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Binocular interaction in the optokinetic system of the crab Carcinus maenas (L.): Optokinetic gain modified by bilateral image flow

Published online by Cambridge University Press:  02 June 2009

Hans-Ortwin Nalbach
Affiliation:
Lehrstuhl für Biokybernetik, Universität Tübingen, Auf der Morgenstelle 28, D-7400 Tübingen, Germany
Peter Thier
Affiliation:
Lehrstuhl für Biokybernetik, Universität Tübingen, Auf der Morgenstelle 28, D-7400 Tübingen, Germany
Dezsö Varjú
Affiliation:
Lehrstuhl für Biokybernetik, Universität Tübingen, Auf der Morgenstelle 28, D-7400 Tübingen, Germany

Abstract

We recorded optokinetic eye movements of the crab, Carcinus maenas, in split-drum experiments. The patterns were either oscillated in antiphase on both sides mimicking translational image flow or they were oscillated in phase producing rotational image flow. Eye movements elicited by the rotational stimulus were larger than those produced by the pseudotranslational pattern movements. The smaller response to the latter is mainly a consequence of binocular interaction, the strength of which depends on both the phase-shift and amplitude of pattern oscillation. We develop two hypotheses to explain our results: either (1) signals from each eye modify the gain of the linkage signals coming from the other eye, or (2) the signals coming from the other eye modify the gain of the control loop itself. Quantitative evaluation of the data favors the second of these two hypotheses, which comprises the models of Barnes and Horridge (1969) and Nalbach et al. (1985). In addition, we found that it is the signals from the two slow channels of the crab's movement-detecting system that are transferred from one eye to the other, while signals of the fastest channel act almost exclusively ipsilaterally. We discuss our results as an adaptation by which an animal with panoramic vision compensates exclusively the rotational component of image flow during locomotion. The fact that freely walking crabs distinguish the two components of image flow better than restrained crabs indicates that further visual and nonvisual signals help to disentangle image flow.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1993

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References

Ariel, M. (1990). Independent eye movements in the turtle. Visual Neuroscience 5, 29–41.CrossRefGoogle ScholarPubMed
Barnes, W.J.P. (1990). Sensory basis and functional role of eye movements elicited during locomotion in the land crab Cardiosoma guan-humi. Journal of Experimental Biology 154, 99–119.Google 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
Bloch, S., Rivaud, S. & Martinoya, C. (1984). Comparing frontal and lateral viewing in the pigeon, III. Different patterns of eye movements for binocular and monocular fixation. Behavioral Brain Research 13, 173–182.CrossRefGoogle ScholarPubMed
Buddenbrock, W. Von & Friedrich, H. (1933). Neue Beobachtungen über die kompensatorischen Augenbewegungen und den Far-bensinn der Taschenkrabben (Carcinus maenas). Zeitschrift für vergleichende Physiologie 19, 747–761.Google Scholar
Collewijn, H. & Noorduin, H. (1972). Conjugate and disjunctive optokinetic eye movements in the rabbit evoked by rotatory and trans-latory motion. Pflügers Archives 335, 173–185.CrossRefGoogle ScholarPubMed
Fernald, R.D. (1985). Eye movements in the African cichlid fish, Haplochromis burtoni. Journal of Comparative Physiology 156, 199–208.CrossRefGoogle Scholar
Fleischer, A.G. (1980). Analysis of the biphasic optokinetic response in the crab Carcinus maenas. Biological Cybernetics 37, 145–158.Google Scholar
Fleischer, A.G. & Pflugradt, M. (1977). Continuous registration of X, Y-coordinates and angular position in behavioural experiments. Experientia 33, 693–695.Google Scholar
Gioanni, H. (1988). Stabilizing gaze reflexes in the pigeon (Columba livia). I. Horizontal and vertical optokinetic eye (OKN) and head (OCR) reflexes. Experimental Brain Research 69, 567–582.CrossRefGoogle ScholarPubMed
Hamada, T. (1986). Nonconjugate monocular optokinetic nystagmus in cats. Vision Research 26, 1311–1314.Google 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. & Goodman, L.J. (1990). Response characteristics of four wide-field motion-sensitive descending interneurones in Apis mellifera. Journal of Experimental Biology 148, 255–279.CrossRefGoogle Scholar
Kern, R., Nalbach, H.-O. & Varjú, D. (1993). Interactions of local movement detectors enhance the detection of rotation. Optokinetic experiments with the rock crab, Pachygrapsus marmoratus. Visual Neuroscience 10, 643–652.CrossRefGoogle ScholarPubMed
Kirmse, W. (1988). Foveal and ambient visuomotor control in Chamae-leons (Squamata) — Experimental results and comparative review. Zoologisches Jahrbuch für Physiologie 92, 341–350.Google Scholar
Kirschfeld, K. (1991) An optomotor control system with automatic compensation for contrast and texture. Proceedings of the Royal Society B (London) 246, 261–268.Google ScholarPubMed
Lazar, G. (1989). Altering the direction of optokinetic head nystagmus: A lesion study and a hypothetical model. Experimental Brain Research 11, 193–200.Google Scholar
Manteuffel, G. (1987). Binocular afferents to the salamander pretec-tum mediate rotation sensitivity of cells selective for visual background motions. Brain Research 422, 381–383.CrossRefGoogle 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). Multisensory control of eyestalk orientation in decapod crustaceans. An ecological approach. Journal of Crustacean Biology 10, 382–399.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 160, 127–135.Google 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.Google Scholar
Paul, H., Nalbach, H.-O. & Varjü, D. (1990). Eye movements in the rock crab Pachygrapsus marmoratus walking along straight and curved paths. Journal of Experimental Biology 154, 81–97.Google Scholar
Sandeman, D.C. (1978). Eye-scanning during walking in the crab Lep-tograpsus variegatus. Journal of Comparative Physiology 124, 349–357.Google Scholar
Steinman, R.M. & Collewijn, H. (1980). Binocular retinal image motion during active head rotation. Vision Research 20, 415–429.CrossRefGoogle ScholarPubMed
Tauber, E.S. & Atkin, A. (1967). Disconjugate eye movement patterns during optokinetic stimulation of the African chameleon, Chameleo melleri. Nature 214, 1008–1010.CrossRefGoogle ScholarPubMed
Winterson, B.J., Collewijn, H. & Steinman, R.M. (1979). Compensatory eye movements to miniature rotations in the rabbit: Implications for retinal stability. Vision Research 19, 1155–1159.Google Scholar
Wylie, D.R. & Frost, B.J. (1990). Binocular neurons in the nucleus of the basal optic root (nBOR) of the pigeon are selective for either translational or rotational visual flow. Visual Neuroscience 5, 489–495.Google Scholar
Yücel, Y.H., Jardon, B. & Bonaventura, N. (1990). Directional asymmetry of the horizontal monocular head and eye optokinetic nystagmus. Vision Research 30, 549–555.CrossRefGoogle ScholarPubMed
Zeil, J., Nalbach, G. & Nalbach, H.-O. (1986). Eyes, eye stalks and the visual world of semi-terrestrial crabs. Journal of Comparative Physiology 159, 801–811.CrossRefGoogle Scholar