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Interactions of local movement detectors enhance the detection of rotation. Optokinetic experiments with the rock crab, Pachygrapsus marmoratus

Published online by Cambridge University Press:  02 June 2009

Roland Kern ,
Hans-Ortwin Nalbach  and
Dezsö Varjú
Roland Kern
Affiliation:
Lehrstuhl für Biokybernetik, Universität Tübingen, Auf der Morgenstelle 28, D-7400 Tübingen, Germany
Hans-Ortwin Nalbach
Affiliation:
Max-Planck-Institut für biologische Kybernetik, Spemannstraße 38, D-7400 Tübingen, Germany
Dezsö Varjú
Affiliation:
Lehrstuhl für Biokybernetik, Universität Tübingen, Auf der Morgenstelle 28, D-7400 Tübingen, Germany
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Abstract

Walking crabs move their eyes to compensate for retinal image motion only during rotation and not during translation, even when both components are superimposed. We tested in the rock crab, Pachygrapsus marmoratus, whether this ability to decompose optic flow may arise from topographical interactions of local movement detectors. We recorded the optokinetic eye movements of the rock crab in a sinusoidally oscillating drum which carried two 10-deg wide black vertical stripes. Their azimuthal separation varied from 20 to 180 deg, and each two-stripe configuration was presented at different azimuthal positions around the crab. In general, the responses are the stronger the more widely the stripes are separated. Furthermore, the response amplitude depends also strongly on the azimuthal positions of the stripes. We propose a model with excitatory interactions between pairs of movement detectors that quantitatively accounts for the enhanced optokinetic responses to widely separated textured patches in the visual field that move in phase. The interactions take place both within one eye and, predominantly, between both eyes. We conclude that these interactions aid in the detection of rotation.

Keywords

CrabFlow fieldRotation detectionOptokinetic responseNonlinear interaction
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 4 , July 1993 , pp. 643 - 652
Copyright
Copyright © Cambridge University Press 1993

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References

Barnes, W.J.P. (1990). Sensory basis and functional role of eye movements elicited during locomotion in the land crab Cardisoma guanhumi. Journal of Experimental Biology 154, 99–119.CrossRefGoogle Scholar
Barnes, W.J.P. & Horridge, G.A. (1969). Interaction of the movements of the two eyecups in the crab Carcinus. Journal of Experimental Biology 50, 651–671.CrossRefGoogle ScholarPubMed
Buddenbrock, W. von & Friedrich, H. (1933). Neue Beobachtungen über die kompensatorischen Augenbewegungen und den Farbensinn der Taschenkrabben (Carcinus maenas). Zeitschrift für vergleichende Physiologie 19, 747–761.CrossRefGoogle Scholar
Collett, T.S. (1980). Some operating rules for the optomotor system of a hoverfly during voluntary flight. Journal of Comparative Physiology 138, 271–282.CrossRefGoogle Scholar
Dahmen, H.J. (1980). A simple apparatus to investigate the orientation of walking insects. Experientia 36, 685–687.CrossRefGoogle Scholar
Fleischer, A.G. (1980). Analysis of the biphasic optokinetic response in the crab Carcinus maenas. Biological Cybernetics 37, 145–158.CrossRefGoogle Scholar
Fleischer, A.G. & Pflugradt, M. (1977). Continuous registration of X, Y coordinates and angular position in behavioural experiments. Experientia 33/3, 693–695.CrossRefGoogle Scholar
Gaffron, M. (1934). Untersuchungen über das Bewegungssehen bei Libellenlarven, Fliegen und Fischen. Zeitschrift für vergleichende Physiologie 20, 299–337.CrossRefGoogle Scholar
Götz, K.G. (1975). The optomotor equilibrium of the Drosophila navigation system. Journal of Comparative Physiology 99, 187–210.CrossRefGoogle Scholar
Hertz, M. (1934). Zur Physiologie des Formen- und Bewegungssehens I. Optomotorische Versuche an Fliegen. Zeitschrift für vergleichende Physiologie 20, 430–449.CrossRefGoogle Scholar
Horridge, G.A. (1966). Adaptation and other phenomena in the optokinetic response of the crab, Carcinus. Journal of Experimental Biology 44, 285–295.CrossRefGoogle ScholarPubMed
Horridge, G.A. & Sandeman, D.C. (1964). Nervous control of optokinetic responses in the crab Carcinus Proceedings of the Royal Society B (London) 161, 216–246.Google ScholarPubMed
Ibbotson, M.R. (1991). Wide-field motion-sensitive neurons tuned to horizontal movement in the honeybee, Apis mellifera. Journal of Comparative Physiology A 168, 91–102.CrossRefGoogle Scholar
Junger, W. & Dahmen, H.J. (1991). Response to self-motion in waterstriders: Visual discrimination between rotation and translation. Journal of Comparative Physiology A 169, 641–646.CrossRefGoogle Scholar
Koenderink, J.J. & Doorn, A.J. van (1976). Local structure of movement parallax of the plane. Journal of the Optical Society of America 66, 717–723.CrossRefGoogle Scholar
Koenderink, J.J. & Doorn, A.J. van (1987). Facts on optic flow. Biological Cybernetics 56, 247–254.CrossRefGoogle ScholarPubMed
Kunze, P. (1963). Der Einfluß der Größe bewegter Felder auf den optokinetischen Augenstielnystagmus der Winkerkrabbe. Ergebnisse der Biologie 26, 55–62.Google Scholar
Kunze, P. (1964). Eye-stalk reactions of the ghost crab Ocypode. In Neural Theory and Modeling, ed. Reiss, R.F., pp. 293–305. Stanford, California: Stanford University Press.Google Scholar
Longuet-Higgins, H.C. & Prazdny, K. (1980). The interpretation of a moving retinal image Proceedings of the Royal Society B (London) 208, 385–397.Google ScholarPubMed
Nalbach, H.-O. (1987). Neuroethologie der Flucht von Krabben. Dissertation der Universität Tübingen, Germany.Google Scholar
Nalbach, H.-O. (1989). Three temporal frequency channels constitute the dynamics of the optokinetic system of the crab, Carcinus maenas (L.). Biological Cybernetics 61, 59–70.CrossRefGoogle Scholar
Nalbach, H.-O. (1990 a). Discontinuous turning reaction during escape in soldier crabs. Journal of Experimental Biology 148, 483–487.CrossRefGoogle Scholar
Nalbach, H.-O. (1990 b). Translational and rotational head movements of pigeons in response to a rotating visual surround. In Brain Perception Cognition, ed. Elsner, N. & Roth, G., p. 271. Stuttgart, New York: Thieme Verlag.Google Scholar
Nalbach, H.-O. & Nalbach, G. (1987). Distribution of optokinetic sensitivity over the eye of crabs: Its relation to habitat and possible role in flow-field analysis. Journal of Comparative Physiology A 160, 127–135.CrossRefGoogle Scholar
Nalbach, H.-O., Thier, P. & Varjú, D. (1985). Light-dependent eye coupling during the optokinetic response of the crab Carcinus maenas (L.). Journal of Experimental Biology 119, 103–114.CrossRefGoogle Scholar
Nalbach, H.-O., Nalbach, G. & Forzin, L. (1989). Visual control of eye-stalk orientation in crabs: Vertical optokinetics, visual fixation of the horizon, and eye design. Journal of Comparative Physiology A 165, 577–587.CrossRefGoogle Scholar
Okada, Y. & Yamaguchi, T. (1985). Eyestalk movements in the crayfish, Procambarus clarkii. Comparative Biochemistry and Physiology 81A, 157–164.CrossRefGoogle Scholar
Paul, H., Nalbach, H.-O. & Varjú, D. (1990). Eye movements in the rock crab Pachygrapsus marmoratus walking along straight and curved paths. Journal of Experimental Biology 154, 81–97.CrossRefGoogle Scholar
Preiss, R. (1987). Motion parallax and figural properties of depth control flight speed in an insect. Biological Cybernetics 57, 1–9.CrossRefGoogle Scholar
Preiss, R. (1991). Separation of translation and rotation by means of eye-region specialization in flying gypsi moths (Lepidoptera: Lyman-triidae). Journal of Insect Behaviour 4(2), 209–219.CrossRefGoogle Scholar
Reichardt, W. & Varjú, D. (1959). Übertragungseigenschaften im Auswertesystem für das Bewegungssehen (Folgerungen aus Experimenten an dem Rüsselkäfer Clorophanus viridis). Zeitschrift für Naturforschung, 14b, 674–689.CrossRefGoogle Scholar
Rieger, J.H. (1983). Information in optical flows induced by curved paths of observation. Journal of the Optical Society of America 73(3), 339–344.CrossRefGoogle ScholarPubMed
Rieger, J.H. & Lawton, D.T. (1985). Processing differential image motion. Journal of the Optical Society of America A 2, 354–360.CrossRefGoogle ScholarPubMed
Sandeman, D.C. (1978). Regionalization in the eye of the crab Leptograpsus variegatus: Eye movements evoked by a target moving in different parts of the visual field. Journal of Comparative Physiology 123, 299–306.CrossRefGoogle Scholar
Sandeman, D.C, Kien, J. & Erber, J. (1975). Optokinetic eye movements in the crab, Carcinus maenas. II. Responses of optokinetic interneurons. Journal of Comparative Physiology 101, 259–274.CrossRefGoogle Scholar
Warren, W.H. Jr, Blackwell, A.W., Kurtz, K.J., Hatsopoulos, N.G. & Kalish, M.L. (1991). On the sufficiency of the velocity field for perception of heading. Biological Cybernetics 65, 311–320.CrossRefGoogle ScholarPubMed
Waterman, T.H., Wiersma, C.A.G. & Bush, B.M.H. (1964). Afferent visual responses in the optic nerve of the crab, Podophthalmus. Journal of Cellular and Comparative Physiology 63, 135–155.CrossRefGoogle ScholarPubMed
Wehner, R. (1981). Spatial vision in insects. In Handbook of Sensory Physiology, Vol. VII/6C: Comparative Physiology and Evolution of Vision in Invertebrates, ed. Autrum, H., pp. 287–616. Berlin, Heidelberg, New York: Springer-Verlag.CrossRefGoogle Scholar
Wiersma, C.A.G., Bush, B.M.H. & Waterman, T.H. (1964). Effeent visual responses of contralateral origin in the optic nerve of the crab Podophthalmus. Journal of Cellular and Comparative Physiology 64, 309–326.CrossRefGoogle ScholarPubMed
Wylie, R.W. & Frost, B.J. (1990). Binocular neurons in the nucleus of the basal root (nBOR) of the pigeon are selective for either translational or rotational visual flow. Visual Neuroscience 5, 489–495.CrossRefGoogle ScholarPubMed
Wylie, R.W. & Frost, B.J. (1991). Purkinje cells in the vestibulocerebellum of the pigeon respond best to either translational or rotational wholefield visual motion. Experimental Brain Research 86, 229–232.CrossRefGoogle ScholarPubMed