Elements of episodic-like memory in animals.
Open accessAbstract
A number of psychologists have suggested that episodic memory is a uniquely human phenomenon and, until recently, there was little evidence that animals could recall a unique past experience and respond appropriately. Experiments on food-caching memory in scrub jays question this assumption. On the basis of a single caching episode, scrub jays can remember when and where they cached a variety of foods that differ in the rate at which they degrade, in a way that is inexplicable by relative familiarity. They can update their memory of the contents of a cache depending on whether or not they have emptied the cache site, and can also remember where another bird has hidden caches, suggesting that they encode rich representations of the caching event. They make temporal generalizations about when perishable items should degrade and also remember the relative time since caching when the same food is cached in distinct sites at different times. These results show that jays form integrated memories for the location, content and time of caching. This memory capability fulfils Tulving's behavioural criteria for episodic memory and is thus termed 'episodic-like'. We suggest that several features of episodic memory may not be unique to humans.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Episodic memory cannot be directly studied in animals given the lack of behavioral markers for their conscious experience.
“It is important to note that given the requirement of a conscious experience to form an episodic memory, at present episodic memory cannot be directly studied in animals given the lack of behavioral markers for their conscious experience (Clayton et al., 2001).”
From Aerobic Exercise as a Tool to Improve Hippocampal Plasticity and Function in Humans: Practical Implications for Mental Health Treatment (2016) · cites this paper as Clayton et al., 2001
Cites
The descent of man and selection in relation to sex
チャールス, ダ., & 茂穂, 田. (1907) · Tokyo Jinrui Gakkai zasshi · doi:10.1537/ase1887.22.495 · Cited by 10,909 · see citing works
(1983) · Medical Entomology and Zoology · Cited by 6,051 · see citing works
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995) · Psychological Review · doi:10.1037/0033-295x.102.3.419 · Cited by 5,256 · see citing works
A process dissociation framework: Separating automatic from intentional uses of memory
Jacoby, L. (1991) · Journal of Memory and Language · doi:10.1016/0749-596x(91)90025-f · Cited by 3,815 · see citing works
(2007) · Cognitive Psychology · doi:10.4135/9781446212967.n15 · Cited by 3,749 · see citing works
Recognizing: The judgment of previous occurrence.
Mandler, G. (1980) · Psychological Review · doi:10.1037/0033-295x.87.3.252 · Cited by 2,753 · see citing works
Gallistel, C. R. (1990) · Cited by 2,571 · see citing works
On the relationship between autobiographical memory and perceptual learning.
Jacoby, L. L., & Dallas, M. (1981) · Journal of Experimental Psychology General · doi:10.1037//0096-3445.110.3.306 · Cited by 2,562 · see citing works
Remembrance of places passed: Spatial memory in rats.
Olton, D. S., & Samuelson, R. J. (1976) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.2.2.97 · Cited by 1,934 · see citing works
Episodic memory, amnesia, and the hippocampal–anterior thalamic axis
Aggleton, J. P., & Brown, M. W. (1999) · Behavioral and Brain Sciences · doi:10.1017/s0140525x99002034 · Cited by 1,879 · see citing works
Gibbon, J., Church, R. M., & Meck, W. H. (1984) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1984.tb23417.x · Cited by 1,806 · see citing works
On the relationship between autobiographical memory and perceptual learning.
Jacoby, L. L., & Dallas, M. (1981) · Journal of Experimental Psychology General · doi:10.1037/0096-3445.110.3.306 · Cited by 1,805 · see citing works
Tomasello, M., & Call, J. (1997) · doi:10.1093/oso/9780195106237.001.0001 · Cited by 1,491 · see citing works
Episodic-like memory during cache recovery by scrub jays
Clayton, N. S., & Dickinson, A. (1998) · Nature · doi:10.1038/26216 · Cited by 1,464 · see citing works
Self-citationThe Structure and Organization of Memory
Squire, L. R., Knowlton, B. J., & Musen, G. (1993) · Annual Review of Psychology · doi:10.1146/annurev.ps.44.020193.002321 · Cited by 1,121 · see citing works
Mental time travel and the evolution of the human mind.
Suddendorf, T., & Corballis, M. C. (1997) · PubMed · Cited by 1,053 · see citing works
Fuller, T. K., & Wall, S. B. V. (1992) · Journal of Wildlife Management · doi:10.2307/3808809 · Cited by 986 · see citing works
The hippocampal memory indexing theory.
Teyler, T. J., & DiScenna, P. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.2.147 · Cited by 871 · see citing works
Cuckoos versus reed warblers: Adaptations and counteradaptations
Davies, N. B., & Brooke, M. D. L. (1988) · Animal Behaviour · doi:10.1016/s0003-3472(88)80269-0 · Cited by 693 · see citing works
Memory for the time of past events.
Friedman, W. J. (1993) · Psychological Bulletin · doi:10.1037/0033-2909.113.1.44 · Cited by 639 · see citing works
(1994) · The MIT Press eBooks · doi:10.7551/mitpress/4545.001.0001 · Cited by 485 · see citing works
What Are the Memory Systems of 1994?
(1994) · The MIT Press eBooks · doi:10.7551/mitpress/4545.003.0002 · Cited by 422 · see citing works
Evolution of spatial cognition: sex-specific patterns of spatial behavior predict hippocampal size.
Jacobs, L. F., Gaulin, S. J. C., Sherry, D. F., & Hoffman, G. E. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.16.6349 · Cited by 366 · see citing works
Alternative representations of time, number, and rate
Church, R. M., & Broadbent, H. A. (1990) · Cognition · doi:10.1016/0010-0277(90)90018-f · Cited by 362 · see citing works
Clayton, N. S., Yu, K. S., & Dickinson, A. (2001) · Journal of Experimental Psychology: Animal Behavior Processes · doi:10.1037//0097-7403.27.1.17 · Cited by 238 · see citing works
Self-citationClayton, N. S., & Dickinson, A. (1999) · Journal of Comparative Psychology · doi:10.1037/0735-7036.113.4.403 · Cited by 227 · see citing works
Self-citationMenzel, C. R. (1999) · Journal of comparative psychology · doi:10.1037/0735-7036.113.4.426 · Cited by 172 · see citing works
Memory for the content of caches by scrub jays (Aphelocoma coerulescens).
Clayton, N. S., & Dickinson, A. (1999) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.25.1.82 · Cited by 133 · see citing works
Self-citationCognitive ecology: a field of substance?
Healy, S., & Braithwaite, V. A. (2000) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(99)01737-1 · Cited by 103 · see citing works
Real, L. A. (1993) · Trends in Ecology & Evolution · doi:10.1016/0169-5347(93)90044-p · Cited by 99 · see citing works
Motivational control of caching behaviour in the scrub jay,Aphelocoma coerulescens
Clayton, N. S., & Dickinson, A. (1999) · Animal Behaviour · doi:10.1006/anbe.1998.0989 · Cited by 84 · see citing works
Self-citationThe Descent of Man, and Selection in Relation to Sex
Darwin, C. R. (2008) · Princeton University Press eBooks · doi:10.1515/9781400820061 · Cited by 80 · see citing works
Stored and encountered seeds: A comparison of two spatial memory tasks in marsh tits and chickadees.
Shettleworth, S. J., & Krebs, J. R. (1986) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.12.3.248 · Cited by 79 · see citing works
Chapter 8 Cooperation, conflict and compromise between circadian and interval clocks in pigeons
Gibbon, J., Fairhurst, S., & Goldberg, B. (1997) · Advances in psychology · doi:10.1016/s0166-4115(97)80060-x · Cited by 39 · see citing works
CHAPTER 15 The Natural History of Valuable Relationships in Primates
van Schaik, C. P., Aureli, F., Strier, K. B., et al. (2001) · University of California Press eBooks · doi:10.1525/9780520924932-022 · Cited by 8 · see citing works
Grings, W. W. (2007) · doi:10.1037/11527-003 · Cited by 1 · see citing works
Episodic memory, semantic memory, and amnesia
Squire, L. R., & Zola, S. M. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1998)8:3
Flagged first, then by citations
Cited by
Sorted by citations
Conway, M. A. (2005) · Journal of Memory and Language · doi:10.1016/j.jml.2005.08.005 · Cited by 2,155 · see citing works
Webster, S. J., Bachstetter, A. D., Nelson, P. T., Schmitt, F. A., & Van Eldik, L. J. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2014.00088 · Cited by 755 · see citing works
“…on episodic-like memory across a number of animal species has suggested otherwise, and several mouse behavioral tasks designed at assessing episodic-like memory have been developed (Clayton and Dickinson, 1998; Clayton et al., 2001; Griffiths and Clayton, 2001; Morris, 2001; Davis et al., 2013a,b).”
BackgroundEffects of experience and social context on prospective caching strategies by scrub jays
Emery, N. J., & Clayton, N. S. (2001) · Nature · doi:10.1038/35106560 · Cited by 565 · see citing works
Self-citationThe evolution of episodic memory
Allen, T. A., & Fortin, N. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301199110 · Cited by 350 · see citing works
Social complexity and transitive inference in corvids
Bond, A. B., Kamil, A. C., & Balda, R. P. (2003) · Animal Behaviour · doi:10.1006/anbe.2003.2101 · Cited by 312 · see citing works
The Hippocampus and Memory for “What,” “Where,” and “When”
Ergorul, C., & Eichenbaum, H. (2004) · Learning & Memory · doi:10.1101/lm.73304 · Cited by 294 · see citing works
Integrated memory for objects, places, and temporal order: Evidence for episodic-like memory in mice
Dere, E., Huston, J. P., & De Souza Silva, M. A. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.07.002 · Cited by 243 · see citing works
Levine, B. (2004) · Brain and Cognition · doi:10.1016/s0278-2626(03)00280-x · Cited by 189 · see citing works
Discrimination of what, when, and where: Implications for episodic-like memory in rats
Babb, S. J., & Crystal, J. D. (2005) · Learning and Motivation · doi:10.1016/j.lmot.2005.02.009 · Cited by 181 · see citing works
Clayton, N. S., Yu, K. S., & Dickinson, A. (2003) · Journal of Experimental Psychology: Animal Behavior Processes · doi:10.1037/0097-7403.29.1.14 · Cited by 164 · see citing works
Self-citationKandola, A., Hendrikse, J., Lucassen, P. J., & Yücel, M. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00373 · Cited by 155 · see citing works
“It is important to note that given the requirement of a conscious experience to form an episodic memory, at present episodic memory cannot be directly studied in animals given the lack of behavioral markers for their conscious experience (Clayton et al., 2001).”
Retrospective cognition by food-caching western scrub-jays
de Kort, S. R., Dickinson, A., & Clayton, N. S. (2005) · Learning and Motivation · doi:10.1016/j.lmot.2005.02.008 · Cited by 107 · see citing works
Self-citationThe episodic nature of episodic-like memories
Easton, A., Webster, L. A. D., & Eacott, M. J. (2012) · Learning & Memory · doi:10.1101/lm.025676.112 · Cited by 67 · see citing works
A bird-brain view of episodic memory
Rattenborg, N. C., & Martinez-Gonzalez, D. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.03.030 · Cited by 45 · see citing works
Davies, J. R., Garcia-Pelegrin, E., & Clayton, N. S. (2024) · PLOS ONE · doi:10.1371/journal.pone.0301298 · Cited by 31 · see citing works
Self-citationEpisodic-like memory in common bottlenose dolphins
Davies, J. R., Garcia-Pelegrin, E., Baciadonna, L., Pilenga, C., Favaro, L., & Clayton, N. S. (2022) · Current Biology · doi:10.1016/j.cub.2022.06.032 · Cited by 29 · see citing works
Self-citationIs episodic-like memory <i>like</i> episodic memory?
Davies, J. R., & Clayton, N. S. (2024) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2023.0397 · Cited by 27 · see citing works
Self-citationWild, free-living hummingbirds can learn what happened, where and in which context
Jelbert, S. A., Hurly, T. A., Marshall, R. E. S., & Healy, S. D. (2014) · Animal Behaviour · doi:10.1016/j.anbehav.2013.12.028 · Cited by 25 · see citing works
Chao, O. Y., Nikolaus, S., Huston, J. P., & de Souza Silva, M. A. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.06.009 · Cited by 24 · see citing works
Location and temporal memory of objects declines in aged marmosets (Callithrix jacchus)
De Castro, V., & Girard, P. (2021) · Scientific Reports · doi:10.1038/s41598-021-88357-7 · Cited by 17 · see citing works
Testing two competing hypotheses for Eurasian jays’ caching for the future
Amodio, P., Brea, J., Farrar, B. G., Ostojić, L., & Clayton, N. S. (2021) · Scientific Reports · doi:10.1038/s41598-020-80515-7 · Cited by 10 · see citing works
Self-citation
- Authors
- Clayton, N. S., Griffiths, D. P., Emery, N. J., & Dickinson, A.
- Affiliations
- University of Cambridge (GB)
- Corresponding author
- Clayton, N. S.
- Venue
- Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2001-09-29
- Volume
- 356
- Issue
- 1413
- Pages
- 1483-1491
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- OpenAlex
- W2138140089
- Cited by
- 289
- References
- 37
- Citations by year
- 2026: 7 · 2025: 4 · 2024: 19 · 2023: 7 · 2022: 16 · 2021: 20 · 2020: 11 · 2019: 6 · 2018: 7 · 2017: 11 · 2016: 7 · 2015: 8 · 2014: 13 · 2013: 22 · 2012: 14
- FWCI
- 0.83
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Developmental and Educational Psychology › Child and Animal Learning Development
- Keywords
- episodic-like memory, animal memory, scrub jay, temporal memory, spatial memory, temporal generalization, comparative cognition
- MeSH terms
- Animals, Birds, Feeding Behavior, Memory
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review