Animal Cognition

, Volume 22, Issue 3, pp 331–341 | Cite as

Dissociation of memory signals for metamemory in rhesus monkeys (Macaca mulatta)

  • Emily Kathryn BrownEmail author
  • Benjamin M. Basile
  • Victoria L. Templer
  • Robert R. Hampton
Original Paper


Some nonhuman species demonstrate metamemory, the ability to monitor and control memory. Here, we identify memory signals that control metamemory judgments in rhesus monkeys by directly comparing performance in two metamemory paradigms while holding the availability of one memory signal constant and manipulating another. Monkeys performed a four-choice match-to-sample memory task. In Experiment 1, monkeys could decline memory tests on some trials for a small, guaranteed reward. In Experiment 2, monkeys could review the sample on some trials. In both experiments, monkeys improved accuracy by selectively declining tests or reviewing samples when memory was poor. To assess the degree to which different memory signals made independent contributions to the metamemory judgement, we made the decline-test or review-sample response available either prospectively, before the test, or concurrently with test stimuli. Prospective metamemory judgements are likely controlled by the current contents of working memory, whereas concurrent metamemory judgements may also be controlled by additional relative familiarity signals evoked by the sight of the test stimuli. In both paradigms, metacognitive responding enhanced accuracy more on concurrent than on prospective tests, suggesting additive contributions of working memory and stimulus-evoked familiarity. Consistent with the hypothesis that working memory and stimulus-evoked familiarity both control metamemory judgments when available, metacognitive choice latencies were longer in the concurrent condition, when both were available. Together, these data demonstrate that multiple memory signals can additively control metacognitive judgements in monkeys and provide a framework for mapping the interaction of explicit memory signals in primate memory.


Metacognition Information seeking Monitoring Working memory Familiarity 



We thank Steven L. Sherrin, Jessica A. Joiner, and Tara A. Dove-VanWormer for assistance with testing animals.


This work was supported by the National Science Foundation (Grants IOS-1146316; BCS-0745573; BCS-1632477) and the National Institutes of Health (Grants RO1MH082819; T32HD071845). This project was supported in part by ORIP/OD P51OD011132.

Compliance with ethical standards

Conflict of interest

All authors declare no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.


  1. Baddeley A (2000) The episodic buffer: a new component of working memory? Trends Cogn Sci 4:417–423CrossRefPubMedGoogle Scholar
  2. Baddeley A (2003) Working memory: looking back and looking forward. Nat Rev Neurosci 4:829CrossRefPubMedGoogle Scholar
  3. Basile BM, Hampton RR (2013) Dissociation of active working memory and passive recognition in rhesus monkeys. Cognition 126:391–396CrossRefPubMedGoogle Scholar
  4. Basile BM, Hampton RR, Suomi SJ, Murray EA (2009) An assessment of memory awareness in tufted capuchin monkeys (Cebus apella). Anim Cogn 12:169–180CrossRefPubMedGoogle Scholar
  5. Basile BM, Schroeder GR, Brown EK, Templer VL, Hampton RR (2015) Evaluation of seven hypotheses for metamemory performance in rhesus monkeys. J Exp Psychol Gen 144:85CrossRefPubMedGoogle Scholar
  6. Beran MJ, Smith JD (2011) Information seeking by rhesus monkeys (Macaca mulatta) and capuchin monkeys (Cebus apella). Cognition 120:90–105. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Brown EK, Templer VL, Hampton RR (2017) An assessment of domain-general metacognitive responding in rhesus monkeys. Behav Process 135:132–144CrossRefGoogle Scholar
  8. Call J, Carpenter M (2001) Do apes and children know what they have seen? Anim Cogn 4:207–220CrossRefGoogle Scholar
  9. Carruthers P (2008) Meta-cognition in animals: a skeptical look. Mind Lang 23:58–89CrossRefGoogle Scholar
  10. Castro L, Wasserman EA (2013) Information-seeking behavior: exploring metacognitive control in pigeons. Anim Cogn 16:241–254. CrossRefPubMedGoogle Scholar
  11. Couchman JJ, Coutinho MV, Beran MJ, Smith JD (2010) Beyond stimulus cues and reinforcement signals: a new approach to animal metacognition. J Comp Psychol 124:356CrossRefPubMedPubMedCentralGoogle Scholar
  12. Coutinho MV, Redford JS, Church BA, Zakrzewski AC, Couchman JJ, Smith JD (2015) The interplay between uncertainty monitoring and working memory: can metacognition become automatic? Mem Cogn 43:990–1006CrossRefGoogle Scholar
  13. Flavell JH (1979) Meta-cognition and cognitive monitoring - new area of cognitive-developmental. Inq Am Psychol 34:906–911CrossRefGoogle Scholar
  14. Fujita K (2009) Metamemory in tufted capuchin monkeys (Cebus apella). Anim Cogn 12:575CrossRefPubMedGoogle Scholar
  15. Hampton RR (2001) Rhesus monkeys know when they remember. Proc Natl Acad Sci USA 98:5359–5362. CrossRefPubMedGoogle Scholar
  16. Hampton RR (2009) Multiple demonstrations of metacognition in nonhumans: converging evidence or multiple mechanisms? Comp Cogn Behav Rev 4:17PubMedPubMedCentralGoogle Scholar
  17. Iwasaki S, Watanabe S, Fujita K (2013) Do pigeons (Columba livia) seek information when they have insufficient knowledge? Anim Cogn 16:211–221CrossRefPubMedGoogle Scholar
  18. Jacoby LL (1991) A process dissociation framework: separating automatic from intentional uses of memory. J Mem Lang 30(5):513–541CrossRefGoogle Scholar
  19. Jozefowiez J, Staddon J, Cerutti D (2009) Metacognition in animals: how do we know that they know? Comp Cogn Behav Rev 4:54–55Google Scholar
  20. Keppel G, Wickens TD (2004) Design and analysis: a researcher’s handbook. Prentice Hall, New YorkGoogle Scholar
  21. Kirk CR, McMillan N, Roberts WA (2014) Rats respond for information: metacognition in a rodent? J Exp Psychol Anim Learn Cogn 40:249CrossRefPubMedGoogle Scholar
  22. Kornell N (2013) Where is the “meta” in animal metacognition? J Comp Psychol 128:143–149CrossRefPubMedGoogle Scholar
  23. Kornell N, Son LK, Terrace HS (2007) Transfer of metacognitive skills and hint seeking in monkeys. Psychol Sci 18:64–71. CrossRefPubMedGoogle Scholar
  24. Le Pelley M (2012) Metacognitive monkeys or associative animals? Simple reinforcement learning explains uncertainty in nonhuman animals. J Exp Psychol Learn Mem Cogn 38:686CrossRefPubMedGoogle Scholar
  25. Maniscalco B, Lau H (2012) A signal detection theoretic approach for estimating metacognitive sensitivity from confidence ratings. Conscious Cogn 21:422–430CrossRefPubMedGoogle Scholar
  26. Marsh HL (2014) Metacognitive-like information seeking in lion-tailed macaques: a generalized search response after all? Anim Cogn 17:1313–1328CrossRefPubMedGoogle Scholar
  27. Marsh HL, MacDonald SE (2012) Information seeking by orangutans: a generalized search strategy? Anim Cogn 15:293–304CrossRefPubMedGoogle Scholar
  28. McMahon S, Macpherson K, Roberts WA (2010) Dogs choose a human informant: metacognition in canines. Behav Process 85:293–298. CrossRefGoogle Scholar
  29. Nelson TO (1996) Consciousness metacognition. Am Psychol 51:102–116CrossRefGoogle Scholar
  30. Sherry DF, Schacter DL (1987) The evolution of multiple memory. Syst Psychol Rev 94:439–454CrossRefGoogle Scholar
  31. Smith JD, Beran MJ, Redford JS, Washburn DA (2006) Dissociating uncertainty responses and reinforcement signals in the comparative study of uncertainty monitoring. J Exp Psychol Gen 135:282CrossRefPubMedGoogle Scholar
  32. Smith JD, Coutinho MV, Church BA, Beran MJ (2013) Executive-attentional uncertainty responses by rhesus macaques (Macaca mulatta). J Exp Psychol Gen 142:458CrossRefPubMedGoogle Scholar
  33. Squire LR, Zola-Morgan S (1991) The medial temporal lobe. Mem Syst Sci 253:1380–1386Google Scholar
  34. Suda-King C (2008) Do orangutans (Pongo pygmaeus) know when they do not remember? Anim Cogn 11:21–42. CrossRefPubMedGoogle Scholar
  35. Suda-King C, Bania AE, Stromberg EE, Subiaul F (2013) Gorillas’ use of the escape response in object choice memory tests. Anim Cogn 16:65–84. CrossRefPubMedGoogle Scholar
  36. Takagi S, Fujita K (2018) Do capuchin monkeys (Sapajus apella) know the contents of memory traces? A study of metamemory for compound stimuli. J Comp Psychol 132:88CrossRefPubMedGoogle Scholar
  37. Templer VL, Hampton RR (2012) Rhesus monkeys (Macaca mulatta) show robust evidence for memory awareness across multiple generalization tests. Anim Cogn 15:409–419. CrossRefPubMedGoogle Scholar
  38. Templer VL, Lee KA, Preston AJ (2017) Rats know when they remember: transfer of metacognitive responding across odor-based delayed match-to-sample tests. Anim Cogn 20:891–906. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Vining AQ, Marsh HL (2015) Information seeking in capuchins (Cebus apella): a rudimentary form of metacognition? Anim Cogn 18:667–681CrossRefPubMedGoogle Scholar
  40. Washburn DA, Gulledge JP, Beran MJ, Smith JD (2010) With his memory magnetically erased, a monkey knows he is uncertain. Biol Lett 6:160–162. CrossRefPubMedGoogle Scholar
  41. Watanabe A, Clayton NS (2016) Hint-seeking behaviour of western scrub-jays in a metacognition task. Anim Cogn 19:53–64CrossRefPubMedGoogle Scholar
  42. Wittig JH, Richmond BJ (2014) Monkeys rely on recency of stimulus repetition when solving short-term memory tasks. Learn Mem 21:325–333CrossRefPubMedPubMedCentralGoogle Scholar
  43. Wittig JH, Morgan B, Masseau E, Richmond BJ (2016) Humans and monkeys use different strategies to solve the same short-term memory tasks. Learn Mem 23:644–647CrossRefPubMedPubMedCentralGoogle Scholar
  44. Yonelinas AP (2002) The nature of recollection and familiarity: a review of 30 years of research. J Mem Lang 46:441–517CrossRefGoogle Scholar
  45. Yonelinas AP, Aly M, Wang WC, Koen JD (2010) Recollection and familiarity: examining controversial assumptions and new directions. Hippocampus 20:1178–1194CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Emily Kathryn Brown
    • 1
    Email author
  • Benjamin M. Basile
    • 2
  • Victoria L. Templer
    • 3
  • Robert R. Hampton
    • 1
  1. 1.Department of Psychology, Yerkes National Primate Research CenterEmory UniversityAtlantaUSA
  2. 2.Laboratory of NeuropsychologyNIMH, NIHBethesdaUSA
  3. 3.Department of PsychologyProvidence CollegeProvidenceUSA

Personalised recommendations