Great apes selectively retrieve relevant memories to guide action.

Animals; Female; Male; Memory/physiology; Mental Recall/physiology; Pan troglodytes/physiology; Perception/physiology; Pongo/physiology; Time Factors; Memory; Mental Recall; Pan troglodytes; Perception; Pongo; Multidisciplinary

Abstract :

[en] Memory allows us to draw on past experiences to inform behaviour in the present. However, memories rarely match the situation at hand exactly, and new situations regularly trigger multiple related memories where only some are relevant to act upon. The flexibility of human memory systems is largely attributed to the ability to disregard irrelevant, but salient, memories in favour of relevant ones. This is considered an expression of an executive function responsible for suppressing irrelevant memories, associated with the prefrontal cortex. It is unclear to what extent animals have access to this ability. Here, we demonstrate, in a series of tool-use tasks designed to evoke conflicting memories, that chimpanzees and an orangutan suffer from this conflict but overcome it in favour of a more relevant memory. Such mnemonic flexibility is among the most advanced expressions of executive function shown in animals to date and might explain several behaviours related to tool-use, innovation, planning and more.

Disciplines :

Animal psychology, ethology & psychobiology

Author, co-author :

Bobrowicz, Katarzyna ; Université de Liège - ULiège > Département de Psychologie > Mémoire et langage ; Department of Philosophy and Cognitive Science, Lund University, Lund, Sweden. katarzyna.a.bobrowicz@gmail.com ; Department of Psychology, Lund University, Lund, Sweden. katarzyna.a.bobrowicz@gmail.com

Johansson, Mikael ; Department of Psychology, Lund University, Lund, Sweden

Osvath, Mathias; Department of Philosophy and Cognitive Science, Lund University, Lund, Sweden

Language :

English

Title :

Great apes selectively retrieve relevant memories to guide action.

Publication date :

28 July 2020

Journal title :

Scientific Reports

eISSN :

2045-2322

Publisher :

Nature Research, England

Volume :

Issue :

Pages :

12603

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://www.nature.com/articles/s41598-020-69607-6.pdf

Funding text :

We thank Andrey Anikin (Lund University, henceforth LU) for his generous help with the statistical analysis and Megan Lambert (Messerli Research Institute, VetMedUni Vienna, LU) for proofreading of the manuscript. Further, we thank Ivo Jacobs (LU), Tomas Persson (LU), Gabriela-Alina Sauciuc (LU), Anton Wrisberg (LU), Joost van der Weijer (LU), Daniel Hansson (Furuvik zoo), Linda-Marie Lenell (Furuvik zoo), Elina Lundholm (Furuvik zoo), Natalie Magnusson (Furuvik zoo) and Lotta Widlund (Furuvik zoo). We also thank three anonymous Reviewers who greatly helped with the manuscript\u2019s clarity and structure. This work was funded by the Swedish National Council, Grant no. 2014-6402 conjoined with Marie Sklodowska Curie Actions, Cofund, INCA 600398, and by Stiftelsen Roy och Maj Franz\u00E9ns fond, Grant no. RFv2017-0183.

Available on ORBi :

since 03 February 2026

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Bibliography

Lee, J. L. C. Reconsolidation: maintaining memory relevance. Trends Neurosci. 32, 413–420. 10.1016/j.tins.2009.05.002 (2009). DOI: 10.1016/j.tins.2009.05.002
Robertson, E. M. New Insights in Human Memory Interference and Consolidation. Curr. Biol. 22, R66–R71. 10.1016/j.tins.2009.05.002 (2012). DOI: 10.1016/j.tins.2009.05.002
Wixted, J. T. The psychology and neuroscience of forgetting. Annu Rev. Psychol. 55, 235–269. 10.1146/annurev.psych.55.090902.141555 (2004). DOI: 10.1146/annurev.psych.55.090902.141555
Gabitov, E. et al. Re-stepping into the same river: competition problem rather than a reconsolidation failure in an established motor skill. Sci. Rep. 7, 9406. 10.1038/s41598-017-09677-1 (2017). DOI: 10.1038/s41598-017-09677-1
Tulving, E. Cue-dependent forgetting. Am. Sci. 62, 74–82 (1974).
Tulving, E. & Pearlstone, Z. Availability versus accessibility of information in memory for words. J. Verbal Learn.Verbal. Behav. 5, 381–391 (1966). DOI: 10.1016/S0022-5371(66)80048-8
Johansson, M., Aslan, A., Bäuml, K. H., Gäbel, A. & Mecklinger, A. When remembering causes forgetting: electrophysiological correlates of retrieval-induced forgetting. Cereb. Cortex 17, 1335–1341. 10.1093/cercor/bhl044 (2007). DOI: 10.1093/cercor/bhl044
Peters, G. J., David, C. N., Marcus, M. D. & Smith, D. M. The medial prefrontal cortex is critical for memory retrieval and resolving interference. Learn. Mem. 20, 201–209. 10.1101/lm.029249.112 (2013). DOI: 10.1101/lm.029249.112
Cheng, K. Context cues eliminate retroactive interference effects in honeybees Apis mellifera. J. Exp. Biol. 208, 1019–1024. 10.1242/jeb.01499 (2005). DOI: 10.1242/jeb.01499
Wright, A. A. Testing complex animal cognition: concept learning, proactive interference, and list memory. J. Exp. Anal. Behav. 109, 87–100. 10.1002/jeab.299 (2018). DOI: 10.1002/jeab.299
Devkar, D. T. & Wright, A. A. Event-based proactive interference in rhesus monkeys. Psychon. Bull. Rev. 23, 1474–1482. 10.3758/s13423-016-1005-x (2016). DOI: 10.3758/s13423-016-1005-x
Redshaw, J. Does metarepresentation make human mental time travel unique?. WIREs Cogn. Sci. 5, 519–531. 10.1002/wcs.1308 (2014). DOI: 10.1002/wcs.1308
Carruthers, P. & Ritchie, J. The emergence of metacognition: Affect and uncertainty in animals in The Foundations of Metacognition (ed. Beran, M., Brandl, J., Perner, J. & Proust, J.) 76–93 (Oxford Univ. Press, Oxford, 2012).
Dennett, D. C. From Bacteria to Bach and Back (Penguin Books Ltd., 2018).
McCormack, T. & Hoerl, C. Tool Use, Planning, and Future Thinking in Children and Animals in Tool use and causal cognition (ed. McCormack, T., Hoerl, C. & Butterfill, S.) 129–147 (Oxford Univ. Press, Oxford, 2011).
Call, J. Do apes know that they could be wrong?. Anim. Cognit. 13, 689–700. 10.1007/s10071-010-0317-x (2010). DOI: 10.1007/s10071-010-0317-x
Basile, B. M., Schroeder, G. R., Brown, E. K., Templer, V. L. & Hampton, R. R. Evaluation of seven hypotheses for metamemory performance in rhesus monkeys. J. Exp. Psychol. Gen. 144, 85–102 (2015). DOI: 10.1037/xge0000031
Reader, S.M., & Laland, K. N. Animal Innovation: An Introduction in Animal Innovation (ed. Reader, S. M. & Laland, K. N.) 3–35 (Oxford Univ. Press, New York, 2003).
Rosati, A. G., Stevens, J. R., Hare, B. & Hauser, M. D. The evolutionary origins of human patience: temporal preferences in chimpanzees, bonobos and human adults. Curr. Biol. 17, 1663–1668. 10.1016/j.cub.2007.08.033 (2007). DOI: 10.1016/j.cub.2007.08.033
Rumbaugh, D. M., Rumbaugh, E. S. & Washburn, D. A. Toward a new outlook on primate learning and behaviour: complex learning and emergent processes in comparative perspective. Jpn. Psychol. Res. 38, 113–125. 10.1111/j.1468-5884.1996.tb00016.x (1996). DOI: 10.1111/j.1468-5884.1996.tb00016.x
MacLean, E. et al. The evolution of self-control. PNAS 20, E2140–E2148. 10.1073/pnas.1323533111 (2014). DOI: 10.1073/pnas.1323533111
Lewis, A., Berntsen, D. & Call, J. Long-term memory of past events in great apes. Curr. Dir. Psychol. Sci. 1, 1. 10.1177/0963721418812781 (2019). DOI: 10.1177/0963721418812781
Gruber, T., Muller, M. N., Reynolds, V., Wrangham, R. & Zuberbühler, K. Community-specific evaluation of tool affordances in wild chimpanzees. Sci. Rep. 1, 128. 10.1038/srep00128 (2011). DOI: 10.1038/srep00128
Harrison, R. A. & Whiten, A. Chimpanzees (Pan troglodytes) display limited behavioral flexibility when faced with a changing foraging task requiring tool use. Peer J. 6, e4366. 10.7717/peerj.4366 (2018). DOI: 10.7717/peerj.4366
Hrubesch, C., Preuschoft, S. & Schaik, C. V. Skill mastery inhibits adoption of observed alternative solutions among chimpanzees (Pan troglodytes). Anim. Cogn. 12, 209–216. 10.1007/s10071-008-0183-y (2009). DOI: 10.1007/s10071-008-0183-y
Jacobson, S. L., & Hopper, L. M. Hardly habitual: chimpanzees and gorillas show flexibility in their motor responses when presented with a causally-clear task. Peer J. e6195. https://doi.org/10.7717/peerj.6195 (2019).
Manrique, H. M. & Call, J. Age-dependent cognitive inflexibility in great apes. Anim. Behav. 102, 1–6. 10.1016/j.anbehav.2015.01.002 (2015). DOI: 10.1016/j.anbehav.2015.01.002
Davis, S. J., Vale, G. L., Schapiro, S. J., Lambeth, S. P. & Whiten, A. Foundations of cumulative culture in apes: improved foraging efficiency through relinquishing and combining witnessed behaviors in chimpanzees (Pan troglodytes). Sci. Rep. 6, 35953. 10.1038/srep35953 (2016). DOI: 10.1038/srep35953
Horner, V. & Whiten, A. Causal knowledge and imitation/emulation switching in chimpanzees (Pan troglodytes) and children. Anim. Cogn. 8, 164–181. 10.1007/s10071-004-0239-6 (2005). DOI: 10.1007/s10071-004-0239-6
Manrique, H. M., Völter, C. J. & Call, J. Repeated innovation in great apes. Anim. Behav. 85, 195–202. 10.1016/j.anbehav.2012.10.026 (2013). DOI: 10.1016/j.anbehav.2012.10.026
Hampton, R. R. Rhesus monkeys know when they remember. PNAS 98, 5359–5362. 10.1073/pnas.071600998 (2001). DOI: 10.1073/pnas.071600998
Roberts, W. A. Are animals stuck in time?. Psychol. Bull. 128, 473–489. 10.1037/0033-2909.128.3.473 (2002). DOI: 10.1037/0033-2909.128.3.473
Wells, J. E. Strength theory and judgments of recency and frequency. J. Verbal Learn. Verbal Behav. 13, 378–392. 10.1016/S0022-5371(74)80016-2 (1974). DOI: 10.1016/S0022-5371(74)80016-2
Hintzman, D. L. Memory strength and recency judgments. Psychol. Bull. Rev. 12, 858–864. 10.3758/BF03196777 (2005). DOI: 10.3758/BF03196777
Stoet, G. & Snyder, L. H. Executive control and task-switching in monkeys. Neuropsychologia. 41, 1357–1364. 10.1016/S0028-3932(03)00048-4 (2003). DOI: 10.1016/S0028-3932(03)00048-4
Tebbich, S., Seed, A. M., Emery, N. J. & Clayton, N. S. Non-tool-using rooks, Corvus frugilegus, solve the trap-tube problem. Anim. Cogn. 10, 225–231. 10.1007/s10071-006-0061-4 (2007). DOI: 10.1007/s10071-006-0061-4
Martin-Ordas, G., Call, J. & Colmenares, F. Tubes, tables and traps: great apes solve two functionally equivalent trap tasks but show no evidence of transfer across tasks. Anim. Cogn. 11, 423–430. 10.1007/s10071-007-0132-1 (2008). DOI: 10.1007/s10071-007-0132-1
Martin-Ordas, G. & Call, J. Assessing generalization within and between trap tasks in the great apes. Int. J. Comp. Psych. 22, 43–60 (2009).
Seed, A. M., Call, J., Emery, N. J. & Clayton, N. S. Chimpanzees solve the trap problem when the confound of tool-use is removed. J. Exp. Psychol. Anim. Behav. Process. 35, 23–34. 10.1037/a0012925 (2009). DOI: 10.1037/a0012925
Vale, G. L. et al. Robust retention and transfer of tool construction techniques in chimpanzees (Pan troglodytes). J. Comp. Psych. 130, 24–35. 10.1037/a0040000 (2016). DOI: 10.1037/a0040000
Bania, A. E., Harris, S., Kinsley, H. R. & Boysen, S. T. Constructive and deconstructive tool modification by chimpanzees (Pan troglodytes). Anim. Cogn. 12, 85–95. 10.1007/s10071-008-0173-0 (2009). DOI: 10.1007/s10071-008-0173-0
Sabbatini, G. et al. Understanding the functional properties of tools: chimpanzees (Pan troglodytes) and capuchin monkeys (Cebus apella) attend to tool features differently. Anim. Cogn. 15, 577–590. 10.1007/s10071-012-0486-x (2012). DOI: 10.1007/s10071-012-0486-x
Manrique, H. M., Gross, A. N. & Call, J. Great Apes Select Tools on the Basis of Their Rigidity. J. Exp. Psychol. Anim. Behav. Process. 36, 409–422. 10.1037/a0019296 (2010). DOI: 10.1037/a0019296
Bakeman, R., Quera, V. & Gnisci, A. Observer-agreement for timed-event sequential data: a comparison of time-based and event-based algorithms. Behav. Res. Methods. 41, 137–147. 10.3758/BRM.41.1.137 (2009). DOI: 10.3758/BRM.41.1.137
Bürkner, P. C. brms: an R package for Bayesian multilevel models using stan. J. Stat. Softw. 80, 1–28. 10.18637/jss.v080.i01 (2017). DOI: 10.18637/jss.v080.i01
Bürkner, P. C. Advanced Bayesian Multilevel Modeling with the R Package brms. R J. 10, 395–411. 10.32614/RJ-2018-017 (2018). DOI: 10.32614/RJ-2018-017
Wickham, H. ggplot2: Elegant graphics for data analysis (Springer, New York, 2016). DOI: 10.1007/978-3-319-24277-4
Anikin, A. Soundgen: an open-source tool for synthesizing nonverbal vocalizations. Behav. Res. Methods. 51, 778–792. 10.3758/s13428-018-1095-7 (2019). DOI: 10.3758/s13428-018-1095-7
Wickham, H. Reshaping data with the reshape package. J. Stat. Softw. 21, 1 (2007). DOI: 10.18637/jss.v021.i12
Yassa, M. A. & Reagh, Z. M. Competitive trace theory: a role for the hippocampus in contextual interference during retrieval. Front. Behav. Neurosci. 7, 107. 10.3389/fnbeh.2013.00107 (2013). DOI: 10.3389/fnbeh.2013.00107
Bekinschtein, P., Weisstaub, N. V., Gallo, F., Renner, M. & Anderson, M. C. A retrieval-specific mechanism of adaptive forgetting in the mammalian brain. Nat. Comm. 9, 4660. 10.1038/s41467-018-07128-7 (2018). DOI: 10.1038/s41467-018-07128-7
Jost, K. et al. Controlling conflict from interfering long-term memory representations. J. Cogn. Neurosci. 24, 1173–1190. 10.1162/jocn_a_00199 (2012). DOI: 10.1162/jocn_a_00199
Parrish, A. E., Otalora-Garcia, A. & Beran, M. J. Dealing with interference: Chimpanzees respond to conflicting cues in a food-choice memory task. J. Exp. Psychol. Anim. Learn. Cogn. 43, 366–376. 10.1037/xan0000151 (2017). DOI: 10.1037/xan0000151
Völter, C. J., Mundry, R., Call, J. & Seed, A. Chimpanzees flexibly update working memory contents and show susceptibility to distraction in the self-ordered search task. Proc. Biol. Sci. 286, 20190715. 10.1098/rspb.2019.0715 (2019). DOI: 10.1098/rspb.2019.0715
Osvath, M. & Osvath, H. Chimpanzee (Pan troglodytes) and orangutan (Pongo abelii) forethought: self-control and pre-experience in the face of future tool use. Anim. Cogn. 11, 661–674. 10.1007/s10071-008-0157-0 (2008). DOI: 10.1007/s10071-008-0157-0
Anderson, M. C., Bjork, R. A. & Bjork, E. L. Remembering can cause forgetting: retrieval dynamics in long-term memory. J. Exp. Psychol. Learn. Mem. Cogn. 20, 1063–1087 (1994). DOI: 10.1037/0278-7393.20.5.1063
Anderson, M. C. Rethinking interference theory: executive control and the mechanisms of forgetting. J. Mem. Lang. 49, 415–445. 10.1016/j.jml.2003.08.006 (2003). DOI: 10.1016/j.jml.2003.08.006
Murayama, K., Miyatsu, T., Buchli, D. & Storm, B. C. Forgetting as a consequence of retrieval: a meta-analytic review of retrieval-induced forgetting. Psychol. Bull. 140, 1383–1409. 10.1037/a0037505 (2014). DOI: 10.1037/a0037505
Wimber, M., Alink, A., Charest, I., Kriegeskorte, N. & Anderson, M. C. Retrieval induces adaptive forgetting of competing memories via cortical pattern suppression. Nat. Neurosci. 18, 582–589. 10.1038/nn.3973 (2015). DOI: 10.1038/nn.3973
Wimber, M. et al. Prefrontal dopamine and the dynamic control of human long-term memory. Transl. Psychiatry. 1, e15. 10.1038/tp.2011.15 (2011). DOI: 10.1038/tp.2011.15
Kuhl, B. A., Dudukovic, N. M., Kahn, I. & Wagner, A. D. Decreased demands on cognitive control reveal the neural processing benefits of forgetting. Nat. Neurosci. 10, 908–914. 10.1038/nn1918 (2007). DOI: 10.1038/nn1918