Skip to main content

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

  • Martin Egelhaaf (a1) and Alexander Borst (a1)

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.

Hide All
Anstis, S.M. (1970). Phi motion as a subtraction process. Vision Research 10, 14111430.
Anstis, S.M. & Mather, G. (1985). Effects of luminance and contrast on direction of ambiguous apparent motion. Perception 14, 167179.
Anstis, S.M. & Rogers, B.J. (1975). Illusory reversal of visual depth and movement during changes of contrast. Vision Research 15, 957961.
Arnett, D.W. (1972). Spatial and temporal integration properties of units in first optic ganglion of dipterans. Journal of Neurophysiology 35, 429444.
Borst, A. & Egelhaaf, M. (1987). Temporal modulation of luminance adapts time constant of fly movement detectors. Biological Cybernetics 56, 209215.
Borst, A. & Egelhaaf, M. (1989). Principles of visual motion detection. Trends in Neuroscience 12, 297306.
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.
Buchner, E. (1976). Elementary movement detectors in an insect visual system. Biological Cybernetics 24, 85101.
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.
Cavanagh, P. & Mather, G. (1989). Motion: The long and short of it. Spatial Vision 4, 103129.
Chaudhuri, A. & Albright, T.D. (1991). Perceptual and optokinetic responses to moving contrast-reversed patterns. Investigative Ophthalmology and Visual Science 32, 827.
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.
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.
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.
Eckert, H. (1973). Optomotorische Untersuchungen am visuellen System der Stubenfliege Musca domestica L. Kybernetik 14, 123.
Eckert, H. (1980). Functional properties of the Hl-neurone in the third optic ganglion of the blowfly, Phaenicia. Journal of Comparative Physiology 135, 2939.
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.
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.
Egelhaaf, M., Borst, A. & Pilz, B. (1990). The role of GABA in detecting visual motion. Brain Research 509, 156160.
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.
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.
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.
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.
Franceschini, N., Monster, A. & Heurkens, G. (1979). Aquatoriales und binokulares Sehen bei der Fliege Calliphora erythrocephala. Verhandlungen der Deutschen Zoologischen Gesellschaft 1979, 209.
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.
Götz, K.G. (1964). Optomotorische Untersuchungen des visuellen Systems einiger Augenmutanten der Fruchtfliege Drosophila. Kybernetik 2, 7792.
Götz, K.G. (1965). Die optischen Uöbertragungseigenschaften der Komplexaugen von Drosophila. Kybernetik 2, 215221.
Götz, K.G. (1972). Principles of optomotor reactions in insects. Bibliotheca Ophthalmologica 82, 251259.
Hassenstein, B. & Reichardt, W. (1956). Systemtheoretische Analyse der Zeit-, Reihenfolgenund Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus. Zeitschrift für Naturforschung 11b, 513524.
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.
Hausen, K. (1981). Monocular and binocular computation of motion in the lobula plate of the fly. Verhandlungen der Deutschen Zoologischen Cesellschaft 74, 4970.
Hausen, K. (1982). Motion sensitive interneurons in the optomotor system of the fly. I. The Horizontal Cells: Structure and signals. Biological Cybernetics 45, 143156.
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.
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.
Kien, J. (1974 a). Sensory integration in the locust optomotor system — I: Behavioural analysis. Vision Research 14, 12451254.
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.
Kien, J. (1975). Neuronal mechanisms subserving directional selectivity in the locust optomotor system. Journal of Comparative Physiology 102, 337355.
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 3768.
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.
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.
Laughlin, S.B. (1987). Form and function in retinal processing. Trends in Neuroscience 10, 478483.
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.
Lelkens, A.M.M. & Koenderink, J.J. (1984). Illusory motion in visual displays. Vision Research 24, 10831090.
Maddess, T. (1986). Afterimage-like effects in the motion-sensitive neuron HI. Proceedings of the Royal Society B (London) 228, 433459.
Mccann, G.D. (1973). The fundamental mechanism of motion detection in the insect visual system. Kybernetik 12, 6473.
Nakayama, K. (1985). Biological image motion processing: A review. Vision Research 25, 625660.
Ögmen, H. & Gagne, S. (1990). Neural network architecture for motion perception and elementary motion detection in the fly visual system. Neural Networks 3, 487505.
Pantle, A. & Picciano, L. (1976). A multistable movement display: Evidence for two separate motion systems in human vision. Science 193, 500502.
Quenzer, T. & Zanker, J.M. (1991). Visual detection of paradoxical motion in flies. Journal of Comparative Physiology A 169, 331340.
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.
Reichardt, W. (1987). Evaluation of optical motion information by movement detectors. Journal of Comparative Physiology A 161, 533547.
Riehle, A. & Franceschini, N. (1984). Motion detection in flies: Parametric control over ON-OFF pathways. Experimental Brain Research 54, 390394.
Rodieck, R.W. (1973). The Vertebrate Retina. San Francisco, California: W.H. Freeman.
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.
Sato, T. (1989). Reversed apparent motion with random dot patterns. Vision Research 29, 17491758.
Schiller, P.H. (1982). Central connections of the retinal on and off pathways. Nature 297, 580583.
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.
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.
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.
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.
Shechter, S. & Hochstein, S. (1990). On and off pathway contributions to apparent motion perception. Vision Research 30, 11891204.
Slaughter, M.M. & Miller, R.F. (1981). 2-amino-4-phosphonobutyric acid: A new pharmacological tool for retina research. Science 211, 182184.
Sperling, G. (1989). Three stages and two systems of visual processing. Spatial Vision 4, 183207.
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.
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.
Van Doorn, A.J. & Koenderink, J.J. (1982a). Spatial properties of the visual detectability of moving spatial white noise. Brain Research 45, 189195.
Van Doorn, A.J. & Koenderink, J.J. (19826). Temporal properties of the visual detectability of moving spatial white noise. Brain Research 45, 179188.
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.
Varju, D. (1959). Optomotorische Reaktionen auf die Bewegung periodischer Helligkeitsmuster. Zeitschrift für Naturforschung 14b, 724735.
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.
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the Mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Neurophysiology 32, 339355.
Zanker, J.M. (1990). Theta motion: A new psychophysical paradigm indicating two levels of motion detection. Naturwissenschaften 77, 243246.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 11 *
Loading metrics...

Abstract views

Total abstract views: 244 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 14th August 2018. This data will be updated every 24 hours.