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Are there separate ON and OFF channels in fly motion vision?

Published online by Cambridge University Press:  02 June 2009

Martin Egelhaaf
Affiliation:
Max-Planck-Institut für biologische Kybernetik, Spemannstrasse 38, D-7400 Tübingen, Germany
Alexander Borst
Affiliation:
Max-Planck-Institut für biologische Kybernetik, Spemannstrasse 38, D-7400 Tübingen, Germany

Abstract

Visual information is processed in a series of subsequent steps. The performance of each of these steps depends not only on the computations it performs itself but also on the representation of the visual surround on which it operates. Here we investigate the consequences of signal preprocessing for the performance of the motion-detection system of the fly. In particular, we analyze whether the retinal input signals are rectified and segregate into separate ON and OFF channels, which then feed independent parallel motion-detection pathways. We recorded the activity of an identified directionally selective interneuron (HI-cell) in response to apparent motion stimuli, i.e. sequential brightness changes at two neighboring locations in the visual field, as well as to brightness changes at only a single location. For apparent motion stimuli, the motion-dependent response component was determined by subtracting from the overall response the responses to the individual stimulus components when presented alone. The following conclusions could be derived: (1) Apparent motion consisting of a sequence of increased or decreased brightness at two locations in the visual field have the same optimum interstimulus time interval (Fig. 3). (2) Sequences of brightness steps of like polarity (either increments or decrements) elicit positive and negative motion-dependent response components when mimicking motion in the cell's preferred and null direction, respectively. The motion-dependent response components are inverted in sign when the brightness steps of a stimulus sequence have a different polarity (Fig. 7). (3) The responses to the beginning and the end of a brightness pulse depend on the pulse duration. For pulse durations of less than 2 s, both events interact with each other (Fig. 9). All of these results do not provide any indication that the fly processes motion information in independent ON and OFF motion detectors. Brightness changes of both signs are rather represented at the input of the same movement detectors, and interactions between signals resulting from both brightness increments and decrements take their sign into account. This type of preprocessing of the retinal input is argued to render a motion-detection system particularly robust against noise.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1992

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References

Anstis, S.M. (1970). Phi motion as a subtraction process. Vision Research 10, 14111430.CrossRefGoogle ScholarPubMed
Anstis, S.M. & Mather, G. (1985). Effects of luminance and contrast on direction of ambiguous apparent motion. Perception 14, 167179.CrossRefGoogle Scholar
Anstis, S.M. & Rogers, B.J. (1975). Illusory reversal of visual depth and movement during changes of contrast. Vision Research 15, 957961.CrossRefGoogle Scholar
Arnett, D.W. (1972). Spatial and temporal integration properties of units in first optic ganglion of dipterans. Journal of Neurophysiology 35, 429444.CrossRefGoogle ScholarPubMed
Borst, A. & Egelhaaf, M. (1987). Temporal modulation of luminance adapts time constant of fly movement detectors. Biological Cybernetics 56, 209215.CrossRefGoogle Scholar
Borst, A. & Egelhaaf, M. (1989). Principles of visual motion detection. Trends in Neuroscience 12, 297306.CrossRefGoogle ScholarPubMed
Borst, A. & Egelhaaf, M. (1990). Direction selectivity of fly motionsensitive neurons is computed in a two-stage process. Proceedings of the National Academy of Sciences of the U.S.A. 87, 93639367.CrossRefGoogle Scholar
Buchner, E. (1976). Elementary movement detectors in an insect visual system. Biological Cybernetics 24, 85101.CrossRefGoogle Scholar
Buchner, E. (1984). Behavioural analysis of spatial vision in insects. In Photoreception and Vision in Invertebrates, ed. Ali, M.A., pp.561621. New York, London: Plenum Press.CrossRefGoogle Scholar
Cavanagh, P. & Mather, G. (1989). Motion: The long and short of it. Spatial Vision 4, 103129.Google Scholar
Chaudhuri, A. & Albright, T.D. (1991). Perceptual and optokinetic responses to moving contrast-reversed patterns. Investigative Ophthalmology and Visual Science 32, 827.Google Scholar
Chubb, C. & Sperling, G. (1989). Two motion perception mechanisms revealed through distance-driven reversal of apparent motion. Proceedings of the National Academy of Sciences of the U.S.A. 68, 29852989.CrossRefGoogle Scholar
Coombe, P.E., Srinivasan, M.V. & Guy, R.G. (1989). Are the large monopolar cells of the insect lamina on the optomotor pathway? Journal of Comparative Physiology A 166, 2335.CrossRefGoogle Scholar
Devoe, R.D. (1985). The eye: Electrical activity. In Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 6 Nervous System: Sensory, ed. Kerkut, G.A. & Gilbert, L.I., pp. 277354. Oxford, New York: Pergamon Press.Google Scholar
Eckert, H. (1973). Optomotorische Untersuchungen am visuellen System der Stubenfliege Musca domestica L. Kybernetik 14, 123.CrossRefGoogle Scholar
Eckert, H. (1980). Functional properties of the Hl-neurone in the third optic ganglion of the blowfly, Phaenicia. Journal of Comparative Physiology 135, 2939.CrossRefGoogle Scholar
Egelhaaf, M. & Borst, A. (1989). Transient and steady-state response properties of movement detectors. Journal of the Optical Society of America A 6, 116127. Errata: Journal of the Optical Society of America A 7, 172.CrossRefGoogle ScholarPubMed
Egelhaaf, M., Borst, A. & Reichardt, W. (1989). The computational structure of a biological motion detection system. Journal of the Optical Society of America A 6, 10701087.CrossRefGoogle Scholar
Egelhaaf, M., Borst, A. & Pilz, B. (1990). The role of GABA in detecting visual motion. Brain Research 509, 156160.CrossRefGoogle ScholarPubMed
Egelhaaf, M. & Borst, A. (1990). Is motion detected by the fly visual system in separate Onand Off-channels? In Brain-PerceptionCognition, ed. Elsner, N. & Roth, G., pp. 209. Stuttgart, New York: Thieme.Google Scholar
Emerson, R.C., Citron, M.C., Vaughn, W.J. & Klein, S.A. (1987). Nonlinear directionally selective subunits in complex cells of cat striate cortex. Journal of Neurophysiology 58, 3365.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1983). On and off pathways through amacrine cells in mammalian retina: The synaptic connections of “starburst” amacrine cells. Vision Research 23, 12651279.CrossRefGoogle ScholarPubMed
Fiorentini, A., Baumgartner, G., Magnussen, S., Schiller, P.H. & Thomas, J.P. (1990). The perception of brightness and darkness: Relations to neuronal receptive fields. In Visual Perception. The Neurophysiological Foundations, ed. Spillman, L. & Werner, J.S., pp. 129161. New York: Academic Press.CrossRefGoogle Scholar
Franceschini, N., Monster, A. & Heurkens, G. (1979). Aquatoriales und binokulares Sehen bei der Fliege Calliphora erythrocephala. Verhandlungen der Deutschen Zoologischen Gesellschaft 1979, 209.Google Scholar
Franceschini, N., Riehle, A. & Le Nestour, A. (1989). Directionally selective motion detection by insect neurons. In Facets of Vision, ed. Stavenga, D.G. & Hardie, R.C., pp. 360390. Berlin, Heidelberg: Springer-Verlag.CrossRefGoogle Scholar
Götz, K.G. (1964). Optomotorische Untersuchungen des visuellen Systems einiger Augenmutanten der Fruchtfliege Drosophila. Kybernetik 2, 7792.CrossRefGoogle Scholar
Götz, K.G. (1965). Die optischen Uöbertragungseigenschaften der Komplexaugen von Drosophila. Kybernetik 2, 215221.CrossRefGoogle ScholarPubMed
Götz, K.G. (1972). Principles of optomotor reactions in insects. Bibliotheca Ophthalmologica 82, 251259.Google Scholar
Hassenstein, B. & Reichardt, W. (1956). Systemtheoretische Analyse der Zeit-, Reihenfolgenund Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus. Zeitschrift für Naturforschung 11b, 513524.CrossRefGoogle Scholar
Hassenstein, B. (1958). Über die Wahrnehmung der Bewegung von Fig 164 M. Egelhaaf and A. Borst uren und unregelmäBigen Helligkeitsmustern. Zeitschrift für Vergleichende Physiologie 40, 556592.CrossRefGoogle Scholar
Hausen, K. (1981). Monocular and binocular computation of motion in the lobula plate of the fly. Verhandlungen der Deutschen Zoologischen Cesellschaft 74, 4970.Google Scholar
Hausen, K. (1982). Motion sensitive interneurons in the optomotor system of the fly. I. The Horizontal Cells: Structure and signals. Biological Cybernetics 45, 143156.CrossRefGoogle Scholar
Hengstenberg, R. (1982). Common visual response properties of giant vertical cells in the lobula plate of the blowfly Calliphora. Journal of Comparative Physiology A 149, 179193.CrossRefGoogle Scholar
Horridge, G.A. & Marcelja, L. (1990). Responses of the H1 neuron of the fly to jumping edges. Philosophical Transactions of the Royal Society B (London) 329, 6573.Google Scholar
Kien, J. (1974 a). Sensory integration in the locust optomotor system — I: Behavioural analysis. Vision Research 14, 12451254.CrossRefGoogle Scholar
Kien, J. (1974 b). Sensory integration in the locust optomotor system II: Direction selective neurons in the circumoesophageal connectives and the optic lobe. Vision Research 14, 12551268.CrossRefGoogle ScholarPubMed
Kien, J. (1975). Neuronal mechanisms subserving directional selectivity in the locust optomotor system. Journal of Comparative Physiology 102, 337355.CrossRefGoogle Scholar
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 3768.CrossRefGoogle ScholarPubMed
Laughlin, S. (1981). Neural principles in the peripheral visual system. In Handbook of Sensory Physiology, VII/6B, ed. Autrum, H., pp. 133280. Berlin, Heidelberg, New York: Springer.Google Scholar
Laughlin, S.B. & Hardie, R.C. (1978). Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. Journal of Comparative Physiology 128, 319340.CrossRefGoogle Scholar
Laughlin, S.B. (1987). Form and function in retinal processing. Trends in Neuroscience 10, 478483.CrossRefGoogle Scholar
Laughlin, S.B., Howard, J. & Blakeslee, B. (1987). Synaptic limitations to contrast coding in the retina of the blowfly Calliphora. Proceedings of the Royal Society B (London) 231, 437467.Google Scholar
Lelkens, A.M.M. & Koenderink, J.J. (1984). Illusory motion in visual displays. Vision Research 24, 10831090.CrossRefGoogle ScholarPubMed
Maddess, T. (1986). Afterimage-like effects in the motion-sensitive neuron HI. Proceedings of the Royal Society B (London) 228, 433459.Google Scholar
Mccann, G.D. (1973). The fundamental mechanism of motion detection in the insect visual system. Kybernetik 12, 6473.CrossRefGoogle ScholarPubMed
Nakayama, K. (1985). Biological image motion processing: A review. Vision Research 25, 625660.CrossRefGoogle ScholarPubMed
Ögmen, H. & Gagne, S. (1990). Neural network architecture for motion perception and elementary motion detection in the fly visual system. Neural Networks 3, 487505.CrossRefGoogle Scholar
Pantle, A. & Picciano, L. (1976). A multistable movement display: Evidence for two separate motion systems in human vision. Science 193, 500502.CrossRefGoogle ScholarPubMed
Quenzer, T. & Zanker, J.M. (1991). Visual detection of paradoxical motion in flies. Journal of Comparative Physiology A 169, 331340.CrossRefGoogle Scholar
Reichardt, W. (1961). Autocorrelation, a principle for the evaluation of sensory information by the central nervous system. In Sensory Communication, ed. Rosenblith, W.A., pp. 303317. New York, London: The M.I.T. Press and John Wiley & Sons.Google Scholar
Reichardt, W. (1987). Evaluation of optical motion information by movement detectors. Journal of Comparative Physiology A 161, 533547.CrossRefGoogle ScholarPubMed
Riehle, A. & Franceschini, N. (1984). Motion detection in flies: Parametric control over ON-OFF pathways. Experimental Brain Research 54, 390394.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1973). The Vertebrate Retina. San Francisco, California: W.H. Freeman.Google Scholar
Ruyter Van Steveninck, R.De Zaagman, W.H. & Mastebroek, H.A.K. (1986). Adaptation of transient responses of a movementsensitive neuron in the visual system of the blowfly Calliphora erythrocephala. Biological Cybernetics 53, 451463.Google Scholar
Sato, T. (1989). Reversed apparent motion with random dot patterns. Vision Research 29, 17491758.CrossRefGoogle ScholarPubMed
Schiller, P.H. (1982). Central connections of the retinal on and off pathways. Nature 297, 580583.CrossRefGoogle ScholarPubMed
Schiller, P.H., Sandell, J.H. & Maunsell, J.H.R. (1986). Functions of the on and off channels of the visual system. Nature 322, 824825.CrossRefGoogle ScholarPubMed
Schiller, P.H. (1990). The on and off channels of the visual system. In Vision and the Brain. The Organization of the Central Visual System, ed. Cohen, B. & Bodis-Wollner, I., pp. 3541. New York: Raven Press.Google Scholar
Schuling, F.H., Mastebroek, H.A.K., Bult, R. & Lenting, B.P.M. (1989). Properties of elementary movement detectors in the fly Calliphora erythrocephala. Journal of Comparative Physiology A 165, 179192.CrossRefGoogle Scholar
Sekuler, R., Anstis, S., Braddick, O.J., Brandt, T., Movshon, J.A. & Orban, G. (1990). The perception of motion. In Visual Perception: The Neurophysiological Foundations, ed. Spillmann, L. & Werner, J.S., pp. 205230.San Diego, New York, Berkeley, Boston, London, Sydney, Tokyo, Toronto: Academic Press.CrossRefGoogle Scholar
Shechter, S. & Hochstein, S. (1990). On and off pathway contributions to apparent motion perception. Vision Research 30, 11891204.CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Miller, R.F. (1981). 2-amino-4-phosphonobutyric acid: A new pharmacological tool for retina research. Science 211, 182184.CrossRefGoogle ScholarPubMed
Sperling, G. (1989). Three stages and two systems of visual processing. Spatial Vision 4, 183207.CrossRefGoogle ScholarPubMed
Srinivasan, M.V. & Dvorak, D.R. (1980). Spatial processing of visual information in the movement-detecting pathway of the fly. Journal of Comparative Physiology 140, 123.CrossRefGoogle Scholar
Van Den Berg, A.V. & Van De Grind, W.A. (1990). Motion detection in the presence of local orientation changes. Journal of the Optical Society of America A 7, 933939.CrossRefGoogle ScholarPubMed
Van Doorn, A.J. & Koenderink, J.J. (1982a). Spatial properties of the visual detectability of moving spatial white noise. Brain Research 45, 189195.CrossRefGoogle ScholarPubMed
Van Doorn, A.J. & Koenderink, J.J. (19826). Temporal properties of the visual detectability of moving spatial white noise. Brain Research 45, 179188.CrossRefGoogle ScholarPubMed
Van Santen, J.P.H. & Sperling, G. (1984). Temporal covariance model of human motion perception. Journal of the Optical Society of America A 1, 451473.CrossRefGoogle ScholarPubMed
Varju, D. (1959). Optomotorische Reaktionen auf die Bewegung periodischer Helligkeitsmuster. Zeitschrift für Naturforschung 14b, 724735.CrossRefGoogle Scholar
Wässle, H., Boycott, B.B. & Illing, R.-B. (1981). Morphology and mosaic of onand off-beta cells in the cat retina and some functional considerations. Proceedings of the Royal Society B (London) 212, 177195.Google Scholar
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the Mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Neurophysiology 32, 339355.CrossRefGoogle ScholarPubMed
Zanker, J.M. (1990). Theta motion: A new psychophysical paradigm indicating two levels of motion detection. Naturwissenschaften 77, 243246.CrossRefGoogle Scholar