Visual control of eye-stalk orientation in crabs: vertical optokinetics, visual fixation of the horizon, and eye design
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Pitch and roll eye movements of three species of crabs (Heloecius cordiformis, Mictyris longicarpus, Pachygrapsus marmoratus) were recorded in response to visual stimuli.
The ‘flat world’ species (Heloecius, Mictyris) with a zone of high vertical acuity around the equator of the eye (Zeil et al. 1986) turn the eye stalks towards a horizontal contrast line presented close to their specialized zone and pursue it for some degrees when it rotates away (Figs. 5a, b, 6a, b, 8, 10a). We interpret this as fixation of the horizon and discuss its relevance for the proposed mechanisms for ‘vision in a flat world’ (Zeil et al. 1986; Nalbach and Nalbach 1987).
Both types of crabs, the ‘flat world’ and the ‘complex world’ species, stabilize their eyes against dynamic perturbations not only via mechanosensory systems (Fig. 7, Nalbach et al. 1989) but also via an optokinetic system (Figs. 1, 2). In roll even nystagmic saccades can be elicited which, however, occur more unreliably and are about four times slower than in yaw. They are missing completely in pitch.
Regional distribution of optokinetic sensitivity over the eye in pitch and roll (Figs. 3, 4) is discussed as adaptation to image flow occurring under natural conditions.
The results obtained with the rock crab,Pachygrapsus (Fig. 4), suggest that movement detectors looking into opposite directions in the visual field might interact specifically to extract global rotational image flow.
KeywordsMovement Detector Visual Control Image Flow Specialized Zone Visual Fixation
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- Barnes WJP (1985) Introduction to The control of equilibrium. In: Barnes WJP, Gladden MH (eds) Feedback and motor control in invertebrates and vertebrates. Croom Helm, London, pp 253–258Google Scholar
- Buddenbrock W von, Friedrich H (1933) Neue Beobachtungen über die kompensatorischen Augenbewegungen und den Farbensinn der Taschenkrabben (Carcinus maenas). Z Vergl Physiol 19:747–761Google Scholar
- Cameron AM (1966) Some aspects of the behaviour of the soldier crab,Mictyris longicarpus. Pacific Sci 20:224–234Google Scholar
- Dahmen HJ (1980) A simple apparatus to investigate the orientation of walking insects. Experientia 36:685–687Google Scholar
- Glantz RM, Nudelman HB, Waldrop B (1984) Linear integration of convergent visual inputs in an oculomotor reflex pathway. J Neurophysiol 52:1213–1225Google Scholar
- Götz KG (1975) The optomotor equilibrium of theDrosophila navigation system. J Comp Physiol 99:187–210Google Scholar
- Hengstenberg R (1984) Roll-stabilization during flight of the blowfly's head and body by mechanical and visual cues. In: Varjú D, Schnitzler HU (eds) Localization and orientation in biology and engineering. Springer, Berlin Heidelberg New York, pp 121–134Google Scholar
- Hengstenberg R (1988) Mechanosensory control of compensatory head roll during flight in the blowflyCalliphora erythrocephala Meig. J Comp Physiol A 163:151–165Google Scholar
- Hengstenberg R, Sandeman DC, Hengstenberg B (1986) Compensatory head roll in the blowflyCalliphora during flight. Proc R Soc Lond B 227:455–482Google Scholar
- Horridge GA, Sandeman DC (1964) Nervous control of optokinetic responses in the crabCarcinus. Proc R Soc Lond B 161:216–246Google Scholar
- Hughes A (1977) The topography of vision in mammals. In: Crescitelli F (ed) The visual system of vertebrates. (Handbook of sensory physiology vol 7/5). Springer, Berlin Heidelberg New York, pp 613–756Google Scholar
- Kunze P (1964) Eyestalk reactions of the ghost crabOcypode. In: Reiss RF (ed) Neural theory and modelling. Stanford University Press, Stanford, pp 293–304Google Scholar
- Nalbach H-O (1987) Neuroethologie der Flucht von Krabben (Decapoda: Brachyura). Doctoral thesis, University of TübingenGoogle Scholar
- Nalbach H-O (1989) Three temporal frequency channels constitute the dynamics of the optokinetic system of the crab,Carcinus maenas (L.). Biol Cybern 61:59–70Google 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. J Comp Physiol A 160:127–135Google Scholar
- Nalbach H-O, Zeil J, Forzin L (1989) Multisensory control of eye-stalk orientation in space: crabs from different habitats rely on different senses. J Comp Physiol A 165:643–649Google Scholar
- Neil DM (1975) The optokinetic responses of the mysid shrimpPraunus flexuosus. J Exp Biol 62:505–518Google Scholar
- Neil DM (1982) Compensatory eye movements. In: Sandeman DC, Atwood HL (eds) The biology of Crustacea vol 4: Neural integration and behavior. Academic, New York, pp 133–163Google Scholar
- Reichardt W, Poggio T (1976) Visual control of orientation behaviour in the fly. Part I. A quantitative analysis. Q Rev Biophys 9:311–375Google Scholar
- Rossel S (1980) Foveal fixation and tracking in the praying mantis. J Comp Physiol 139:307–331Google Scholar
- Sandeman DC (1968) A sensitive position measuring device for biological systems. Comp Biochem Physiol 24:635–638Google Scholar
- Sandeman DC (1983) The balance and visual systems of the swimming crab: their morphology and interaction. Fortschr Zool 28:213–229Google Scholar
- Sandeman DC, Erber J, Kien J (1975) Optokinetic eye movements in the crabCarcinus maenas. Eye torque. J Comp Physiol 101:243–258Google Scholar
- Varjú D (1975) Stationary and dynamic responses during visual edge fixation by walking insects. Nature 255:330–332Google Scholar
- Wiersma CAG (1970) Neuronal components of the optic nerve of the crab,Carcinus maenas. Proc K Ned Akad Wet Amsterdam 73C:25–34Google Scholar
- Wiersma CAG, Hou L-HR, Martini EM (1977) Visually reacting neuronal units in the optic nerve of the crabPachygrapsus crassipes. Proc K Ned Akad Wet Amsterdam 80C:135–143Google Scholar
- Yarbus AL (1967) Eye movements and vision. Plenum, New YorkGoogle Scholar
- Zeil J (1983) Sexual dimorphism in the visual system of flies: the free flight behaviour of male Bibionidae (Diptera). J Comp Physiol 150:395–412Google Scholar
- Zeil J, Nalbach G, Nalbach H-O (1986) Eyes, eye-stalks and the visual world of semi-terrestrial crabs. J Comp Physiol A 159:801–811Google Scholar