Activity labeling patterns in the medulla of Drosophila melanogaster caused by motion stimuli

SummaryWe quantitatively describe 2-deoxyglucose (2-DG) neuronal activity labeling patterns in the first and second visual neuropil regions of the Drosophila brain, the lamina and the medulla. Careful evaluation of activity patterns resulting from large-field motion stimulation shows that the stimulus-specific bands in the medulla correspond well to the layers found in a quantitative analysis of Golgi-impregnated columnar neurons. A systematic analysis of autoradiograms of different intensities reveals a hierarchy of labeling in the medulla. Under certain conditions, only neurons of the lamina are labeled. Their characteristic terminals in the medulla are used to differentiate among the involved lamina monopolar cell types. The 2-DG banding pattern in the medulla marks layers M1 and M5, the input layers of pathway p1 (the L1 pathway). Therefore, activity labeling of L1 by motion stimuli is very likely. More heavily labeled autoradiograms display activated cells also in layers M2, M9, and M10. The circuitry involved in the processing of motion information thus concentrates on pathways p1 and p2. Layers M4 and M6 of the distal medulla hardly display any label under the stimulus conditions used. The functional significance of selective activity in the medulla is discussed.

[1]  V. Braitenberg,et al.  Patterns of projection in the visual system of the fly II. Quantitative aspects of second order neurons in relation to models of movement perception , 2004, Experimental Brain Research.

[2]  Santiago Ramón y Cajal,et al.  Contribución al conocimiento de los centros nerviosos de los insectos , 1915 .

[3]  W. Oertel,et al.  Cell-specific immuno-probes for the brain of normal and mutant Drosophila melanogaster , 1988, Cell and Tissue Research.

[4]  M. Egelhaaf.  On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly , 1985 .

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

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

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

[8]  Nicholas J. Strausfeld,et al.  Beneath the Compound Eye: Neuroanatomical Analysis and Physiological Correlates in the Study of Insect Vision , 1989 .

[9]  V. Braitenberg.  Periodic structures and structural gradients in the visual ganglia of the fly , 1972 .

[10]  N. Strausfeld.  Mosaic Organizations, Layers, and Visual Pathways in the Insect Brain , 1976 .

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

[12]  N. Strausfeld,et al.  Neuronal basis for parallel visual processing in the fly , 1991, Visual Neuroscience.

[13]  R. Hengstenberg,et al.  2-Deoxy-D-glucose maps movement-specific nervous activity in the second visual ganglion of Drosophila. , 1979, Science.

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

[15]  N. Strausfeld.  The optic lobes of Diptera. , 1970, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[16]  Werner Reichardt,et al.  Processing of optical information by the visual system of the fly , 1986, Vision Research.

[17]  E. Buchner,et al.  Mapping stimulus-induced nervous activity in small brains by [3H]2-deoxy-D-glucose , 2004, Cell and Tissue Research.

[18]  Simon B. Laughlin,et al.  Coding Efficiency and Design in Visual Processing , 1989 .

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

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

[21]  M. Heisenberg,et al.  Genetic Dissection of Optomotor Behavior in Droso- phila melanogaster Studies on Wild-Type and the , 1986 .

[22]  I. Meinertzhagen,et al.  Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster , 1991, The Journal of comparative neurology.

[23]  S. Laughlin,et al.  Early Visual Processing in the Compound Eye: Physiology and Pharmacology of the Retina-Lamina Projection in the Fly , 1989 .

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

[25]  E. Buchner,et al.  Identification of [3H]deoxyglucose-labelled interneurons in the fly from serial autoradiographs , 1984, Brain Research.

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

[27]  M. Egelhaaf.  On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly , 1985 .

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

[29]  N. Strausfeld.  Insect Vision and Olfaction: Common Design Principles of Neuronal Organization , 1989 .

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

[31]  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 .

[32]  E. Buchner,et al.  Anatomical Localization of Functional Activity in Flies Using 3H-2-Deoxy-d-Glucose , 1983 .

[33]  M. Heisenberg,et al.  Identification of H1 visual interneuron in Drosophila by [3H]2-deoxyglucose uptake during stationary flight , 1990, Brain Research.

[34]  K G Götz,et al.  Principles of optomotor reactions in insects. , 1972, Bibliotheca ophthalmologica : supplementa ad ophthalmologica.

[35]  Cole Gilbert,et al.  Discrimination of visual motion from flicker by identified neurons in the medulla of the fleshfly Sarcophaga bullata , 1991, Journal of Comparative Physiology A.

[36]  M. Tsacopoulos,et al.  Honeybee retinal glial cells transform glucose and supply the neurons with metabolic substrate. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[37]  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 .