Animal Cognition

, Volume 16, Issue 3, pp 445–458 | Cite as

Automated cognitive testing of monkeys in social groups yields results comparable to individual laboratory-based testing

  • Regina Paxton GazesEmail author
  • Emily Kathryn Brown
  • Benjamin M. Basile
  • Robert R. Hampton
Original Paper


Cognitive abilities likely evolved in response to specific environmental and social challenges and are therefore expected to be specialized for the life history of each species. Specialized cognitive abilities may be most readily engaged under conditions that approximate the natural environment of the species being studied. While naturalistic environments might therefore have advantages over laboratory settings for cognitive research, it is difficult to conduct certain types of cognitive tests in these settings. We implemented methods for automated cognitive testing of monkeys (Macaca mulatta) in large social groups (Field station) and compared the performance to that of laboratory-housed monkeys (Laboratory). The Field station animals shared access to four touch-screen computers in a large naturalistic social group. Each Field station subject had an RFID chip implanted in each arm for computerized identification and individualized assignment of cognitive tests. The Laboratory group was housed and tested in a typical laboratory setting, with individual access to testing computers in their home cages. Monkeys in both groups voluntarily participated at their own pace for food rewards. We evaluated performance in two visual psychophysics tests, a perceptual classification test, a transitive inference test, and a delayed matching-to-sample memory test. Despite the differences in housing, social environment, age, and sex, monkeys in the two groups performed similarly in all tests. Semi-free ranging monkeys living in complex social environments are therefore viable subjects for cognitive testing designed to take advantage of the unique affordances of naturalistic testing environments.


Transitive inference Memory Classification Psychophysics Rhesus macaque Social housing RFID 



The Yerkes National Primate Research Center is fully accredited by the American Association for Accreditation of Laboratory Animal Care. This project was funded by the National Center for Research Resources P51RR165, currently supported by the Office of Research Infrastructure Programs/OD P51OD11132, the Center for Behavioral Neuroscience under the STC Program of the NSF under Agreement IBN-9876754, a grant from the James S. McDonnell Foundation, NIH grant R01MH082819, NSF grants 0745573 and 1146316. Regina Paxton Gazes was supported in part by the National Science Foundation grant DGE-0231900 and by Zoo Atlanta. We thank Dina P. Chou, Steven R.L. Sherrin, Jacey Jones, and Angela Tripp for help testing subjects. We thank Tom Hassett for help collecting dominance hierarchy data on Field station subjects, and the colony management and veterinary staff of the Yerkes Field Station for their gracious support of this work.


  1. Adachi I, Chou DP, Hampton RR (2009) Thatcher effect in monkeys demonstrates conservation of face perception across primates. Curr Biol 19(15):1270–1273PubMedCrossRefGoogle Scholar
  2. Andrews MW, Rosenblum LA (1994) Automated recording of individual performance and hand preference during joystick task acquisition in group-living bonnet macaques (Macaca radiata). J Comp Psychol 108:358–362PubMedCrossRefGoogle Scholar
  3. Aron A, Aron E (1999) Statistics for Psychology. Prentice Hall, Upper Saddle RiverGoogle Scholar
  4. Barbet I, Fagot J (2011) Processing of contour closure by baboons (Papio papio). J Exp Psychol Anim Behav Process 3:407–419CrossRefGoogle Scholar
  5. Basile BM, Hampton RR (2010) Rhesus monkeys (Macaca mulatta) show robust primacy and recency in memory for lists from small, but not large, image sets. Behav Proc 83:183–190CrossRefGoogle Scholar
  6. Basile BM, Hampton RR (2011) Monkeys recall and reproduce simple shapes from memory. Curr Biol 21(9):774–778PubMedCrossRefGoogle Scholar
  7. Basile BM, Hampton RR (2012) Dissociation of active working memory and passive recognition in rhesus monkeys. Cognition. doi: 10.1016/j.cognition.2012.10.012
  8. Bergman TJ, Beehner JC, Cheney DL, Seyfarth RM (2003) Hierarchical classification by rank and kinship in baboons. Science 302:1234–1236PubMedCrossRefGoogle Scholar
  9. Bernstein IS (1970) Primate status hierarchies. In: Rosenblum LA (ed) Primate behavior. Academic Press, New YorkGoogle Scholar
  10. Biben M, Bernhards D (1994) Naive recognition of chuck calls in squirrel monkeys (Saimiri sciureus macrodon). Lang Commun 14:167–181CrossRefGoogle Scholar
  11. Biondi LM, Bo MS, Vassallo AI (2010) Inter-individual and age differences in exploration, neophobia and problem-solving ability in a Neotropical raptor (Milvago chimango). Anim Cogn 15:701–710CrossRefGoogle Scholar
  12. Bond A, Wei CA, Kamil AC (2010) Cognitive representation in transitive inference: a comparison of four corvid species. Behav Process 85:283–292CrossRefGoogle Scholar
  13. Bonte E, Flemming T, Fagot J (2011) Executive control of perceptual features and abstract relations by baboons (Papio papio). Behav Brain Res 222:176–182PubMedCrossRefGoogle Scholar
  14. Cheney DL, Seyfarth RM (1982) Recognition of individuals within and between groups of free-ranging vervet monkeys. Am Zool 22:519–529Google Scholar
  15. Cheney DL, Seyfarth RM (1999) Recognition of other individuals’ social relationships by female baboons. Anim Behav 58:67–75PubMedCrossRefGoogle Scholar
  16. D’Amato MR, Van Sant P (1988) The person concept in monkeys (Cebus apella). J Exper Psychol Anim Behav Process 14:43–55CrossRefGoogle Scholar
  17. De Vries H, Appleby MC (2000) Finding an appropriate order for a hierarchy: a comparison of the I&SI and the BBS methods. Anim Behav 59:239–245PubMedCrossRefGoogle Scholar
  18. Drea CM (1998) Social context affects how rhesus monkeys explore their environment. Am J Primatol 44:205–214PubMedCrossRefGoogle Scholar
  19. Drea CM, Wallen K (1999) Low-status monkeys “play dumb” when learning in mixed social groups. Proc Nat Acad Sci 96:12965–12969PubMedCrossRefGoogle Scholar
  20. Fagot J, Bonte E (2010) Automated testing of cognitive performance in monkeys: use of a battery of computerized test systems by a troop of semi-free-ranging baboons (Papio papio). Behav Res Methods 42:507–516PubMedCrossRefGoogle Scholar
  21. Fagot J, De Lillo C (2011) A computerized study of working memory: immediate serial spatial recall in baboons (Papio papio) and humans. Neuropsychologia 49:3870–3880PubMedCrossRefGoogle Scholar
  22. Fagot J, Paleressompoulle D (2009) Automatic testing of cognitive performance in baboons maintained in social groups. Behav Res Methods 41:396–404PubMedCrossRefGoogle Scholar
  23. Fagot J, Thompson RKR (2011) Generalized relational matching by guinea baboons (Papio papio) in two-by-two-item analogy problems. Psychol Sci 22(10):1304–1309PubMedCrossRefGoogle Scholar
  24. Fischer J (2004) Emergence of individual recognition in young macaques. Anim Behav 67:655–661CrossRefGoogle Scholar
  25. Gazes RP, Hampton RR, Chee NW (2012) Cognitive mechanisms for transitive inference performance in rhesus monkeys: measuring the influence of associative strength and inferred order. J Exp Psychol Anim Behav Process 38(4):331–345PubMedCrossRefGoogle Scholar
  26. Gersick AS, Snyder-Mackler N, White DJ (2012) Ontogeny of social skills: social complexity improves mating and competitive strategies in male brown-headed cowbirds. Anim Behav 83:1171–1177CrossRefGoogle Scholar
  27. Glickman SE, Sroges RW (1966) Curiosity in zoo animals. Behavior 26:151–188CrossRefGoogle Scholar
  28. Grainger J, Dufau S, Montant M, Ziegler JC, Fagot J (2012) Orthographic processing in baboons (Papio papio). Science 336:245–248PubMedCrossRefGoogle Scholar
  29. Grosenick L, Clement TS, Fernald RD (2007) Fish can infer social rank by observation alone. Nature 445:429–432PubMedCrossRefGoogle Scholar
  30. Hasset JM, Martin-Malivel J, Lange H, Fischer A, Wallen K (2007) Age and rank influences on access to an automated system for cognitive testing in socially housed rhesus monkeys Paper presented at the International Conference on Comp Cogn, Melbourne, FLGoogle Scholar
  31. Henderson J, Hurly TA, Healy SD (2001) Rufous hummingbirds’ memory for flower location. Anim Behav 61:981–986CrossRefGoogle Scholar
  32. Lazareva OF, Smirnova AA, Bagozkaja MS, Zorina ZA, Rayevsky VV, Wasserman EA (2004) Transitive responding in hooded crows requires linearly ordered stimuli. J Exp Anal Behav 82:1–19PubMedCrossRefGoogle Scholar
  33. Logie RH (1986) Visuo-spatial processing in working memory. Q J Exp Psychol Sec A 38:229–247CrossRefGoogle Scholar
  34. MacLean EL, Merritt DJ, Brannon EM (2007) Transitive inference in two species of prosimian primates. Am J Primatol 69:102Google Scholar
  35. McGonigle BO, Chalmers M (1977) Are monkeys logical. Nature 267:694–696PubMedCrossRefGoogle Scholar
  36. Mishkin M, Murray E (1998) Object recognition and location memory in monkeys with excitotoxic lesions of the amygdala and hippocampus. J Neurosci 18(16):6568–6582PubMedGoogle Scholar
  37. Morand-Ferron J, Cole EF, Rawles JEC, Quinn JL (2011) Who are the innovators? A field experiment with 2 passerine species. Behav Ecol 22:1241–1248CrossRefGoogle Scholar
  38. Paxton R, Basile BM, Adachi I, Suzuki WA, Wilson M, Hampton RR (2010) Rhesus monkeys (Macaca mulatta) rapidly learn to select dominant individuals in videos of artificial social interactions between unfamiliar conspecifics. J Comp Psychol 124(4):395–401PubMedCrossRefGoogle Scholar
  39. Phillips WA, Christie DFM (1977) Interference with visualization. Q J Exp Psychol 29:637–650PubMedCrossRefGoogle Scholar
  40. Piaget J (1960) Logic and Psychology. Basic Books, Inc., New YorkGoogle Scholar
  41. Rapp PR, Kansky MT, Eichenbaum H (1996) Learning and memory for hierarchical relationships in the monkey: effects of aging. Behav Neurosci 110(5):887–897PubMedCrossRefGoogle Scholar
  42. Roberts WA, Phelps MT (1994) Transitive inference in rats: a test of the spatial coding hypothesis. Psychol Sci 5:368–374CrossRefGoogle Scholar
  43. Rommeck I, Capitanio JP, Strand SC, McCowan B (2011) Early social experience affects behavioral and physiological responsiveness to stressful conditions in infant rhesus macaques (Macaca mulatta). Am J Primatol 73:692–701PubMedCrossRefGoogle Scholar
  44. Schrier AM, Brady PM (1987) Categorization of natural stimuli by monkeys (Macaca mulatta): effects of stimulus set size and modification of exemplars. J Exp Psychol Anim Behav Process 13:136–143PubMedCrossRefGoogle Scholar
  45. Schrier AM, Angarella R, Povar ML (1984) Studies of concept formation by stumptailed monkeys: concepts humans, monkeys, and letter A. J Exp Psychol Anim Behav Process 10:564–584CrossRefGoogle Scholar
  46. Schwandt ML, Lindell SG, Sjoberg RL, Chisholm KL, Higley JD, Suomi SJ et al (2010) Gene-environment interactions and response to social intrusion in male and female rhesus macaques. Biol Psychiatr 67:323–330CrossRefGoogle Scholar
  47. Shettleworth SJ (2009) Cognition, evolution, and behavior, 2nd edn. Oxford University Press, New YorkGoogle Scholar
  48. Templer VL, Hampton RR (2012) Rhesus monkeys (Macaca mulatta) show robust evidence for memory awareness across multiple generalization tests. Anim Cogn 15:409–415PubMedCrossRefGoogle Scholar
  49. Treichler FR, Raghanti MA (2010) Serial list combination by monkeys (Macaca mulatta): test cues and linking. Anim Cogn 13:121–131PubMedCrossRefGoogle Scholar
  50. Treichler FR, Van Tilburg D (1996) Concurrent conditional discrimination tests of transitive inference by macaque monkeys: list linking. J Exper Psychol Anim Behav Proc 22:105–117CrossRefGoogle Scholar
  51. Tu HW, Hampton RR (2012) One-trial memory and habit contribute independently to matching-to-sample performance in rhesus monkeys (Macaca mulatta). J Comp Psychol. doi:  10.1037/a0030496
  52. Von Fersen L, Wynne CDL, Delius JD, Staddon JER (1991) Transitive inference formation in pigeons. J Exp Psychol Anim Behav Process 17:334–341CrossRefGoogle Scholar
  53. Washburn DA, Astur RS (1998) Nonverbal working memory of humans and monkeys: rehearsal in the sketchpad? Mem Cogn 26:277–286CrossRefGoogle Scholar
  54. Weiß BM, Kehmeier S, Schloegl C (2010) Transitive inference in free-living greylag geese, Anser anser. Anim Behav 79:1277–1283CrossRefGoogle Scholar
  55. White DJ, Gersick AS, Freed-Brown G, Snyder-Mackler N (2010) The ontogeny of social skills: experimental increases in social complexity enhance reproductive success in adult cowbirds. Anim Behav 79:385–390CrossRefGoogle Scholar
  56. White DJ, Gersick AS, Snyder-Mackler N (2012) Social networks and the development of social skills in cowbirds. Philos Trans R Soc B Biol Sci 367:1892–1900CrossRefGoogle Scholar
  57. Windfelder TL (2001) Interspecific communication in mixed-species groups of tamarins: evidence from playback experiments. Anim Behav 61:1193–1201CrossRefGoogle Scholar
  58. Wright AA, Urcuioli RJ, Sands SF (1986) Proactive interference in animal memory. In: Kendrick DF, Riling M, Denny R (eds) Theories of animal memory. Earlbaum, Hillsdale, pp 101–125Google Scholar
  59. Zuberbuhler K, Cheney DL, Seyfarth RM (1999) Conceptual semantics in a nonhuman primate. J Comp Psychol 113:33–42CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Regina Paxton Gazes
    • 1
    • 2
    Email author
  • Emily Kathryn Brown
    • 2
  • Benjamin M. Basile
    • 2
  • Robert R. Hampton
    • 2
  1. 1.AtlantaUSA
  2. 2.Department of Psychology and Yerkes National Primate Research CenterEmory UniversityAtlantaUSA

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