Serial reversal learning and the evolution of behavioral flexibility in three species of North American corvids (Gymnorhinus cyanocephalus, Nucifraga columbiana, Aphelocoma californica).

In serial reversal learning, subjects learn to respond differentially to 2 stimuli. When the task is fully acquired, reward contingencies are reversed, requiring the subject to relearn the altered associations. This alternation of acquisition and reversal can be repeated many times, and the ability of a species to adapt to this regimen has been considered as an indication of behavioral flexibility. Serial reversal learning of 2-choice discriminations was contrasted in 3 related species of North American corvids: pinyon jays (Gymnorhinus cyanocephalus), which are highly social; Clark's nutcrackers (Nucifraga columbiana), which are relatively solitary but specialized for spatial memory; and western scrub jays (Aphelocoma californica), which are ecological generalists. Pinyon jays displayed significantly lower error rates than did nutcrackers or scrub jays after reversal of reward contingencies for both spatial and color stimuli. The effect was most apparent in the 1st session following each reversal and did not reflect species differences in the rate of initial discrimination learning. All 3 species improved their performance over successive reversals and showed significant transfer between color and spatial tasks, suggesting a generalized learning strategy. The results are consistent with an evolutionary association between behavioral flexibility and social complexity.

[1]  Guillermo Paz-y-Miño C,et al.  Pinyon jays use transitive inference to predict social dominance , 2004, Nature.

[2]  D. Crews,et al.  Spatial and reversal learning in congeneric lizards with different foraging strategies , 1999, Animal Behaviour.

[3]  D. Leger Comparative perspectives in modern psychology. , 1987, Nebraska Symposium on Motivation. Nebraska Symposium on Motivation.

[4]  L. Day,et al.  Use of position and feature cues in discrimination learning by the whiptail lizard (Cnemidophorus inornatus). , 2003, Journal of comparative psychology.

[5]  David W. Bessemer,et al.  Retention of Discriminations and an Analysis of Learning Set , 1971 .

[6]  K. Strier Behavioral Flexibility in Primates. Causes and Consequences , 2006, International journal of primatology.

[7]  M. Bitterman THE EVOLUTION OF INTELLIGENCE. , 1965, Scientific American.

[8]  J. Warren Reversal learning and the formation of learning sets by cats and rhesus monkeys. , 1966, Journal of Comparative and Physiological Psychology.

[9]  Performance of Four Seed-Caching Corvid Species in the Radial-Arm Maze Analog , 1994 .

[10]  B. Doty,et al.  Reversal Learning of Object and Positional Discriminations by Mink, Ferrets and Skunks , 1969 .

[11]  Phyllis C. Lee The Genesis of Animal Play. Testing the Limits, Gordon M. Burghardt. J. Wiley, Chichester (2005), Pp. xvi+501. Price £32.95 , 2005 .

[12]  N. Mackintosh,et al.  Factors underlying improvement in serial reversal learning. , 1968, Canadian journal of psychology.

[13]  A. Bond,et al.  Kea, Bird of Paradox: The Evolution and Behavior of a New Zealand Parrot , 1999 .

[14]  W. J. Carmen,et al.  Noncooperative breeding in the California scrub-jay , 2004 .

[15]  Warren Jm Reversal learning and the formation of learning sets by cats and rhesus monkeys. , 1966 .

[16]  Tf Voogd,et al.  Animal Cognition in Nature , 1998 .

[17]  M. Bitterman PHYLETIC DIFFERENCES IN LEARNING. , 1965, The American psychologist.

[18]  B. Gibson,et al.  The fine-grained spatial abilities of three seed-caching corvids , 2005, Learning & behavior.

[19]  D. Evans,et al.  Book Reviews: Insect Defenses. Adaptive Mechanisms and Strategies of Prey and Predators. , 1990 .

[20]  Daniel Sol,et al.  Behavioural flexibility and invasion success in birds , 2002, Animal Behaviour.

[21]  L. Lefebvre,et al.  Positive and negative correlates of feeding innovations in birds: evidence for limited modularity , 2003 .

[22]  E Stüssi [Biomechanics in sports]. , 1989, Schweizerische Rundschau fur Medizin Praxis = Revue suisse de medecine Praxis.

[23]  A. Bond,et al.  Social complexity and transitive inference in corvids , 2003, Animal Behaviour.

[24]  D. Upton The Management of Manufacturing Flexibility , 1994 .

[25]  Robin I. M. Dunbar,et al.  Both social and ecological factors predict ungulate brain size , 2006, Proceedings of the Royal Society B: Biological Sciences.

[26]  N. Mackintosh The psychology of animal learning , 1974 .

[27]  PETER A BEDNEKOFF,et al.  Clark's nutcracker spatial memory: many errors might not be due to forgetting , 1997, Animal Behaviour.

[28]  B. Monroe,et al.  A World Checklist of Birds , 1993 .

[29]  A. Townsend Peterson,et al.  Western Scrub-Jay (Aphelocoma californica) , 2002 .

[30]  N. Emery,et al.  The cognitive neuroscience of social behaviour , 2005 .

[31]  J. Warren THE COMPARATIVE PSYCHOLOGY OF LEARNING. , 1965, Annual review of psychology.

[32]  P. Godfrey‐Smith Environmental complexity and the evolution of cognition. , 2002 .

[33]  K. Breland,et al.  The misbehavior of organisms. , 1961 .

[34]  Morten L Kringelbach,et al.  Neural correlates of rapid reversal learning in a simple model of human social interaction , 2003, NeuroImage.

[35]  Serial reversal training and nonreversal shift learning. , 1969, Journal of comparative and physiological psychology.

[36]  E. Bernays,et al.  Insect Defenses: Adaptive Mechanisms and Strategies of Prey and Predators , 1991 .

[37]  S. Baird,et al.  The birds of North America , 1974 .

[38]  A. Kamil,et al.  A synthetic approach to the study of animal intelligence. , 1987, Nebraska Symposium on Motivation. Nebraska Symposium on Motivation.

[39]  A C Kamil,et al.  Performance of four seed-caching corvid species in operant tests of nonspatial and spatial memory. , 1995, Journal of comparative psychology.

[40]  Charles H. Southwick,et al.  Behavior of Nonhuman Primates , 1966, The Yale Journal of Biology and Medicine.

[41]  W. Robinson Predator-prey interactions, informational complexity, and the origins of intelligence , 1985 .

[42]  N. Mackintosh,et al.  Transfer of Serial Reversal Learning in the Pigeon , 1986 .

[43]  A. Kamil,et al.  Positive transfer from successive reversal training to learning set in Blue Jays (Cyanocitta cristata) , 1977 .

[44]  R. Quesada,et al.  Espinosa de los monteros , 2000 .

[45]  Jody L. Lewis,et al.  Interference effects in the memory for serially presented locations in Clark's nutcrackers, Nucifraga columbiana. , 2006, Journal of experimental psychology. Animal behavior processes.

[46]  J. E. Mazur,et al.  Learning and Behavior , 1966 .

[47]  HighWire Press Philosophical Transactions of the Royal Society of London , 1781, The London Medical Journal.

[48]  A. Easton Behavioural flexibility, social learning, and the frontal cortex. , 2005 .

[49]  J. Cracraft,et al.  Intergeneric relationships of the new world Jays inferred from cytochrome b gene sequences , 1997 .

[50]  P. Bednekoff,et al.  Long-term spatial memory in four seed-caching corvid species , 1997, Animal Behaviour.

[51]  Marcel Eens,et al.  The evolution of hippocampus volume and brain size in relation to food hoarding in birds , 2004 .

[52]  O. Güntürkün,et al.  Selective deficits in reversal learning after neostriatum caudolaterale lesions in pigeons: Possible behavioral equivalencies to the mammalian prefrontal system , 1998, Behavioural Brain Research.

[53]  K. Armitage,et al.  Life history consequences of social complexity a comparative study of ground-dwelling sciurids , 1998 .

[54]  E. Wasserman,et al.  Comparative cognition : experimental explorations of animal intelligence , 2009 .

[55]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.

[56]  The Neural Basis of Cognitive Flexibility in Birds , 2009 .

[57]  S. Shettleworth Cognition, evolution, and behavior , 1998 .

[58]  G. Keppel,et al.  Design and Analysis: A Researcher's Handbook , 1976 .

[59]  E. Martins The Comparative Method in Evolutionary Biology, Paul H. Harvey, Mark D. Pagel. Oxford University Press, Oxford (1991), vii, + 239 Price $24.95 paperback , 1992 .

[60]  Cecilia Heyes,et al.  Evolution of Cognition , 2001 .

[61]  L. Lefebvre,et al.  Brains, Innovations and Evolution in Birds and Primates , 2004, Brain, Behavior and Evolution.

[62]  K. Laland,et al.  Animal innovation: An introduction. , 2003 .

[63]  L. Lefebvre,et al.  Relative Size of the Hyperstriatum ventrale Is the Best Predictor of Feeding Innovation Rate in Birds , 2000, Brain, Behavior and Evolution.

[64]  N. Emery Cognitive ornithology: the evolution of avian intelligence , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[65]  A. Kamil,et al.  The Ecology and Evolution of Spatial Memory in Corvids of the Southwestern USA: The Perplexing Pinyon Jay , 1998 .

[66]  O. Güntürkün,et al.  Impaired learning of a color reversal task after NMDA receptor blockade in the pigeon (Columba livia) associative forebrain (neostriatum caudolaterale). , 2002, Behavioral neuroscience.