Animal Learning & Behavior

, Volume 22, Issue 4, pp 409–420 | Cite as

Performance of goldfish trained in allocentric and egocentric maze procedures suggests the presence of a cognitive mapping system in fishes

  • Fernando Rodriguez
  • Emilio Duran
  • Juan P. Vargas
  • Blas Torres
  • Cosme Salas


Goldfish were trained to obtain food in a four-arm maze placed in a room with relevant spatial cues. Four experimental conditions were run: allocentric, egocentric, egocentric + allocentric, and control. Relative to controls, all groups were able to solve the different tasks with high accuracy after 1 week of training. Subsequent transfer tests revealed place and response strategies for allocentric and egocentric groups, respectively, and both types of strategies for the ego-allocentric group. Moreover, the allocentric group showed the capacity to choose the appropriate trajectory toward the goal, even from novel starting points, presumably by using the distal cues as a whole. The results suggest that, in addition to using egocentric strategies, goldfish are able to solve spatial tasks on the basis of allocentric frames of reference and to build complex spatial cognitive representations of their environment.


Probe Trial Transfer Test Error Perseveration Transfer Trial Betta Splendens 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Able, K. P. (1991). Common themes and variations in animal orientation systems.American Zoologist,31, 157–167.Google Scholar
  2. Aronson, L. R. (1951, January 17). Orientation and jumping behavior in the gobiid fishBaihygobius soporator.American Museum Novitates (No. 1486), pp. 1–22.Google Scholar
  3. Aronson, L. R. (1971). Further studies on orientation and jumping behavior in die gobiid fishBathygobius soporator. In H. E. Adler (Ed.),Orientation: Sensory bases (Annals of the New York Academy of Sciences, Vol. 188, pp. 378–392). New York: New York Academy of Sciences.Google Scholar
  4. Biegler, R., &Morris, R. G. M. (1993). Landmark stability is a prerequisite for spatial but not discrimination learning.Nature,361, 631–633.CrossRefPubMedGoogle Scholar
  5. Bingman, V. P. (1990). Spatial navigation in birds. In R. Kesner, & D. S. Olton (eds),Neurobiology of comparative cognition (pp. 423–477). Hillsdale, NJ: Erlbaum.Google Scholar
  6. Bingman, V. P., Bagnoli, P., Ioalé, P., &Casini, G. (1989). Behavioral and anatomical studies of the avian hippocampus. In V. Chan-Palay & C. Kohler (Eds),The hippocampus: New vistas (pp. 379–394). New York: Alan R. Liss.Google Scholar
  7. Blodgett, H. C., &Mccutchan, K. (1947). Place versus response learning in the simple T-maze.Journal of Experimental Psychology,37, 412–422.CrossRefPubMedGoogle Scholar
  8. Collet, T. S., Cartwright, B. A., &Smith, B. A. (1986). Landmark learning and visuo-spatial memories in gerbils.Journal of Comparative Physiology A,158, 835–851.CrossRefGoogle Scholar
  9. Dodson, J. J. (1988). The nature and role of learning in the orientation and migratory behavior of fishes.Environmental Biology of Fishes,23, 161–182.CrossRefGoogle Scholar
  10. Hallacher, L. E. (1984). Relocation of original territories by displaced black-and-yellow rockfish,Sebastes chrysomelas, from Carmel Bay, California.Californian Fish & Game,7, 158–162.Google Scholar
  11. Helfman, G. S., Meyer, J. L., &McFarland, W. N. (1982). The ontogeny of twilight migration patterns in grunts (pisces: Haemulidae).Anima Behaviour,30, 317–326.CrossRefGoogle Scholar
  12. Helfman, G. S., &Schultz, E. T. (1984). Social transmission of behavioral traditions in a coral reef fish.Animal Behaviour,32, 379–384.CrossRefGoogle Scholar
  13. Hicks, L. H. (1964). Effects of overtraining on acquisition and reversal of place and response learning.Psychological Reports,15, 459–462.Google Scholar
  14. Hill, C. W., &Thune, L. E. (1952). Place and response learning in the white rat under simplified and mutually isolated conditions.Journal of Experimental Psychology,43, 289–297.CrossRefPubMedGoogle Scholar
  15. Ingle, D., &Sahagian, D. (1973). Solution of a spatial constancy problem by goldfish.Physiological Psychology,1, 83–84.Google Scholar
  16. Kleerekoper, H., Matis, J., Gensler, P., &Maynard, P. (1974). Exploratory behaviour of goldfishCarassius auratus.Animal Behaviour,22, 124–132.CrossRefGoogle Scholar
  17. Leonard, B. J., &Mcnaughton, B. L. (1990). Spatial representation in the rat: Conceptual, behavioral and neurophysiological perspectives. In R. P. Kesner & D. S. Olton (Eds),Neurobiology of comparative cognition (pp. 363–422). Hillsdale, NJ: Erlbaum.Google Scholar
  18. Mackintosh, N. J. (1965). Overtraining, transfer to proprioceptive control, and position reversal.Quarterly Journal of Experimental Psychology,17, 26–36.CrossRefPubMedGoogle Scholar
  19. Markevich, A. I. (1988). Nature of territories and homing in the eastern sea-perchSebastes taczanowski.Journal of Ichthyology,28, 161–163.Google Scholar
  20. Mazmanian, D. S., &Roberts, W. A. (1983). Spatial memory in rats under restricted viewing conditions.Learning & Motivation,14, 123–139.CrossRefGoogle Scholar
  21. McNaughton, B. L. (1987). Neural associations of movements and space: Preliminary steps toward a non-cartographic theory of spatial representation and learning.Neuroscience Letters,29, S143-S144.Google Scholar
  22. Means, L. W., &Douglas, R. J. (1970). Effects of hippocampal lesions on cue utilization in spatial discrimination in rats.Journal of Comparative & Physiological Psychology,73, 254–260.CrossRefGoogle Scholar
  23. Morris, R. G. M. (1981). Spatial localization does notrequire the presence of local cues.Learning & Motivation,12, 239–260.CrossRefGoogle Scholar
  24. Nadel, L. (1991). The hippocampus and space revisited.Hippocampus,1, 221–229.CrossRefPubMedGoogle Scholar
  25. O’keefe, J., &Conway, D. H. (1978). Hippo campal place units in the freely moving rat: Why they fire where they fire.Experimental Brain Research,31, 573–590.Google Scholar
  26. O’keefe, J., &Nadel, L. (1978).The hippocampus as a cognitive map. Oxford: Oxford University Press, Clarendon Press.Google Scholar
  27. O’keefe, J., &Nadel, L. (1979). Precis of O’Keefe & Nadel’sThe hippocampus as a cognitive map.Brain & Behavioral Sciences,2, 487–533.Google Scholar
  28. Olton, D. S. (1979). Mazes, maps and memory.American Psycholo-gist,34, 583–596.CrossRefGoogle Scholar
  29. Pitcher, T. J., &Magurran, A. E. (1983). Shoal size, patch profitability andinformation exchange in foraging goldfish.Animal Behaviour,31, 546–555.CrossRefGoogle Scholar
  30. Poucet, B., Chafuis, N., Durup, M., &Thinus-blanc, C. (1986). A study of exploratory behavior as an index of spatial knowledge in hamsters.Animal Learning & Behavior,14, 93–100.CrossRefGoogle Scholar
  31. Qutnn, T. P. (1980). Evidence for celestial and magnetic compass orientation in lake migrating sockeye salmon fry.Journal of Comparative Physiology A,137, 243–248.CrossRefGoogle Scholar
  32. Qutnn, T. P., &Brannon, E. L. (1982). The use of celestial and magnetic cues by orienting sockeye salmon smolts.Journal of Comparative Physiology A,147, 547–552.CrossRefGoogle Scholar
  33. Quinn, T. P., Merrill, R. T., &Brannon, E. L. (1981). Magnetic field detection in sockeye salmon.Journal of Experimental Zoology,217, 137–142.CrossRefGoogle Scholar
  34. Reese, E. S. (1989). Orientation behavior of butterfly fishes (family Chaetodontidae) on coral reefs: Spatial learning of route specific landmarks and cognitive maps.Environmental Biology of Fishes,25, 79–86.CrossRefGoogle Scholar
  35. Restle, F. (1957). Discrimination of cues in mazes: A resolution of the “place-vs-response” question.Psychological Review,64, 217–228.CrossRefPubMedGoogle Scholar
  36. Reynolds, L. F. (1983). Migrations patterns of five fish species in the Murray-Darling river system.Australian Journal of Marine & Freshwater Research,34, 857–871.CrossRefGoogle Scholar
  37. Roitblat, H. L., Tham, W., &Golub, L. (1982). PerformanceBetta splendens in a radial arm maze.Animal Learning & Behavior,10, 108–114.CrossRefGoogle Scholar
  38. Scharlock, D. P. (1955). The role of extramaze cues in place and response learning.Journal of Experimental Psychology,50, 249–254.CrossRefPubMedGoogle Scholar
  39. Schenk, F., &Morris, R. G. M. (1985). Dissociation between components of spatial memory in rats after recovery from the effects of the retrohippocampal lesions.Experimental Brain Research,58, 11–28.CrossRefGoogle Scholar
  40. Sutherland, N. S., &Mackintosh, N. J. (1971).Mechanisms of animal discrimination learning. New York: Academic Press.Google Scholar
  41. Sutherland, R. J., &Rudy, J. W. (1989). Configural association theory: The role of the hippocampal formation in learning, memory, and amnesia.Psychobiology,17, 129–144.Google Scholar
  42. Suzuki, S., Augerinos, G., &Black, A. H. (1980). Stimulus control of spatial behavior on the eight-arm maze in rats.Learning & Motivation,11, 1–18.CrossRefGoogle Scholar
  43. Teyke, T. (1989). Learning and remembering the environment in the blind cave fishAnoptichthysjordani.Journal of Comparative Physiology A,164, 655–662.CrossRefGoogle Scholar
  44. Thinus-blanc, C., Bouzouba, L., Chaix, K., Chapuis, N., Durup, M., &Poucet, B. (1987). A study of spatial parameters encoded during exploration in hamsters.Journal of Experimental Psychology: Animal Behavior Processes,13, 418–427.CrossRefGoogle Scholar
  45. Thinus-blanc, C., &Ingle, D. (1985). Spatial behavior in gerbils (Meriones unguiculatus).Journal of Comparative Psychology,99, 311–315.CrossRefGoogle Scholar
  46. Tolman, E. C. (1948). Cognitive maps in rats and men.Psychological Review,55, 189–208.CrossRefPubMedGoogle Scholar
  47. Tolman, E. C., Ritchie, B. F., &Kalish, D. (1946). Studies in spatial learning: II. Place learning versus response learning.Journal of Experimental Psychology,3, 221–229.CrossRefGoogle Scholar
  48. Walker, M. M. (1984). Learned magnetic field discrimination in yel-lowfin tuna,Thunnus albacares.Journal of Comparative Physiology A,155, 673–679.CrossRefGoogle Scholar
  49. Walker, M. M., &Bitterman, M. E. (1986). Attempts to train goldfish to respond to magnetic field stimuli.Naturwissenschaften,73, 12–16.CrossRefPubMedGoogle Scholar
  50. Warburton, K. (1990). The use of local landmarks by foraging goldfish.Animal Behaviour,40, 500–505.CrossRefGoogle Scholar
  51. Welker, W. I., &Welker, J. (1958). Reaction offish (Eucinostomus guld) to environmental changes.Ecology,39, 283–288.CrossRefGoogle Scholar
  52. Whishaw, I. Q. (1989). Dissociating performance and learning deficits on spatial navigation tasks in rats subjected to cholinergic muscarinic blockade.Brain Research Bulletin,23, 347–358.CrossRefPubMedGoogle Scholar
  53. Whishaw, I. Q., &Mittleman, G. (1986). Visits to starts, routes and places by rats (Rattus norvegicus) in swimming pool navigation tasks.Journal of Comparative Psychology,100, 422–431.CrossRefPubMedGoogle Scholar
  54. Worden, R. (1992). Navigation by fragment fitting: A theory of hippocampal function.Hippocampus,2, 165–188.CrossRefPubMedGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 1994

Authors and Affiliations

  • Fernando Rodriguez
    • 1
  • Emilio Duran
    • 1
  • Juan P. Vargas
    • 1
  • Blas Torres
    • 1
  • Cosme Salas
    • 1
  1. 1.University of SevilleSevilleSpain

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