This review addresses studies of spatial memory and learning in birds performed using the radial maze method. Descriptions of different versions of this test (standard and “giant” tunnel-type mazes, as well as unstructured “analogs”) are described and the methodological problems of testing birds are discussed. Behavioral measures from birds and laboratory rats, as the “standard” system for radial maze studies, are compared. The characteristics of spatial learning in birds of different systematic groups (pigeons, tits, corvids, chickens, etc.) are compared. Particular attention is paid to studies addressing spatial memory in closely related bird species with different ecological features, in terms of the ability to hoard food and finding their hoards after prolonged time periods, as well as to the few reports of results from experiments with migrant birds and homing pigeons.
Similar content being viewed by others
References
L. S. Bogoslavskaya and G. I. Polyakov, Pathways for the Morphological Progression of Nerve Centers in Higher Vertebrates [in Russian], Nauka, Moscow (1981).
L. N. Boronov, L. S. Bogoslavskaya, and E. G. Markova, “Comparative study of the morphology of the telencephalon in corvid birds in relation to their feeding specializations,” Zool. Zh., 7, No. 10, 82–97 (1994).
Z. A. Zorina, “Reasoning in animals: laboratory experiments and observations in nature,” Zool. Zh., 84, No. 1, 134–149 (2005).
Z. A. Zorina, A. A. Smirnova, M. G. Pleskacheva, and E. V. Dubynina, “New findings in studies of the brain and higher nervous activity in corvid birds (2002–2005). Ecology of corvid birds in conditions of natural and anthropogenic landscapes in Russia,” in: Proceedings of the 7th All-Russia Scientific Conference on Studies of the Ecology of Corvid Birds in Russia [in Russian], V. M. Konstantinov and I. I. Rakhimov (eds.), Novoe Znanie, Kazan (2006), pp. 16–43.
V. D. Il’ichev and E. K. Vilks, Spatial Orientation in Birds [in Russian], Nauka, Moscow (1978).
N. L. Krushinskaya, “A number of complex food-related forms of behavior in nutcrackers after ablation of the archecortex,” Zh. Évolyuts. Biokhim. Fiziol., 2, No. 6, 563–568 (1966).
L. V. Krushinskii, Formation of Animal Behavior in Normal and Pathological Conditions [in Russian], Moscow State University Press, Moscow (1960).
L. V. Krushinskii, Biological Bases of Cognitive Activity [in Russian], Moscow State University Press (1986).
D. K. Obukhov, Current Concepts on the Structural-Functional Organization of the Telencephalon in Birds. Morphogenesis and Reactive Rearrangement of the Nervous System [in Russian], O. S. Sotnikov (ed.), St. Petersburg University Press, St. Petersburg (1996), pp. 113–133.
M. G. Pleskacheva, P. A. Kuptsov, A. A. Smirnova, M. G. Bagotskaya, and Kh.-P. Lipp, “Training of gray crows (Corvus cornix L.) in a ‘giant’ 8-arm radial maze,” Zh. Vyssh. Nerv. Deyat., 53, No. 6, 808–811 (2003).
A. G. Rezanov, Feeding Behavior: A Method for Digital Coding and Database Analysis [in Russian], Izdat-Shkola, Moscow (2000).
R. P. Balda and A. C. Kamil, “The spatial memory of Clark’s nutcrackers (Nucifraga columbiana) in an analog of the radial-arm maze,” Anim. Learn. Behav., 16, 116–122 (1988).
R. P. Balda and A. C. Kamil, “A comparative study of cache recovery by three corvid species,” Anim. Behav., 38, 486–495 (1989).
R. P. Balda, A. C. Kamil, P. A. Bednekoff, and A. C. Hile, “Species differences in spatial memory performance on a three-dimensional task,” Ethology, 103, 47–55 (1997).
J. A. Basil, A. C. Kamil, R. P. Balda, and F. V. Kite, “Differences in hippocampal volume among food storing corvids,” Brain Behav. Evol., 47, No. 3, 156–164 (1996).
W. W. Beatty and D. A. Shavalia, “Spatial memory in rats: time course of working memory and effect of anesthetics,” Behav. Neural Biol., 28, 454–462 (1980).
K. E. Bell and W. M. Baum, “Group foraging sensitivity to predictable and unpredictable changes in food distribution: past experience or present circumstances?” J. Exptl. Anal. Behav., 78, No. 2, 179–194 (2002).
V. P. Bingman, T. J. Jones, R. Strasser, A. Gagliardo, and P. Ioale, “Homing pigeons, hippocampus and spatial cognition,” in: Behavioural Brain Research in Naturalistic and Semi-Naturalistic Settings: Possibilities and Perspectives, E. Alleva, A. Fasolo, H. P. Lipp, L. Nadel, and L. Ricceri (eds.), Kluwer, Dordrecht (1995), pp. 207–224.
V. P. Bingman, G. E. Hough, M. C. Kahn, and J. J. Siegel, “The homing pigeon hippocampus and space: in search of adaptive specialization,” Brain Behav. Evol., 62, No. 2, 117–127 (2003).
M. E. Bitterman, “Phyletic differences in learning,” Amer. Psychol., 20, 396–410 (1965).
A. B. Bond, R. G. Cook, and M. R. Lamb, “Spatial memory and the performance of rats and pigeons in the radial-arm maze,” Anim. Learn. Behav., 9, No. 4, 575–580 (1981).
A. Brodin and K. Lundborg, “Is hippocampal volume affected by specialization for food hoarding in birds?” Proc. Biol. Sci., 270, No. 1524, 1555–1563 (2003).
M. Colombo, N. J. Broadbent, S. C. Taylor, and N. Frost, “The role of the avian hippocampus in orientation in space and time,” Brain Res., 919, No. 2, 292–301 (2001).
W. E. Crusio, H. Schwegler, and H. P. Lipp, “Radial-maze performance and structural variation of the hippocampus in mice: a correlation with mossy fibre distribution,” Brain Res., 425, No. 1, 182–185 (1987).
R. H. Dale, “Spatial memory in pigeons on a four-arm radial maze,” Can. J. Psychol., 42, No. 1, 78–83 (1988).
W. N. Dember and H. Fowler, “Spontaneous alternation behavior,” Psychol. Bull., 55, 412–428 (1958).
I. Divac, J. Mogensen, and A. Bjorklund, “The prefrontal ‘cortex’ in the pigeon. Biochemical evidence,” Brain Res., 332, No. 2, 365–368 (1985).
P. Ebinger and R. Lohmer, “A volumetric comparison of brains between greylag geese (Anser anser L.) and domestic geese,” J. Hirnforsch., 28, No. 3, 291–299 (1987).
N. J. Emery, “Cognitive ornithology: the evolution of avian intelligence,” Phil. Trans. Roy. Soc. Lond. B. Biol. Sci., 361, No. 1465, 23–43 (2006).
N. J. Emery and N. S. Clayton, “The mentality of crows: convergent evolution of intelligence in corvids and apes,” Science, 306, No. 5703, 1903–1907 (2004).
A. S. Etienne, S. Sitbon, C. Dahn-Hurni, and R. Maurer, “Golden hamsters on the eight-arm maze in light and darkness: the role of dead reckoning,” Q. J. Exptl. Psychol. (B), 47, No. 4, 401–425 (1994).
E. A. Gaffan and J. A. Davies, “The role of exploration in win-shift and win-stay performance on a radial maze,” Learn. Motiv., 12, 282–299 (1981).
A. Gagliardo, M. Mazzotto, and I. Divac, “Memory of radial maze behavior in pigeons after ablations of the presumed equivalent of mammalian prefrontal cortex,” Behav. Neurosci., 111, 955–962 (1997).
L. Z. Garamszegi and M. Eens, “The evolution of hippocampus volume and brain size in relation to food hoarding in birds,” Ecol. Lett., 7, No. 12, 1216–1224 (2004).
D. Goodwin, Pigeons and Doves of the World, British Museum (Natural History) London (1967).
R. L. Gossette, M. F. Gossette, and W. Riddell, “Comparisons of successive discrimination reversal performances among closely and remotely related avian species,” Anim. Behav., 14, No. 4, 560–564 (1966).
K. Gould-Beierle, “A comparison of four corvid species in a working and reference memory task using a radial maze,” J. Comp. Psychol., 114, No. 4, 347–356 (2000).
R. R. Hampton, D. F. Sherry, S. J. Shuttleworth, M. Khurgel, and G. Ivy, “Hippocampal volume and food-storing behavior are related in parids,” Brain Behav. Evol., 45, No. 1, 54–61 (1995).
S. D. Healy and J. R. Krebs, “Development of hippocampal specialization in a food-storing bird,” Behav. Brain Res., 53, No. 1–2, 127–131 (1993).
S. C. Hilton and J. R. Krebs, “Spatial memory of four species of Parus: performance in an open-field analogue of a radial maze,” Q. J. Exptl. Psychol. (B), 42, No. 4, 345–368 (1990).
R. A. Holland, “The role of visual landmarks in the avian familiar area map,” J. Exptl. Biol., 206, No. 11, 1773–1778 (2003).
W. K. Honig, “Studies of working memory in the pigeon,” in: Cognitive Processes in Animal Behavior, S. H. Hulse, H. Fowler, and W. K. Honig (eds.), Erlbaum, Hillsdale, N.J. (1978), pp. 211–248.
S. H. Hulse and D. K. O’Leary, “Serial pattern learning: teaching an alphabet to rats,” J. Exptl. Psychol.: Anim. Behav. Proc., 8, 260–273 (1982).
L. S. Janis, T. W. Bishop, and G. L. Dunbar, “Medial septal lesions in rats produce permanent deficits for strategy selection in a spatial memory task,” Behav. Neurosci., 108, 892–898 (1994).
A. C. Kamil and R. P. Banda, “Cache recovery and spatial memory in Clark’s nutcrackers (Nucifraga columbiana),” J. Exptl. Psychol.: Anim. Behav. Proc., 11, 95–111 (1985).
A. C. Kamil, R. P. Balda, and D. J. Olson, “Performance of four seed-caching corvid species in the radial-arm maze analog,” J. Comp. Psychol., 108, No. 4, 385–393 (1994).
A. C. Kamil and S. I. Yoerg, “Learning and foraging behavior,” Persp. Ethol., 5, 325–346 (1982).
R. P. Kesner, A. A. Chiba, and P. Jackson-Smith, “Rats do show primacy and recency effects in memory for lists of spatial locations: a reply to Gaffan,” Anim. Learn. Behav., 22, 214–218 (1994).
J. R. Krebs, D. F. Sherry, S. D. Healy, V. H. Perry, and A. L. Vaccarino, “Hippocampal specialization of food-storing birds,” Proc. Natl. Acad. Sci. USA, 86, No. 4, 1388–1392 (1989).
L. Lefebvre, P. Whittle, E. Lascaris, and A. Finkelstein, “Feeding innovations and forebrain size in birds,” Anim. Behav., 53, No. 3, 549–560 (1997).
H. P. Lipp, M. G. Pleskacheva, H. Gossweiler, L. Ricceri, A. A. Smirnova, N. N. Garin, O. P. Perepiolkina, D. N. Voronkov, P. A. Kuptsov, and G. Dell’Omo, “A large outdoor radial maze for comparative studies in birds and mammals,” Neurosci. Biobehav. Rev., 25, No. 1, 83–99 (2001).
H. P. Lipp, A. L. Vyssotski, D. P. Wolfer, S. Renaudineau, M. Savini, G. Troster, and G. Dell’Omo, “Pigeon homing along highways and exits,” Curr. Biol., 14, No. 14, 1239–1249 (2004).
J. R. Lucas, A. Brodin, S. R. de Kort, and N. S. Clayton, “Does hippocampal size correlate with the degree of caching specialization?” Proc Biol. Sci., 271, No. 1556, 2423–2429 (2004).
E. M. Macphail, “The role of the avian hippocampus in spatial memory,” Psichologica, 23, 93–108 (2002).
E. F. Meehan, “Effects of MK-801 on spatial memory in homing and nonhoming pigeon breeds,” Behav. Neurosci., 110, No. 6, 1487–1491 (1996).
C. Mettke-Hofmann and E. Gwinner, “Long-term memory for a life on the move,” Proc. Natl. Acad. Sci. USA, 100, No. 10, 5863–5866 (2003).
S. J. Mizumori, M. R. Rozenzweig, and M. G. Kermisch, “Failure of mice to demonstrate spatial memory in the radial maze,” Behav. Neural. Biol., 35, No. 1, 33–45 (1982).
F. R. Moore and T. E. Osadchuk, “Spatial memory in a passerine migrant,” in: Avian Navigation, F. Papi and H. G. Wallraff (eds.), Springer, New York (1982), pp. 319–325.
R. G. Morris, P. Garrud, J. N. Rawlins, and J. O’Keefe, “Place navigation impaired in rats with hippocampal lesions,” Nature, 297, 681–683 (1982).
N. Nikolakakis and L. Lefebvre, “Forebrain size and innovation rate in European birds: feeding, nesting and confounding variables,” Behaviour, 137, 1415–1429 (2000).
J. O’Keefe and L. Nadel, The Hippocampus as a Cognitive Map, Oxford University Press, Oxford (1978).
D. J. Olson, A. C. Kamil, and R. P. Balda, “Effects of response strategy and retention interval on performance of Clark’s nutcrackers in a radial maze analogue,” J. Exptl. Psychol.: Anim. Behav. Proc., 19, No. 2, 138–148 (1993).
D. S. Olton, “Characteristics of spatial memory,” in: Cognitive Processes in Animal Behavior, S. H. Hulse, H. Fowler, and W. K. Honig (eds.), Lawrence Erlbaum Assoc., Hillsdale, N.J. (1978), pp. 341–373.
D. S. Olton, C. Collison, and M. A. Werz, “Spatial memory and radial arm maze performance of rats,” Learn. Motiv., 8, 289–314 (1977).
D. S. Olton, G. E. Handlemann, and J. A. Walker, “Spatial memory and food searching strategies,” in: Foraging Behavior: Ecological, Ethological, and Psychological Approaches, A. C. Kamil and T. D. Sargent (eds.), Garland STPM Press, New York (1981), pp. 333–354.
D. S. Olton and R. J. Samuelson, “Remembrance of places passed: spatial memory in rats,” J. Exptl. Psychol.: Anim. Behav. Proc., 2, 97–116 (1976).
D. S. Olton, J. A. Walker, and W. A. Wolf, “A disconnection analysis of hippocampal function,” Brain Res., 233, 241–253 (1982).
F. Papi, “Recent experiments on pigeon navigation, in: Behavioural Brain Research in Naturalistic and Semi-Naturalistic Settings: Possibilities and Perspectives, E. Alleva, A. Fasolo, H. P. Lipp, L. Nadel, and L. Ricceri (eds.), Kluwer, Dordrecht (1995), pp. 225–238.
M. G. Pleskacheva, G. dell’Omo, P. A. Kuptsov, D. N. Voronkov, N. N. Garin, and H.-P. Lipp, “Domestic birds in a giant radial maze: spatial learning in chickens, guinea fowls and geese,” Soc. Neurosci. Abstr., 27, program No. 536.6, 27 (2001).
M. G. Pleskacheva, P. A. Kuptsov, D. N. Voronkov, G. Dell’Omo, and H.-P. Lipp, “Pigeons in a giant radial maze,” FENS Forum Abstr., 2, A182.10 (2004).
A. Portmann, “Etudes sur la cerebralisation chez les oiseaux. II. Les indices intra-cerebraux,” Alauda, 15, No. 1, 1–15 (1947).
R. W. Powell and W. Kelly, “Responding under positive and negative response contingencies in pigeons and crows,” J. Exptl. Anal. Behav., 25, No. 2, 219–225 (1976).
V. V. Pravosudov and S. R. de Kort, “Is the western scrub-jay (Aphelocoma californica) really an underdog among food-caching corvids when it comes to hippocampal volume and food caching propensity?” Brain Behav. Evol., 67, No. 1, 1–9 (2006).
V. V. Pravosudov, A. S. Kitayski, and A. Omanska, “The relationship between migratory behaviour, memory and the hippocampus: an intraspecific comparison,” Proc. Biol. Sci., 273, No. 1601, 2641–2649 (2006).
H. Prior and O. Gunturkun, “Parallel working memory for spatial location and food-related object cues in foraging pigeons: binocular and lateralized monocular performance,” Learn. Mem., 8, No. 1, 44–51 (2001).
G. Rehkamper, H. Frahm, and M. D. Mann, “Evolutionary constraints of large telencephala,” in: Brain Evolution and Cognition, G. Roth and M. Wulliman (eds.), John Willey and Sons, Spektrum Akad. Verlag, New York, Heidelberg (2001), pp. 49–77.
G. Rehkamper, E. Haase, and H. D. Frahm, “Allometric comparison of brain weight and brain structure volumes in different breeds of the domestic pigeon, Columba livia f.d. (fantails, homing pigeons, strassers),” Brain Behav. Evol., 31, No. 3, 141–149 (1988).
A. Reiner, D. J. Perkel, L. L. Bruce, A. B. Butler, A. Csilag, W. Kuenzel, L. Medina, G. Paxinos, T. Shimizu, G. Striedter, M.Wild, G. F. Ball, S. Durand, O. Gunturkun, D. W. Lee, C. V. Mello, A. Powers, S. A. White, G. Hough, L. Kubikova, T. V. Smulders, K.Wada, J. Dugas-Ford, S. Husband, K. Yamamoto, J. Yu, C. Siang, E. D. Jarvis, and O. Gunturkun, “Revised nomenclature for avian telencephalon and some related brainstem nuclei,” J. Comp. Neurol., 473, No. 3, 377–414 (2004).
W. A. Roberts and R. H. I. Dale, “Remembrance of place lasts: Proactive inhibition and pattern of choice in rat spatial memory,” Learn. Motiv., 12, 261–281 (1981).
W. A. Roberts and D. S. Grant, “Studies of short-term memory in the pigeon using the delayed matching-to-sample procedure,” in: Processes of Animal Memory, D. L. Medin, W. A. Roberts, and R. T. Davis (eds.), Lawrence Erlbaum Assoc., Hillsdale, New Jersey (1976), pp. 79–112.
W. A. Roberts and W. E. Smythe, “Memory for lists of spatial events in the rat,” Learn. Motiv., 10, 313–336 (1979).
W. A. Roberts and N. Van Veldhuizen, “Spatial memory in pigeons on the radial maze,” J. Exptl. Psychol.: Anim. Behav. Proc., 11, No. 2, 241–260 (1985).
H. L. Roitblat, W. Tham, and L. Golub, “Performance of Betta splendens in a radial arm maze,” Anim. Learn. Behav., 10, 108–114 (1982).
P. Roullet and J. M. Lassalle, “Radial maze learning using exclusively distant visual cues reveals learners and nonlearners among inbred mouse strains,” Physiol. Behav., 58, No. 6, 1189–1195 (1995).
S. J. Shettleworth, “Learning and behavioural ecology,” in: Behavioural Ecology: An Evolutionary Approach, J. R. Krebs and N. Davis (eds.), Blackwell Scientific, Oxford (1994), pp. 170–194.
B. F. Skinner, “Autoshaping,” Science, 173, No. 998, 752–753 (1971).
M. L. Spetch and C. A. Edwards, “Spatial memory in pigeons (Columba livia) in an open-field feeding environment,” J. Comp. Psychol., 100, 266–278 (1986).
M. L. Spetch and W. K. Honig, “Characteristics of pigeons’ spatial working memory in an open-field task,” Anim. Learn. Behav., 16, 123–131 (1988).
B. L. Stafford, R. P. Balda, and A. C. Kamil, “Does seed-caching experience affect spatial memory performance by pinyon jays?” Ethology, 112, No. 12, 1202–1208 (2006).
T. A. Stevens and J. R. Krebs, “Retrieval of stored food by marsh tits Parus palustris in the field,” Ibis, 128, 513–525 (1986).
S. Timmermans, L. Lefebvre, D. Boire, and P. Basu, “Relative size of the hyperstriatum ventrale is the best predictor of feeding innovation rate in birds,” Brain Behav. Evol., 56, No. 4, 196–203 (2000).
S. V. Vander Wall and R. P. Balda, “Ecology and evolution of foodstorage behavior in conifer-seed-caching corvids,” Z. Tierpsychol., 56, 217–242 (1981).
S. B. Vander Wall and H. E. Hutchins, “Dependence of Clark’s nutcracker, Nucifraga columbiana, on conifer seeds during the postfledging period,” Can. Field Naturalist, 97, 208–214 (1983).
H. G. Wallraff, “Navigation by homing pigeon: updated perspective,” Ethol. Ecol. Evol., 13, No. 1, 1–48 (2001).
D. M. Wilkie and P. Slobin, “Gerbils in space: performance on the 17-arm radial maze,” J. Exptl. Anal. Behav., 40, No. 3, 301–312 (1983).
D. M. Wilkie, M. L. Spetch, and L. Chew, “The ring dove’s shortterm memory capacity for spatial information,” Anim. Behav., 29, 639–641 (1981).
B. J. Wilson, N. J. Macintosh, and R. A. Boakes, “Transfer of relational rules in matching and oddity learning by pigeons and corvids,” Q. J. Exptl. Psychol (B), 37, 313–332 (1985).
R. Wiltschko and W. Wiltschko, “Avian navigation: from historical to modern concepts,” Anim. Behav., 65, No. 2, 257–272 (2003).
L. Zoladek and W. A. Roberts, “The sensory basis of spatial memory in the rat,” 6, 77–81 (1978).
Z. A. Zorina, Reasoning in Birds, Overseas Publ. Assoc., Amsterdam (1997), pp. 1–47.
Author information
Authors and Affiliations
Corresponding author
Additional information
Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 58, No. 4, pp. 389–407, July–August, 2008.
Rights and permissions
About this article
Cite this article
Pleskacheva, M.G. Behavior and Spatial Learning in Radial Mazes in Birds. Neurosci Behav Physi 39, 725–739 (2009). https://doi.org/10.1007/s11055-009-9199-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11055-009-9199-2