Este artículo es de Acceso Abierto y puede ser descargado en su versión final desde nuestro repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor


Animals, from invertebrates to humans, stabilize the panoramic optic flow through compensatory movements of the eyes, the head or the whole body, a behavior known as optomotor response (OR). The same optic flow moved clockwise or anticlockwise elicits equivalent compensatory right or left turning movements, respectively. However, if stimulated monocularly, many animals show a unique effective direction of motion, i.e., a unidirectional OR. This phenomenon has been reported in various species from mammals to birds, reptiles, and amphibious, but among invertebrates, it has only been tested in flies, where the directional sensitivity is opposite to that found in vertebrates. Although OR has been extensively investigated in crabs, directional sensitivity has never been analyzed. Here, we present results of behavioral experiments aimed at exploring the directional sensitivity of the OR in two crab species belonging to different families: the varunid mud crab Neohelice granulata and the ocypode fiddler crab Uca uruguayensis. By using different conditions of visual perception (binocular, left or right monocular) and direction of flow field motion (clockwise, anticlockwise), we found in both species that in monocular conditions, OR is effectively displayed only with progressive (front-to-back) motion stimulation. Binocularly elicited responses were directional insensitive and significantly weaker than monocular responses. These results are coincident with those described in flies and suggest a commonality in the circuit underlying this behavior among arthropods. Additionally, we found the existence of a remarkable eye dominance for the OR, which is associated to the size of the larger claw. This is more evident in the fiddler crab where the difference between the two claws is huge. Copyright © 2019 Barnatan, Tomsic and Sztarker. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.


Documento: Artículo
Título:Unidirectional Optomotor Responses and Eye Dominance in Two Species of Crabs
Autor:Barnatan, Yair; Tomsic, Daniel; Sztarker, Julieta
Filiación:Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:Adult; Animal behavior; Animal experiment; Arthropod; Crab; Eye dominance; Eye movement; Male; Motor performance; Neohelice granulata; Nonhuman; Uca uruguayensis; Vision; Visual stimulation; Eye dominance; Lateralization; Monocular vision; Optic flow; Semiterrestrial crabs; Unidirectional optomotor response
Número de artículo:586
Página de inicio:1
Página de fin:11
Título revista:Frontiers in Physiology
Título revista abreviado:Front. Physiol.


  • Barnes, W. J. P., and Barnes, P. (1990). Sensory basis and functional role of eye movements elicited during locomotion in the land crab Cardisoma guanhumi. J. Exp. Biol. 154, 99–118.
  • Barnes, W. J., and Horridge, G. A. (1969). Two-dimensional records of the eyecup movements of the crab Carcinus. J. Exp. Biol. 50, 673–682.
  • Barnes, W. J. P., and Nalbach, H.-O. (1993). Eye movements in freely moving crabs: their sensory basis and possible role in flow-field analysis. Comp. Biochem. Physiol. A Physiol. 104, 675–693. doi: 10.1016/0300-9629(93)90145-T
  • Bates, D., Maechler, M., Bolker, B., and Walker, S. (2015). Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. doi: 10.18637/jss.v067.i01
  • Ahmed, M. (1978). Development of asymmetry in the fiddler crab Uca cumulanta crane, 1943 (Decapoda Brachyura). Crustaceana 34, 294–300. doi: 10.1163/156854078X00853
  • Astrada, M. B., Bengochea, M., Medan, V., and Tomsic, D. (2012). Regionalization in the eye of the grapsid crab Neohelice granulata (=Chasmagnathus granulatus): variation of resolution and facet diameters. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 198, 173–180. doi: 10.1007/s00359-011-0697-7
  • Beersma, D. G. M., Stavenga, D. G., and Kuiper, J. W. (1977). Retinal lattice, visual field and binocularities in flies. J. Comp. Physiol. 119, 207–220. doi: 10.1007/BF00656634
  • Berón de Astrada, M., Tuthill, J. C., and Tomsic, D. (2009). Physiology and morphology of sustaining and dimming neurons of the crab Chasmagnathus granulatus (Brachyura: Grapsidae). J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 195, 791–798. doi: 10.1007/s00359-009-0448-1
  • Bengochea, M., and Berón de Astrada, M. (2014). Organization of columnar inputs in the third optic ganglion of a highly visual crab. J. Physiol. Paris 108, 61–70. doi: 10.1016/j.jphysparis.2014.05.005
  • Bengochea, M., Berón de Astrada, M., Tomsic, D., and Sztarker, J. (2018). A crustacean lobula plate: morphology, connections, and retinotopic organization. J. Comp. Neurol. 526, 109–119. doi: 10.1002/cne.24322
  • Borst, A., and Egelhaaf, M. (1989). Principles of visual motion detection. Trends Neurosci. 12, 297–306. doi: 10.1016/0166-2236(89)90010-6
  • Borst, A., and Haag, J. (2002). Neural networks in the cockpit of the fly. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 188, 419–437. doi: 10.1007/s00359-002-0316-8
  • Byrne, R. A., Kuba, M. J., and Meisel, D. V. (2004). Lateralized eye use in Octopus vulgaris shows antisymmetrical distribution. Anim. Behav. 68, 1107–1114. doi: 10.1016/j.anbehav.2003.11.027
  • Caves, E. M., Frank, T. M., and Johnsen, S. (2016). Spectral sensitivity, spatial resolution and temporal resolution and their implications for conspecific signalling in cleaner shrimp. J. Exp. Biol. 219, 597–608. doi: 10.1242/jeb.122275
  • Collewijn, H. (1969). Optokinetic eye movements in the rabbit: input-output relations. Vis. Res. 9, 117–132. doi: 10.1016/0042-6989(69)90035-2
  • Daly, I. M., How, M. J., Partridge, J. C., and Roberts, N. W. (2017). The independence of eye movements in a stomatopod crustacean is task dependent. J. Exp. Biol. 220, 1360–1368. doi: 10.1242/jeb.153692
  • De Astrada, M. B., Medan, V., and Tomsic, D. (2011). How visual space maps in the optic neuropils of a crab. J. Comp. Neurol. 519, 1631–1639. doi: 10.1002/cne.22612
  • Duistermars, B. J., Care, R. A., and Frye, M. A. (2012). Binocular interactions underlying the classic optomotor responses of flying flies. Front. Behav. Neurosci. 6:6. doi: 10.3389/fnbeh.2012.00006
  • Easter, S. S. (1972). Pursuit eye movements in goldfish (Carassius auratus). Vis. Res. 12, 673–688. doi: 10.1016/0042-6989(72)90161-7
  • Frasnelli, E. (2013). Brain and behavioral lateralization in invertebrates. Front. Psychol. 4:939. doi: 10.3389/fpsyg.2013.00939
  • Fukuda, T. (1959). The unidirectionality of the labyrinthine reflex in relation to the unidirectionality of the optokinetic reflex. Acta Otolaryngol. 50, 507–516. doi: 10.3109/00016485909129226
  • Hausen, K. (1982a). Motion sensitive interneurons in the optomotor system of the fly I. Biol. Cybern. 45, 143–156. doi: 10.1007/BF00335241
  • Hausen, K. (1982b). Motion sensitive interneurons in the optomotor system of the fly II. Biol. Cybern. 46, 67–79. doi: 10.1007/BF00335352
  • Heisenberg, M., Wonneberger, R., and Wolf, R. (1978). Optomotor-blind H31—a Drosophila mutant of the lobula plate giant neurons. J. Comp. Physiol. 124, 287–296. doi: 10.1007/BF00661379
  • Honkanen, A., Takalo, J., Heimonen, K., Vähäsöyrinki, M., and Weckström, M. (2014). Cockroach optomotor responses below single photon level. J. Exp. Biol. 217, 4262–4268. doi: 10.1242/jeb.112425
  • Horridge, G. A. (1965). “The optomotor response of the crab, Carcinus” in Proceedings of the symposium on information processing in sight sensory systems (Pasadena, California: CALTECH).
  • Horridge, G. A., and Burrows, M. (1968). The onset of the fast phase in the optokinetic response of the crab, Carcinus. J. Exp. Biol. 49, 299–313. Available at:
  • Horridge, G. A., and Sandeman, D. C. (1964). Nervous control of optokinetic responses in the crab carcinus. Proc. R. Soc. Lond. B Biol. Sci. 161, 216–246. doi: 10.1098/rspb.1964.0091
  • Jardon, B., and Bonaventure, N. (1995). Are retinal or mesencephalic dopaminergic systems involved in monocular optokinetic nystagmus asymmetry in frog? Vis. Res. 35, 381–388. doi: 10.1016/0042-6989(94)00143-A
  • Johnson, A. P., Horseman, B. G., Macauley, M. W. S., and Barnes, W. J. P. (2002). PC-based visual stimuli for behavioural and electrophysiological studies of optic flow field detection. J. Neurosci. Methods 114, 51–61. doi: 10.1016/S0165-0270(01)00508-8
  • Kells, A. R., and Goulson, D. (2001). Evidence for handedness in bumblebees. J. Insect Behav. 14, 47–55. doi: 10.1023/A:1007897512570
  • Kern, R., and Egelhaaf, M. (2000). Optomotor course control in flies with largely asymmetric visual input. J. Comp. Physiol. A 186, 45–55. doi: 10.1007/s003590050006
  • Kern, R., Lutterklas, M., and Egelhaaf, M. (2000). Neuronal representation of optic flow experienced by unilaterally blinded flies on their mean walking trajectories. J. Comp. Physiol. A 186, 467–479. doi: 10.1007/s003590050445
  • Kern, R., Nalbach, H. O., and Varjú, D. (1993). Interactions of local movement detectors enhance the detection of rotation. Optokinetic experiments with the rock crab, Pachygrapsus marmoratus. Vis. Neurosci. 10, 643–652. doi:10.1017/S0952523800005344
  • Labhart, T., and Wiersma, C. A. (1976). Habituation and inhibition in a class of visual interneurons of the rock lobster, Panulirus interruptus. Comp. Biochem. Phys. A 55, 219–224.
  • Land, M. F. (1999). Motion and vision: why animals move their eyes. J. Comp. Physiol. A 185, 341–352.
  • Layne, J., Land, M., and Zeil, J. (1997). Fiddler crabs use the visual horizon to distinguish predators from conspecifics: a review of the evidence. J. Mar. Biol. Assoc. U. K. 77, 43–54. doi: 10.1017/S0025315400033774
  • Letzkus, P., Boeddeker, N., Wood, J. T., Zhang, S.-W., and Srinivasan, M. V. (2008). Lateralization of visual learning in the honeybee. Biol. Lett. 4, 16–19. doi: 10.1098/rsbl.2007.0466
  • Letzkus, P., Ribi, W. A., Wood, J. T., Zhu, H., Zhang, S.-W., and Srinivasan, M. V. (2006). Lateralization of olfaction in the honeybee Apis mellifera. Curr. Biol. 16, 1471–1476. doi: 10.1016/j.cub.2006.05.060
  • Mariappan, P., Balasundaram, C., and Schmitz, B. (2000). Decapod crustacean chelipeds: an overview. J. Biosci. 25, 301–313. doi: 10.1007/BF02703939
  • Medan, V., Berón De Astrada, M., Scarano, F., and Tomsic, D. (2015). A network of visual motion-sensitive neurons for computing object position in an arthropod. J. Neurosci. 35, 6654–6666. doi: 10.1523/JNEUROSCI.4667-14.2015
  • Medan, V., Oliva, D., and Tomsic, D. (2007). Characterization of lobula giant neurons responsive to visual stimuli that elicit escape behaviors in the crab Chasmagnathus. J. Neurophysiol. 98, 2414–2428. doi: 10.1152/jn.00803.2007
  • Miller, C. S., Johnson, D. H., Schroeter, J. P., Myint, L. L., and Glantz, R. M. (2002). Visual signals in an optomotor reflex: systems and information theoretic analysis. J. Comput. Neurosci. 13, 5–21. doi: 10.1023/A:1019601809908
  • Mowrer, O. H. (1936). A comparison of the reaction mechanisms mediating optokinetic nystagmus in human beings and in pigeons. Psychol. Monogr. 47, 294–305. doi: 10.1037/h0093419
  • Munguia, P., and Heldt, K. (2016). Dichotomous male asymmetry in metapopulations of a marine amphipod. J. Crustac. Biol. 36, 451–455. doi: 10.1163/1937240X-00002437
  • Nalbach, H.-O., and 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, 127–135. doi: 10.1007/BF00613448
  • Nalbach, H. O., Thier, P., and Varjú, D. (1993). Binocular interaction in the optokinetic system of the crab Carcinus maenas (L.): optokinetic gain modified by bilateral image flow. Vis. Neurosci. 10, 873–885. doi: 10.1017/S0952523800006088
  • Nityananda, V., Tarawneh, G., Errington, S., Serrano-Pedraza, I., and Read, J. (2017). The optomotor response of the praying mantis is driven predominantly by the central visual field. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 203, 77–87. doi: 10.1007/s00359-016-1139-3
  • Ocklenburg, S., Beste, C., and Güntürkün, O. (2013). Handedness: a neurogenetic shift of perspective. Neurosci. Biobehav. Rev. 37, 2788–2793. doi: 10.1016/j.neubiorev.2013.09.014
  • Pérez Sáez, J. M. (2003). “Origen de la variabilidad en respuestas a estímulos visuales en el cangrejo Chasmagnathus” in Alteraciones, ajuste y posible reorganización neural del sistema visual (FCEN-UBA: Tesis de Licenciatura).
  • R Core Team (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at:
  • Sandeman, D. C., Kien, J., and Erber, J. (1975). Optokinetic eye movements in the crab, Carcinus maenas. J. Comp. Physiol. 101, 259–274. doi: 10.1007/BF00657186
  • Wiersma, C. A. (1966). Integration in the visual pathway of crustacea. Symp. Soc. Exp. Biol. 20, 151–177.
  • Wiersma, C. A. (1970). Neuronal components of the optic nerve of the crab, Carcinus maenas. Proc. K. Ned. Akad. Wet. C 73, 25–34.
  • Wiersma, C. A., and Mill, P. J. (1965). “Descending” neuronal units in the commissure of the crayfish central nervous system; and their integration of visual, tactile and proprioceptive stimuli. J. Comp. Neurol. 125, 67–94. doi: 10.1002/cne.901250107
  • Wiersma, C. A., and Yamaguchi, T. (1967). The integration of visual stimuli in the rock lobster. Vis. Res. 7, 197–203. doi: 10.1016/0042-6989(67)90084-3
  • Wiersma, C. A., and Yanagisawa, K. (1971). On types of interneurons responding to visual stimulation present in the optic nerve of the rock lobster, Panulirus interruptus. J. Neurobiol. 2, 291–309. doi: 10.1002/neu.480020403
  • Wiersma, C. A., and York, B. (1972). Properties of the seeing fibers in the rock lobster: field structure, habituation, attention and distraction. Vis. Res. 12, 627–640. doi: 10.1016/0042-6989(72)90158-7
  • Windsor, S. P., Bomphrey, R. J., and Taylor, G. K. (2014). Vision-based flight control in the hawkmoth Hyles lineata. J. R. Soc. Interface 11:20130921. doi:10.1098/rsif.2013.0921
  • Young, R. E., and Govind, C. K. (1983). Neural asymmetry in male fiddler crabs. Brain Res. 280, 251–262. doi: 10.1016/0006-8993(83)90055-0
  • Yücel, Y. H., Jardon, B., Kim, M.-S., and Bonaventure, N. (1990). Directional asymmetry of the horizontal monocular head and eye optokinetic nystagmus: effects of picrotoxin. Vis. Res. 30, 549–555. doi: 10.1016/0042-6989(90)90067-U
  • Scarano, F., Sztarker, J., Medan, V., Berón de Astrada, M., and Tomsic, D. (2018). Binocular neuronal processing of object motion in an arthropod. J. Neurosci. 38, 6933–6948. doi: 10.1523/JNEUROSCI.3641-17.2018
  • Smolka, J., and Hemmi, J. M. (2009). Topography of vision and behaviour. J. Exp. Biol. 212, 3522–3532. doi: 10.1242/jeb.032359
  • Spivak, E. D., Gavio, M. A., and Navarro, C. E. (1991). Life history and structure of the world’s southernmost Uca population: Uca Uruguayensis (Crustacea, Brachyura) in Mar Chiquita Lagoon (Argentina). Available at: (Accessed February 15, 2019).
  • Sztarker, J., Strausfeld, N., Andrew, D., and Tomsic, D. (2009). Neural organization of first optic neuropils in the littoral crab Hemigrapsus oregonensis and the semiterrestrial species Chasmagnathus granulatus. J. Comp. Neurol. 513, 129–150. doi: 10.1002/cne.21942
  • Sztarker, J., Strausfeld, N. J., and Tomsic, D. (2005). Organization of optic lobes that support motion detection in a semiterrestrial crab. J. Comp. Neurol. 493, 396–411. doi: 10.1002/cne.20755
  • Sztarker, J., and Tomsic, D. (2004). Binocular visual integration in the crustacean nervous system. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 190, 951–962. doi: 10.1007/s00359-004-0551-2
  • Sztarker, J., and Tomsic, D. (2014). Neural organization of the second optic neuropil, the medulla, in the highly visual semiterrestrial crab Neohelice granulata. J. Comp. Neurol. 522, 3177–3193. doi: 10.1002/cne.23589
  • Tauber, E. S., and Atkin, A. (1968). Optomotor responses to monocular stimulation: relation to visual system organization. Science 160, 1365–1367. doi: 10.1126/science.160.3834.1365
  • Tomsic, D., and Maldonado, H. (1990). Central effect of morphine pretreatment on short- and long-term habituation to a danger stimulus in the crab Chasmagnathus. Pharmacol. Biochem. Behav. 36, 787–793. doi: 10.1016/0091-3057(90)90078-V
  • Waterman, T. H., Wiersma, C. A., and Bush, B. M. (1964). Afferent visual responses in the optic nerve of the crab, Podophthalmus. J. Cell. Comp. Physiol. 63, 135–155. doi: 10.1002/jcp.1030630203
  • Wehrhahn, C., and Hausen, K. (1980). How is tracking and fixation accomplished in the nervous system of the fly? Biol. Cybern. 38, 179–186. doi: 10.1007/BF00337407


---------- APA ----------
Barnatan, Yair, Tomsic, Daniel & Sztarker, Julieta (2019) . Unidirectional Optomotor Responses and Eye Dominance in Two Species of Crabs. Frontiers in Physiology, 10, 1-11.
---------- CHICAGO ----------
Barnatan, Yair, Tomsic, Daniel, Sztarker, Julieta. "Unidirectional Optomotor Responses and Eye Dominance in Two Species of Crabs" . Frontiers in Physiology 10 (2019) : 1-11.
---------- MLA ----------
Barnatan, Yair, Tomsic, Daniel, Sztarker, Julieta. "Unidirectional Optomotor Responses and Eye Dominance in Two Species of Crabs" . Frontiers in Physiology, vol. 10, 2019, pp. 1-11.
---------- VANCOUVER ----------
Barnatan, Yair, Tomsic, Daniel, Sztarker, Julieta. Unidirectional Optomotor Responses and Eye Dominance in Two Species of Crabs. Front. Physiol. 2019;10:1-11.