Skip to main content
Log in

Horizontal compensatory eye movements in goldfish (Carassius auratus)

II. A comparison of normal and deafferented animals

  • Published:
Journal of comparative physiology Aims and scope Submit manuscript

Summary

  1. 1.

    Goldfish were deprived of visual input and/or normally functional horizontal semicircular canals.

  2. 2.

    Their horizontal eye movements were measured from cinematographic records, and the extent to which the eyes compensated for horizontal rotations of the head was given by the “compensation factor,” CF, the ratio (rotation of the eyes relative to the head)/(rotation of the head). All data were obtained from freely-swimming fish.

  3. 3.

    The CF's for normal, canal-lesioned, blinded, and blinded/canal-lesioned animals were: −0.95±0.10, −0.80±0.10, −0.50±0.04, and −0.41±0.06 (means ±2 S.E.M.), respectively.

  4. 4.

    These figures lead to the conclusion that the visual input contributes −0.39 to −0.45 to the CF, while the canal input contributes only −0.09 to −0.17. Thus, the visual input is the major factor; the canals are quantitatively much less important. There is in addition a third source (or sources) contributing to the CF, since the blinded/canal-lesioned fish compensated partially.

  5. 5.

    Experiments of partially restrained animals showed that this third source is not a preprogrammed instruction, nor is it dependent on sensory feedback from the rest of the labyrinth, tactile receptors, lateral line current detectors, or proprioceptors in the trunk. Its identity remains a mystery.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Benjamins, C. E.: Contribution à la connaissance des réflexes toniques des muscles de l'oeil. Archs. néerl. Physiol.2, 536–544 (1918)

    Google Scholar 

  • Biederman-Thorson, M., Thorson, J.: Rotation-compensating reflexes independent of the labyrinth: neuromuscular correlates in the pigeon. J. comp. Physiol.83, 103–122 (1973)

    Google Scholar 

  • Bizzi, E., Kalil, R. E., Tagliasco, V.: Eye-head coordination in monkeys: evidence for centrally patterned organization. Science173, 452–454 (1971)

    Google Scholar 

  • Collewijn, H.: Optokinetic eye movements in the rabbit: input-output relations. Vision Res.9, 117–132 (1969)

    Google Scholar 

  • Delius, J. E., Vollrath, F. W.: Rotation compensating reflexes independent of the labyrinth: neurosensory correlates in pigeons. J. comp. Physiol.83, 123–124 (1973)

    Google Scholar 

  • Dijkgraaf, S.: Die Augenstielbewegungen der Languste (Panulirus vulgaris). Experientia (Basel)11, 329–330 (1955)

    Google Scholar 

  • Dijkgraaf, S.: Über die kompensatorischen Augenstielbewegungen bei Brachyuren. Pubbl. Staz. Zool. Napoli28, 341–358 (1956)

    Google Scholar 

  • Dijkgraaf, S.: The functioning and significance of the lateral-line organs. Biol. Rev.38, 51–105 (1963)

    Google Scholar 

  • Easter, S. S.: Spontaneous eye movements in restrained goldfish. Vision Res.11, 333–342 (1971)

    Google Scholar 

  • Easter, S. S.: Pursuit eye movements in goldfish (Carassius auratus). Vision Res.12, 673–688 (1972a)

    Google Scholar 

  • Easter, S. S.: Optokinetic nystagmus in goldfish. Soc. Neurosci. Abstracts2, 212 (1972b)

    Google Scholar 

  • Easter, S. S., Johns, P. R., Heckenlively, D.: Horizontal compensatory eye movements in goldfish (Carassius auratus). I. The normal animal. J. comp. Physiol.92, 23–35 (1974)

    Google Scholar 

  • Evoy, W. H., Cohen, M. J.: Central and peripheral control of arthropod movements. Advance comp. Physiol. Biochem.4, 225–266 (1971)

    Google Scholar 

  • Harden-Jones, F. R.: The reaction of fish to moving backgrounds. J. exp. Biol.40, 437–446 (1963)

    Google Scholar 

  • Harris, A. J.: Eye movements of the dogfishSqualus acanthias L. J. exp. Biol.43, 107–130 (1965)

    Google Scholar 

  • Hermann, H. T., Constantine, M.: Eye movements in the goldfish. Vision Res.11, 313–333 (1971)

    Google Scholar 

  • Horridge, G. A.: Study of a system, as illustrated by the Optokinetic response. In: S.E.B. Symp.20, Nervous and hormonal mechanisms of integration, p. 179–197 (1966)

    Google Scholar 

  • Lowenstein, O.: The tonic function of the horizontal semicircular canals in fishes. J. exp. Biol.14, 473–482 (1937)

    Google Scholar 

  • Lowenstein, O.: The labyrinth. In: Fish Physiology, Vol. V, 207–241 (ed. Hoar, W. D., and D. J. Randall). New York: Academic Press 1971

    Google Scholar 

  • Lowenstein, O., Sand, A.: The individual and integrated activity of the semicircular canals of the elasmobranch labyrinth. J. Physiol. (Lond.)99, 89–101 (1940)

    Google Scholar 

  • Lyon, E. P.: A contribution to the comparative physiology of compensatory motions. Amer. J. Physiol.3, 86–114 (1899)

    Google Scholar 

  • Lyon, E. P.: Compensatory motions in fishes. Amer. J. Physiol.4, 77–82 (1900)

    Google Scholar 

  • Roberts, B. L.: Activity of lateral-line sense organs in swimming dogfish. J. exp. Biol.56, 105–118 (1972)

    Google Scholar 

  • Robinson, D. A.: Eye movement control in primates. Science161, 1219–1224 (1968)

    Google Scholar 

  • Skavenski, A. A., Robinson, D. A.: Role of abducens neurons in vestibuloocular reflex. J. Neurophysiol.36, 724–738 (1973)

    Google Scholar 

  • Szentágothai, J.: The elementary vestibulo-ocular reflex arc. J. Neurophysiol.13, 395–407 (1950)

    Google Scholar 

  • Ter Braak, J. W. G.: Untersuchungen über optokinetischen Nystagmus. Arch. néerl. Physiol.21, 309–376 (1936)

    Google Scholar 

  • Traill, A. B., Mark, R. F.: Optic and static contributions to ocular counterrotation in carp. J. exp. Biol.52, 109–124 (1970)

    Google Scholar 

  • Trevarthen, C.: Vision in fish: the origins of the visual frame of action in vertebrates. In: The central nervous system and fish behavior (ed. D. Ingle), p. 61–96. Chicago: Chicago University Press 1968

    Google Scholar 

  • Walls, G. L.: The evolutionary history of eye movements. Vision Res.2, 69–80 (1962)

    Google Scholar 

  • Zenkin, G. M., Pigarev, I. N.: Detector properties of the ganglion cells of the pike retina. Biophysics14, 763–772 (1969)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This work was supported by grant EY-00168 from the National Eye Institute of the United States Public Health Service.

We thank Drs. M. Alpern, R. Knighton, and E. Pugh for useful critical discussions, C. Gans for the extended loan of the motion picture analyzer, Mr. L. Martonyi for photographic services, Ms. J. Smith for typing, and the staff of the Statistical Research Laboratory for the use of the MIDAS Program.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Easter, S.S., Johns, P.R. Horizontal compensatory eye movements in goldfish (Carassius auratus). J. Comp. Physiol. 92, 37–57 (1974). https://doi.org/10.1007/BF00696525

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00696525

Keywords

Navigation