986 .

[13]  K. Hausen Motion sensitive interneurons in the optomotor system of the fly , 1982, Biological Cybernetics.

[14]  N. Strausfeld Atlas of an Insect Brain , 1976, Springer Berlin Heidelberg.

[15]  F. Zettler,et al.  Electrophysiological-histological studies on some functional properties of visual cells and second order neurons of an insect retina , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[16]  A. Spurr A low-viscosity epoxy resin embedding medium for electron microscopy. , 1969, Journal of ultrastructure research.

[17]  H. Hartley,et al.  Tests of significance in harmonic analysis. , 1949, Biometrika.

[18]  S. Shaw Early visual processing in insects. , 1984, The Journal of experimental biology.

[19]  N. Franceschini,et al.  Motion detection in flies: Parametric control over ON-OFF pathways , 2004, Experimental Brain Research.

[20]  Alexander Borst,et al.  The role of GABA in detecting visual motion , 1990, Brain Research.

[21]  N. Strausfeld,et al.  Synaptic connections of intrinsic cells and basket arborizations in the external plexiform layer of the fly's eye. , 1973, Brain research.

[22]  Daniel Osorio,et al.  Mechanisms for Neural Signal Enhancement in the Blowfly Compound Eye , 1989 .

[23]  Isabelle Bülthoff,et al.  Deoxyglucose mapping of nervous activity induced inDrosophila brain by visual movement , 2004, Journal of Comparative Physiology A.

[24]  K. M. Kelly,et al.  Electrophysiology and anatomy of medulla interneurons in the optic lobe of the cockroach, Periplaneta americana , 1990, Journal of Comparative Physiology A.

[25]  K. Kirschfeld The visual system of Musca: Studies on optics, structure and function , 1972 .

[26]  A. S. French,et al.  The transmission of information by first and second order neurons in the fly visual system , 1978, Journal of Comparative Physiology.

[27]  I. Bülthoff Deoxyglucose mapping of nervous activity induced in Drosophila brain by visual movement. 2. Optomotor blind H31 and lobula plate-less N684 visual mutants. , 1985 .

[28]  K. Mimura Neural mechanisms, subserving directional selectivity of movement in the optic lobe of the fly , 1972, Journal of comparative physiology.

[29]  M. F. Land,et al.  Maps of the acute zones of fly eyes , 1985, Journal of Comparative Physiology A.

[30]  P. Detwiler,et al.  Selective uptake of lucifer yellow by bipolar cells in the turtle retina , 1981, Neuroscience Letters.

[31]  R. Hardie Functional Organization of the Fly Retina , 1985 .

[32]  Daniel Osorio,et al.  Matched filtering in the visual system of the fly : large monopolar cells of the lamina are optimized to detect moving edges and blobs , 1990, Proceedings of the Royal Society of London. B. Biological Sciences.

[33]  M Wilcox,et al.  Illumination induces dye incorporation in photoreceptor cells. , 1984, Science.

[34]  Robert D. DeVoe,et al.  Movement sensitivities of cells in the fly's medulla , 1980, Journal of comparative physiology.

[35]  Robert D. DeVoe,et al.  Intracellular responses from cells of the medulla of the fly, Calliphora erythrocephala , 1976, Biological Cybernetics.

[36]  Nicolas Franceschini,et al.  Sampling of the Visual Environment by the Compound Eye of the Fly: Fundamentals and Applications , 1975 .

[37]  R. G. Guy,et al.  Are the large monopolar cells of the insect lamina on the optomotor pathway? , 2004, Journal of Comparative Physiology A.

[38]  K. Hausen,et al.  The synaptic organization of visual interneurons in the lobula complex of flies , 1980, Cell and Tissue Research.

[39]  Cole Gilbert,et al.  Membrane Conductance Changes Associated with the Response of Motion Sensitive Insect Visual Neurons , 1990, Zeitschrift fur Naturforschung. C, Journal of biosciences.

[40]  J. Brockes Synaptic connections , 1977, Nature.

[41]  A. Dubs The spatial integration of signals in the retina and lamina of the fly compound eye under different conditions of luminance , 1982, Journal of comparative physiology.

[42]  Isabelle Bülthoff,et al.  Deoxyglucose mapping of nervous activity induced inDrosophila brain by visual movement , 1984, Journal of Comparative Physiology A.

[43]  E. Buchner Elementary movement detectors in an insect visual system , 1976, Biological Cybernetics.

[44]  W. Reichardt,et al.  Computational structure of a biological motion-detection system as revealed by local detector analysis in the fly's nervous system. , 1989, Journal of the Optical Society of America. A, Optics and image science.

[45]  N. Franceschini,et al.  Early processing of colour and motion in a mosaic visual system. , 1985, Neuroscience research. Supplement : the official journal of the Japan Neuroscience Society.

[46]  S B Laughlin,et al.  Single photon signals in fly photoreceptors and first order interneurones at behavioral threshold. , 1981, The Journal of physiology.

[47]  Christian Wehrhahn,et al.  Visual guidance of flies during flight , 1985 .

[48]  K. Mimura Movement discrimination by the visual system of flies , 1971, Zeitschrift für vergleichende Physiologie.

[49]  N. Strausfeld,et al.  The optic lobes of Lepidoptera. , 1970, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[51]  N. J. Strausfeld,et al.  Functional Neuroanatomy of the Blowfly’s Visual System , 1984 .

[52]  Alexa Riehle,et al.  Directionally Selective Motion Detection by Insect Neurons , 1989 .

[53]  N. Strausfeld,et al.  Columns and Layers in the Second Synaptic Region of the Fly’s Visual System: The Case for Two Superimposed Neuronal Architectures , 1972 .

[54]  D. Osorio,et al.  Directionally selective cells in the locust medulla , 1986, Journal of Comparative Physiology A.

[55]  P. L. Carras,et al.  Not by Ganglion Cells Alone: Directional Selectivity is Widespread in Identified Cells of the Turtle Retina , 1989 .

[56]  Alexander Borst,et al.  Principles of visual motion detection , 1989, Trends in Neurosciences.