GABAergic Lateral Interactions Tune the Early Stages of Visual Processing in Drosophila

Neuron

Volumn 78, Issue 6, 2013, Pages 1075-1089

  Freifeld, Limor ^a   Clark, DamonA ^b,c   Schnitzer, MarkJ ^b   Horowitz, MarkA ^a   Clandinin, ThomasR ^b  

^a Stanford University   (United States)

^b STANFORD UNIVERSITY   (United States)

^c YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; CALCIUM ION;

ANIMAL EXPERIMENT; ANISOTROPY; ARTICLE; CONTRAST SENSITIVITY; CONTROLLED STUDY; DROSOPHILA; EVOKED VISUAL RESPONSE; FUNCTIONAL ANATOMY; GABAERGIC SYSTEM; IN VIVO STUDY; INTERNEURON; MOLECULAR IMAGING; NERVE CELL NETWORK; NERVE ENDING; NERVE FUNCTION; NEUROANATOMY; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RECEPTIVE FIELD; SIGNAL TRANSDUCTION; VISION; VISUAL ACUITY;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA; GABAERGIC NEURONS; GENE KNOCKDOWN TECHNIQUES; MOTION PERCEPTION; PHOTIC STIMULATION; VISUAL CORTEX; VISUAL FIELDS; VISUAL PATHWAYS;

EID: 84879250538     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.04.024     Document Type: Article

References (94)

1. Arnett D.W. Spatial and temporal integration properties of units in first optic ganglion of dipterans. J.Neurophysiol. 1972, 35:429-444.
2. Atick J.J. Could information theory provide an ecological theory of sensory processing?. Network 1992, 3:213-251.
3. Baccus S.A., Ölveczky B.P., Manu M., Meister M. A retinal circuit that computes object motion. J.Neurosci. 2008, 28:6807-6817.
4. Barlow H. Possible principles underlying the transformations of sensory messages. Sensory Communication 1961, 217-234. MIT Press, Cambridge. W.A. Rosenblith (Ed.).
5. Barlow R.B. Inhibitory fields in the Limulus lateral eye. J.Gen. Physiol. 1969, 54:383-396.
6. Baylor D.A., Fuortes M.G.F., O'Bryan P.M. Receptive fields of cones in the retina of the turtle. J.Physiol. 1971, 214:265-294.
7. Blagburn J.M., Sattelle D.B. Presynaptic depolarization mediates presynaptic inhibition at a synapse between an identified mechanosensory neurone and giant interneurone 3 in the first instar cockroach, periplaneta americana. J.Exp. Biol. 1987, 127:135-157.
8. Borst A., Reisenman C., Haag J. Adaptation of response transients in fly motion vision. II: Model studies. Vision Res. 2003, 43:1309-1322.
9. Borst A., Haag J., Reiff D.F. Fly motion vision. Annu. Rev. Neurosci. 2010, 33:49-70.
10. Brumberg J.C., Pinto D.J., Simons D.J. Spatial gradients and inhibitory summation in the rat whisker barrel system. J.Neurophysiol. 1996, 76:130-140.
11. Buchner E., Bader R., Buchner S., Cox J., Emson P.C., Flory E., Heizmann C.W., Hemm S., Hofbauer A., Oertel W.H. Cell-specific immuno-probes for the brain of normal and mutant Drosophila melanogaster. I. Wildtype visual system. Cell Tissue Res. 1988, 253:357-370.
12. Burrows M., Matheson T. A presynaptic gain control mechanism among sensory neurons of a locust leg proprioceptor. J.Neurosci. 1994, 14:272-282.
13. Cajal S.R., Sanchez D. Contribucion al conocimiento de los centros nerviosos del los insectos. Trab. Lab. Invest. Biol. 1915, 13:1-168.
14. Clandinin T.R., Zipursky S.L. Making connections in the fly visual system. Neuron 2002, 35:827-841.
15. Clark D.A., Bursztyn L., Horowitz M.A., Schnitzer M.J., Clandinin T.R. Defining the computational structure of the motion detector in Drosophila. Neuron 2011, 70:1165-1177.
16. Cleland T.A. Inhibitory glutamate receptor channels. Mol. Neurobiol. 1996, 13:97-136.
17. Dacey D., Packer O.S., Diller L., Brainard D., Peterson B., Lee B. Center surround receptive field structure of cone bipolar cells in primate retina. Vision Res. 2000, 40:1801-1811.
18. Davis G.W., Naka K.-I. Spatial organization of catfish retinal neurons. I. Single- and random-bar stimulation. J.Neurophysiol. 1980, 43:807-831.
19. DeVries S.H. Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 2000, 28:847-856.
20. C feedback at bipolar terminals in the tiger salamander retina. J.Neurophysiol. 1998, 79:2171-2180.
21. Dubs A. The spatial integration of signals in the retina and lamina of the fly compound eye under different conditions of luminance. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1982, 146:321-343.
22. Dubs A., Laughlin S.B., Srinivasan M.V. Single photon signals in fly photoreceptors and first order interneurones at behavioral threshold. J.Physiol. 1981, 317:317-334.
23. Egelhaaf M., Borst A. Transient and steady-state response properties of movement detectors. J.Opt. Soc. Am. A 1989, 6:116-127.
24. Egelhaaf M., Borst A. Are there separate ON and OFF channels in fly motion vision?. Vis. Neurosci. 1992, 8:151-164.
25. Eichner H., Joesch M., Schnell B., Reiff D.F., Borst A. Internal structure of the fly elementary motion detector. Neuron 2011, 70:1155-1164.
26. Enell L., Hamasaka Y., Kolodziejczyk A., Nässel D.R. γ-Aminobutyric acid (GABA) signaling components in Drosophila: immunocytochemical localization of GABA(B) receptors in relation to the GABA(A) receptor subunit RDL and a vesicular GABA transporter. J.Comp. Neurol. 2007, 505:18-31.
27. Enroth-Cugell C., Freeman A.W. The receptive-field spatial structure of cat retinal Y cells. J.Physiol. 1987, 384:49-79.
28. Euler T., Masland R.H. Light-evoked responses of bipolar cells in a mammalian retina. J.Neurophysiol. 2000, 83:1817-1829.
29. Fahey P.K., Burkhardt D.A. Center-surround organization in bipolar cells: symmetry for opposing contrasts. Vis. Neurosci. 2003, 20:1-10.
30. Fleet D.J., Jepson A.D. Spatiotemporal inseparability in early vision: centre-surround models and velocity selectivity. Comput. Intell. 1985, 1:89-102.
31. Fleet D.J., Hallett P.E., Jepson A.D. Spatiotemporal inseparability in early visual processing. Biol. Cybern. 1985, 52:153-164.
32. Glantz R.M., Bartels A. The spatiotemporal transfer function of crayfish lamina monopolar neurons. J.Neurophysiol. 1994, 71:2168-2182.
33. Gollisch T., Meister M. Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 2010, 65:150-164.
34. Hardie R.C. Is histamine a neurotransmitter in insect photoreceptors?. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1987, 161:201-213.
35. Hardie R.C. A histamine-activated chloride channel involved in neurotransmission at a photoreceptor synapse. Nature 1989, 339:704-706.
36. Hartline H.K., Wagner H.G., Ratliff F. Inhibition in the eye of Limulus. J.Gen. Physiol. 1956, 39:651-673.
37. Hassenstein B., Reichardt W. Systemtheoretische analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der bewegungsperzeption des rüsselkäfers Chlorophanus. Z.Naturforsch. B 1956, 11b:513-524.
38. Järvilehto M., Zettler F. Electrophysiological-histological studies on some functional properties of visual cells and second order neurons of an insect retina. Z.Zellforsch. Mikrosk. Anat.Mikrosk Anat. 1973, 136:291-306.
39. Joesch M., Schnell B., Raghu S.V., Reiff D.F., Borst A. ON and OFF pathways in Drosophila motion vision. Nature 2010, 468:300-304.
40. Johnston D., Wachtel H. Electrophysiological basis for the spatialdependence of the inhibitory coupling in the Limulus retina. J.Gen. Physiol. 1976, 67:1-25.
41. Juusola M., French A.S. Visual acuity for moving objects in first- and second-order neurons of the fly compound eye. J.Neurophysiol. 1997, 77:1487-1495.
42. Juusola M., Weckström M., Uusitalo R.O., Korenberg M.J., French A.S. Nonlinear models of the first synapse in the light-adapted fly retina. J.Neurophysiol. 1995, 74:2538-2547.
43. Kaneko A. Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina. J.Physiol. 1970, 207:623-633.
44. Kaneko A., Tachibana M. Effects of γ-aminobutyric acid on isolated cone photoreceptors of the turtle retina. J.Physiol. 1986, 373:443-461.
45. Kennedy D., Calabrese R.L., Wine J.J. Presynaptic inhibition: primary afferent depolarization in crayfish neurons. Science 1974, 186:451-454.
46. Knudsen E.I., Konishi M. Center-surround organization of auditory receptive fields in the owl. Science 1978, 202:778-780.
47. Kolodziejczyk A., Sun X., Meinertzhagen I.A., Nässel D.R. Glutamate, GABA and acetylcholine signaling components in the lamina of the Drosophila visual system. PLoS ONE 2008, 3:e2110.
48. Laughlin S.B. Neural integration in the first optic neuropile of dragonflies. II. Receptor signal interactions in the lamina. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1974, 92:357-375.
49. Laughlin S.B. Neural integration in the first optic neuropile of dragonflies. III. The transfer of angular information. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1974, 92:377-396.
50. Laughlin S.B. A simple coding procedure enhances a neuron's information capacity. Z.Naturforsch., C, Biosci. 1981, 36:910-912.
51. Laughlin S.B. Matching coding, circuits, cells, and molecules to signals: general principles of retinal design in the fly's eye. Prog. Retin. Eye Res. 1994, 13:165-196.
52. Laughlin S.B., Hardie R.C. Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1978, 128:319-340.
53. Laughlin S.B., Osorio D. Mechanisms for neural signal enhancement in the blowfly compound eye. J.Exp. Biol. 1989, 144:113-146.
54. Laughlin S.B., Howard J., Blakeslee B. Synaptic limitations to contrast coding in the retina of the blowfly Calliphora. Proc. R. Soc. Lond. B Biol. Sci. 1987, 231:437-467.
55. Liu X., Krause W.C., Davis R.L. GABAA receptor RDL inhibits Drosophila olfactory associative learning. Neuron 2007, 56:1090-1102.
56. Mank M., Santos A.F., Direnberger S., Mrsic-Flogel T.D., Hofer S.B., Stein V., Hendel T., Reiff D.F., Levelt C., Borst A., et al. A genetically encoded calcium indicator for chronic invivo two-photon imaging. Nat. Methods 2008, 5:805-811.
57. Masland R.H. The fundamental plan of the retina. Nat. Neurosci. 2001, 4:877-886.
58. Masu M., Iwakabe H., Tagawa Y., Miyoshi T., Yamashita M., Fukuda Y., Sasaki H., Hiroi K., Nakamura Y., Shigemoto R., et al. Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell 1995, 80:757-765.
59. Meinertzhagen I.A., O'Neil S.D. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J.Comp. Neurol. 1991, 305:232-263.
60. Mimura K. Some spatial properties in the first optic ganglion of the fly. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1976, 105:65-82.
61. Molnar A., Werblin F.S. Inhibitory feedback shapes bipolar cell responses in the rabbit retina. J.Neurophysiol. 2007, 98:3423-3435.
62. Nakanishi S., Nakajima Y., Masu M., Ueda Y., Nakahara K., Watanabe D., Yamaguchi S., Kawabata S., Okada M. Glutamate receptors: brain function and signal transduction. Brain Res. Brain Res. Rev. 1998, 26:230-235.
63. Olsen S.R., Wilson R.I. Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 2008, 452:956-960.
64. Olshausen B.A., Field D.J. Natural image statistics and efficient coding. Network 1996, 7:333-339.
65. Owen W.G., Hare W.A. Signal transfer from photoreceptors to bipolar cells in the retina of the tiger salamander. Neurosci. Res. Suppl. 1989, 10:S77-S87.
66. Pitkow X., Meister M. Decorrelation and efficient coding by retinal ganglion cells. Nat. Neurosci. 2012, 15:628-635.
67. Ratliff F., Hartline H.K., Miller W.H. Spatial and temporal aspects of retinal inhibitory interaction. J.Opt. Soc. Am. 1963, 53:110-120.
68. Reiff D.F., Plett J., Mank M., Griesbeck O., Borst A. Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila. Nat. Neurosci. 2010, 13:973-978.
69. Richter J., Ullman S. A model for the temporal organization of X- and Y-type receptive fields in the primate retina. Biol. Cybern. 1982, 43:127-145.
70. Rister J., Pauls D., Schnell B., Ting C.-Y., Lee C.-H., Sinakevitch I., Morante J., Strausfeld N.J., Ito K., Heisenberg M. Dissection of the peripheral motion channel in the visual system of Drosophila melanogaster. Neuron 2007, 56:155-170.
71. Rivera-Alba M., Vitaladevuni S.N., Mishchenko Y., Lu Z., Takemura S.Y., Scheffer L., Meinertzhagen I.A., Chklovskii D.B., de Polavieja G.G. Wiring economy and volume exclusion determine neuronal placement in the Drosophila brain. Curr. Biol. 2011, 21:2000-2005.
72. Rodieck R.W. Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Res. 1965, 5:583-601.
73. Root C.M., Masuyama K., Green D.S., Enell L.E., Nässel D.R., Lee C.-H., Wang J.W. A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 2008, 59:311-321.
74. Sanes J.R., Zipursky S.L. Design principles of insect and vertebrate visual systems. Neuron 2010, 66:15-36.
75. Shapley R., Lennie P. Spatial frequency analysis in the visual system. Annu. Rev. Neurosci. 1985, 8:547-583.
76. Shaw S.R. Retinal resistance barriers and electrical lateral inhibition. Nature 1975, 255:480-482.
77. Shields C.R., Tran M.N., Wong R.O., Lukasiewicz P.D. Distinct ionotropic GABA receptors mediate presynaptic and postsynaptic inhibition in retinal bipolar cells. J.Neurosci. 2000, 20:2673-2682.
78. Srinivasan M.V. Generalized gradient schemes for the measurement of two-dimensional image motion. Biol. Cybern. 1990, 63:421-431.
79. Srinivasan M.V., Dvorak D.R. Spatial processing of visual information in the movement-detecting pathway of the fly. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1980, 140:1-23.
80. Srinivasan M.V., Laughlin S.B., Dubs A. Predictive coding: a freshview of inhibition in the retina. Proc. R. Soc. Lond. B Biol. Sci. 1982, 216:427-459.
81. Srinivasan M.V., Pinter R.B., Osorio D. Matched filtering in thevisual system of the fly: large monopolar cells of the lamina are optimized to detect moving edges and blobs. Proc. R. Soc. Lond. B Biol. Sci. 1990, 240:279-293.
82. Stavenga D.G. Angular and spectral sensitivity of fly photoreceptors. II. Dependence on facet lens F-number and rhabdomere type in Drosophila. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2003, 189:189-202.
83. Tammero L.F., Frye M.A., Dickinson M.H. Spatial organization of visuomotor reflexes in Drosophila. J.Exp. Biol. 2004, 207:113-122.
84. Thoreson W.B., Mangel S.C. Lateral interactions in the outer retina. Prog. Retin. Eye Res. 2012, 31:407-441.
85. Toyoda J.-I., Fujimoto M. Analyses of neural mechanisms mediating the effect of horizontal cell polarization. Vision Res. 1983, 23:1143-1150.
86. van Hateren J.H. Theoretical predictions of spatiotemporal receptive fields of fly LMCs, and experimental validation. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1992, 171:157-170.
87. Vigh J., Vickers E., von Gersdorff H. Light-evoked lateral GABAergic inhibition at single bipolar cell synaptic terminals is driven by distinct retinal microcircuits. J.Neurosci. 2011, 31:15884-15893.
88. Weber F., Machens C.K., Borst A. Spatiotemporal response properties of optic-flow processing neurons. Neuron 2010, 67:629-642.
89. Weckström M., Laughlin S. Extracellular potentials modify the transfer of information at photoreceptor output synapses in the blowfly compound eye. J.Neurosci. 2010, 30:9557-9566.
90. Weckström M., Kouvalainen E., Djupsund K., Järvilehto M. More than one type of conductance is activated during responses of Blowfly monopolar neurones. J.Exp. Biol. 1989, 144:147-154.
91. Werblin F.S., Dowling J.E. Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J.Neurophysiol. 1969, 32:339-355.
92. Wilson R.I., Laurent G. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J.Neurosci. 2005, 25:9069-9079.
93. Zanker J.M., Srinivasan M.V., Egelhaaf M. Speed tuning in elementary motion detectors of the correlation type. Biol. Cybern. 1999, 80:109-116.
94. Zhang A.J., Wu S.M. Receptive fields of retinal bipolar cells are mediated by heterogeneous synaptic circuitry. J.Neurosci. 2009, 29:789-797.