Deoxyglucose mapping of nervous activity induced inDrosophila brain by visual movement

SummaryLocal metabolic activity was mapped in the brain ofDrosophila by the radioactive deoxyglucose technique. The distribution of label in serial autoradiographs allows us to draw the following conclusions concerning neuronal processing of visual movement information in the brain ofDrosophila.1.The visual stimuli used (homogeneous flicker, moving gratings, reversing contrast gratings) cause only a small increase in metabolic activity in the first visual neuropil (lamina).2.In the second visual neuropil (medulla) at least four layers respond to visual movement and reversing contrast gratings by increased metabolic activity; homogeneous flicker is less effective.3.With the current autoradiographic resolution (2—3 μm) no directional selectivity can be detected in the medulla.4.In the lobula, the anterior neuromere of the third visual neuropil, movement-specific activity is observed in three layers, two of which are more strongly labelled by ipsilateral front-to-back than by back-to-front movement.5.In its posterior counterpart, the lobula plate, four movement-sensitive layers can be identified in which label accumulation specifically depends on the direction of the movement: Ipsilateral front-to-back movement labels a superficial anterior layer, back-to-front movement labels an inner anterior layer, upward movement labels an inner posterior layer and downward movement labels a superficial posterior layer.6.A considerable portion of the stimulus-enhanced labelling of medulla and lobula complex is restricted to those columns which connect to the stimulated ommatidia. This retinotopic distribution of label suggests the involvement of movement-sensitive small-field neurons.7.Certain axonal profiles connecting the lobula plate and the lateral posterior protocerebrum are labelled by ipsilateral front-to-back movement. Presumably different structures in the same region are labelled by ipsilateral downward movement. Conspicuously labelled foci and commissures in the central brain cannot yet be associated with a particular stimulus. The results are discussed in the light of present anatomical and physiological knowledge of the visual movement detection system of flies.

[1]  W Reichardt,et al.  Visual control of orientation behaviour in the fly: Part I. A quantitative analysis , 1976, Quarterly Reviews of Biophysics.

[2]  K. Fischbach,et al.  Cell degeneration in the developing optic lobes of the sine oculis and small-optic-lobes mutants of Drosophila melanogaster. , 1984, Developmental biology.

[3]  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.

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

[5]  A. Gelperin,et al.  Localization of [3H]-2-deoxy glucose in single molluscan neurones , 1980, Nature.

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

[7]  K. R. Hengstenberg The Number and Structure of Giant Vertical Cells (VS) in the Lobula Plate of the Blowfly , 2022 .

[8]  The effect of light on glycogen turnover in the retina of the intact honeybee drone (Apis mellifera) , 1983, Journal of comparative physiology.

[9]  M. Srinivasan,et al.  Spatial processing of visual information in the movement-detecting pathway of the fly , 2004, Journal of comparative physiology.

[10]  R. Wolf,et al.  Optomotor-blindH31—aDrosophila mutant of the lobula plate giant neurons , 1978, Journal of comparative physiology.

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

[12]  R. Hengstenberg The Effect of Pattern Movement on the Impulse Activity of the Cervical Connective of Drosophila melanogaster , 1973, Zeitschrift fur Naturforschung. Teil C: Biochemie, Biophysik, Biologie, Virologie.

[13]  H. Bülthoff,et al.  Analogous motion illusion in man and fly , 1979, Nature.

[14]  P. Coombe The role of retinula cell types in fixation behaviour of walkingDrosophila melanogaster , 1984, Journal of Comparative Physiology A.

[15]  T. Nagatsu,et al.  Demonstration of aromatic l-amino acid decarboxylase activity in human brain with l-dopa and l-5-hydroxytryptophan as substrates by high-performance liquid chromatography with electrochemical detection , 1982, Neurochemistry International.

[16]  Christian Wehrhahn,et al.  How is tracking and fixation accomplished in the nervous system of the fly? , 1980, Biological Cybernetics.

[17]  Erich Buchner,et al.  Evidence for one-way movement detection in the visual system of Drosophila , 1978, Biological Cybernetics.

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

[19]  M Heisenberg,et al.  Structural brain mutant of Drosophila melanogaster with reduced cell number in the medulla cortex and with normal optomotor yaw response. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[20]  W J Schwartz,et al.  Metabolic mapping of functional activity in the hypothalamo-neurohypophysial system of the rat. , 1979, Science.

[21]  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 .

[22]  I. Bülthoff,et al.  Freeze-substitution of Drosophila heads for subsequent [3H]2-deoxyglucose autoradiography , 1985, Journal of Neuroscience Methods.

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

[24]  H. Bülthoff Drosophila mutants disturbed in visual orientation , 1982, Biological Cybernetics.

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

[26]  Martin Heisenberg,et al.  The three-dimensional optomotor torque system ofDrosophila melanogaster , 1982, Journal of comparative physiology.

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

[28]  J. C. Hall,et al.  Genetics of the nervous system in Drosophila , 1982, Quarterly Reviews of Biophysics.

[29]  Heinrich H. Bülthoff,et al.  Three-Dimensional Reconstruction and Stereoscopic Display of Neurons in the Fly Visual System , 1983 .

[30]  T. Woolsey,et al.  Cellular localization of 2-[3H]deoxy-D-glucose from paraffin-embedded brains , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[32]  R. Hengstenberg Common visual response properties of giant vertical cells in the lobula plate of the blowflyCalliphora , 1982, Journal of comparative physiology.

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

[34]  Martin Heisenberg,et al.  The rôle of retinula cell types in visual behavior ofDrosophila melanogaster , 2004, Journal of comparative physiology.

[35]  T. Poggio,et al.  A synaptic mechanism possibly underlying directional selectivity to motion , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

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

[37]  Karl Georg Götz,et al.  Visual control of locomotion in the walking fruitflyDrosophila , 1973, Journal of comparative physiology.

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

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

[40]  R. Greenspan,et al.  Genetic analysis of Drosophila neurobiology. , 1979, Annual review of genetics.

[41]  M. Heisenberg,et al.  The use of mutations for the partial degradation of vision inDrosophila melanogaster , 1975, Journal of comparative physiology.

[42]  Erich Buchner,et al.  Behavioural Analysis of Spatial Vision in Insects , 1984 .

[43]  M. Heisenberg,et al.  Isolation of Anatomical Brain Mutants of Drosophila by Histological Means , 1979 .

[44]  Werner Reichardt,et al.  Musterinduzierte Flugorientierung , 1973, Naturwissenschaften.

[45]  H. Bülthoff,et al.  Recurrent inversion of visual orientation in the walking fly,Drosophila melanogaster , 1982, Journal of comparative physiology.

[46]  M. Reivich,et al.  THE [14C]DEOXYGLUCOSE METHOD FOR THE MEASUREMENT OF LOCAL CEREBRAL GLUCOSE UTILIZATION: THEORY, PROCEDURE, AND NORMAL VALUES IN THE CONSCIOUS AND ANESTHETIZED ALBINO RAT 1 , 1977, Journal of neurochemistry.

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

[48]  W. G. Young,et al.  Effects of blood glucose levels on [14C]2-deoxyglucose uptake in rat brain tissue , 1980, Neuroscience Letters.

[49]  M. Heisenberg,et al.  Vision in Drosophila , 1984 .

[50]  R. P. Zimmerman Field potential analysis and the physiology of second-order neurons in the visual system of the fly , 1978, Journal of comparative physiology.

[51]  G. Wegener Comparative Aspects of Energy Metabolism in Nonmammalian Brains Under Normoxic and Hypoxic Conditions , 1981 .

[52]  L. Sokoloff The Radioactive Deoxyglucose Method , 1982 .

[53]  Heinrich Bülthoff,et al.  Drosophila mutants disturbed in visual orientation , 1982, Biological Cybernetics.

[54]  W Reichardt,et al.  Visual control of orientation behaviour in the fly: Part II. Towards the underlying neural interactions , 1976, Quarterly Reviews of Biophysics.