Keeping track of time: evidence for episodic-like memory in great apes
Open accessAbstract
Episodic memory, as defined by Tulving, can be described in terms of behavioural elements (what, where and when information) but it is also accompanied by an awareness of one's past (chronesthesia) and a subjective conscious experience (autonoetic awareness). Recent experiments have shown that corvids and rodents recall the where, what and when of an event. This capability has been called episodic-like memory because it only fulfils the behavioural criteria for episodic memory. We tested seven chimpanzees, three orangutans and two bonobos of various ages by adapting two paradigms, originally developed by Clayton and colleagues to test scrub jays. In Experiment 1, subjects were fed preferred but perishable food (frozen juice) and less preferred but non-perishable food (grape). After the food items were hidden, subjects could choose one of them either after 5 min or 1 h. The frozen juice was still available after 5 min but melted after 1 h and became unobtainable. Apes chose the frozen juice significantly more after 5 min and the grape after 1 h. In Experiment 2, subjects faced two baiting events happening at different times, yet they formed an integrated memory for the location and time of the baiting event for particular food items. We also included a memory task that required no temporal encoding. Our results showed that apes remember in an integrated fashion what, where and when (i.e., how long ago) an event happened; that is, apes distinguished between different events in which the same food items were hidden in different places at different times. The temporal control of their choices was not dependent on the familiarity of the platforms where the food was hidden. Chimpanzees' and bonobos' performance in the temporal encoding task was age-dependent, following an inverted U-shaped distribution. The age had no effect on the performance of the subjects in the task that required no temporal encoding.
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Written from the paper’s full text.
TL;DR
Great apes remembered what, where, and when food was hidden in an integrated fashion, choosing perishable frozen juice more after 5 min and non-perishable grape after 1 h. Performance on this episodic-like memory task followed an inverted U-shaped age pattern, while a non-temporal memory task showed no age effect.
Key findings
- In Experiment 1, apes chose frozen juice significantly more often after a 5-min retention interval than after 1 h (Wilcoxon: z = 2.55, p = 0.011, n = 12); 4 of 12 subjects showed this reversal individually.
- In the pre-test requiring no temporal encoding, apes remembered food location above chance across delays (Wilcoxon: z = 3.12, p = 0.002, n = 12), with no age effect (r_s = 0.08, p = 0.41).
- Experiment 1 www-memory performance showed an inverted U-shaped age trend (permutation test: c² = −0.142, p = 0.0682, n = 12); for chimpanzees and bonobos alone this was significant (c² = −0.026, p = 0.002, n = 9).
- In Experiment 2, subjects chose frozen juice significantly more often from the platform baited last than from the platform baited first (Wilcoxon: z = 1.79, p = 0.037, one-tailed, n = 5), supporting integrated what–where–when memory.
Methods
- Experiment 1 tested 7 chimpanzees, 3 orangutans, and 2 bonobos (12 total; ages 6–31 years) at the Wolfgang Köhler Primate Research Centre, using a platform with three possible baiting sites and two food types: preferred perishable frozen juice and less preferred non-perishable grape.
- Subjects chose after 5-min or 1-h retention intervals; analyses used Wilcoxon tests, Pearson chi-square, and permutation-based quadratic models of age effects.
- Experiment 2 tested 5 successful subjects (2 bonobos, 2 chimpanzees, 1 orangutan; ages 10–14 years) with two baiting events separated by 1 h and choice tests 5 min after the second event, analyzed with a one-tailed Wilcoxon test.
Limitations
- The paper states that the reduced sample size did not allow more fine-grained analyses to distinguish differences between great ape species or developmental patterns.
- The paper states that the data do not allow the conclusion that apes are actually recalling the baiting episode, and the mechanism used to keep track of time remains undetermined.
- The paper notes that orangutan performance could reflect species differences or simply that the tested orangutans were too young or too old; more broadly, the study assesses behavioral criteria for episodic-like memory, not autonoetic awareness.
Model-written summary. Check it against the paper before relying on it.
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Claims the paper makes
0 of 47 cited sources checked · 0 supported · 0 flagged
- Findingown data
Four out of 12 subjects chose the frozen juice significantly more often than the grape after the short retention interval and the grape after the long retention interval.
“Individual analyses showed that 4 out of 12 subjects chose the frozen juice significantly more often than the grape after the short RI and the grape after the long RI (Table 1).”
Quote in the paperSubstantial claim - Findingown data
Performance on the what-where-when memory test revealed an inverted U-shaped trend as a function of age.
“the performance on the www-memory test revealed an inverted U-shaped trend as a function of age (permutation test: c 2 = −0.142, p = 0.0682, n = 12, Fig. 1).”
Quote in the paperNot a substantial claim - Findingown data
Apes remembered the location of food above chance after each retention interval (2 min, 1 h, 2 h, 24 h) in the memory ability pre-test.
“Overall apes remembered the location of the food after each RI above the chance levels in the memory ability pre-test (Wilcoxon test: z = 3.12, p = 0.002, n = 12 in all intervals, Fig. 1)”
Quote in the paperSubstantial claim - Findingown data
There was no change in performance across ages in the memory ability pre-test (task requiring no temporal encoding).
“there was no change in performance across ages (r s=0.08, p = 0.41, n = 12).”
- Also stated in: § Abstract · plain
“The age had no effect on the performance of the subjects in the task that required no temporal encoding.”
Quote in the paperNot a substantial claim - Also stated in: § Abstract · plain
- Findingnone given
The temporal control of the apes' choices was not dependent on the familiarity of the platforms where the food was hidden.
“The temporal control of their choices was not dependent on the familiarity of the platforms where the food was hidden.”
Quote in the paperSubstantial claim
- Findingown data
In Experiment 2, subjects formed an integrated memory for the location and time of the baiting event for particular food items.
“In Experiment 2, subjects faced two baiting events happening at different times, yet they formed an integrated memory for the location and time of the baiting event for particular food items.”
Quote in the paperSubstantial claim- Rests on an assumption: Frozen juice remains available/edible after 5 min but melts and becomes unobtainable after 1 h.
- Findingown data
Apes chose the frozen juice significantly more often after a 5-min retention interval than after a 1-h retention interval.
“Apes chose the frozen juice significantly more after 5 min and the grape after 1 h.”
- Also stated in: § Results · plain
“Subjects chose the frozen juice significantly more often after the 5-min interval than after the 1-h interval (Wilcoxon test: z = 2.55, p = 0.011, n = 12; Fig. 2).”
Quote in the paperSubstantial claim- Rests on an assumption: Frozen juice remains available/edible after 5 min but melts and becomes unobtainable after 1 h.
- Rests on an assumption: The grape is a non-perishable food.
- Also stated in: § Results · plain
- Findingown data
Focusing solely on chimpanzees and bonobos (genus Pan) confirmed the inverted U-shaped age trend in the what-where-when memory test.
“Focusing solely on members of the genus Pan (chimpanzees and bonobos) confirmed this result (permutation test: c 2 = −0.026, p = 0.002, n = 9).”
- Also stated in: § Abstract · plain
“Chimpanzees’ and bonobos’ performance in the temporal encoding task was age-dependent, following an inverted U-shaped distribution.”
Quote in the paperNot a substantial claim - Also stated in: § Abstract · plain
- Findingown data
Apes' performance in the www-memory task showed an inverted U-shaped curve in which middle-age subjects performed better than the youngest and oldest subjects.
“Additionally, apes’ performance in the www-memory task showed an inverted U-shaped curve in which middle-age subjects performed better than the youngest and oldest subjects.”
- Also stated in: § General discussion · plain
“Additionally, subjects’ performance in the www-memory task showed an age-dependent inverted U-shaped curve.”
Quote in the paperNot a substantial claim - Also stated in: § General discussion · plain
- Findingown data
The performance in the 24-h delay condition was as good as that after a 2-min delay condition.
“In fact, the performance in the 24-h delay condition was as good as that after a 2-min delay condition.”
Quote in the paperNot a substantial claim - Findingown data
There was no age effect in the pre-test in which no temporal information was needed to be encoded.
“In contrast, there was no age effect in the pre-test in which no temporal information was needed to be encoded.”
- Also stated in: § General discussion · plain
“In contrast, no age effect was observed in a memory task that required no encoding of temporal information.”
Quote in the paperSubstantial claim - Also stated in: § General discussion · plain
- Findingown data
During the pre-test, subjects were capable of remembering the location of the food reward after 24 h had elapsed since baiting.
“During the pre-test, subjects were capable of remembering the location of the food reward after 24 h had elapsed since baiting.”
Quote in the paperNot a substantial claim - Findingown data
Subjects chose the frozen juice significantly more often in the table baited last compared to the table baited first (Wilcoxon test: z = 1.79, p = 0.037, 1-tailed, n = 5).
“Subjects chose the frozen juice significantly more often in the table baited last compared to the table baited first (Wilcoxon test: z = 1.79, p = 0.037, 1-tailed, n = 5, Table 1).”
Quote in the paperSubstantial claim - Findingnone given
The performance of the members of the genus Pan (chimpanzees and bonobos) followed an inverted U-shaped distribution.
“The performance of the members of the genus Pan (chimpanzees and bonobos) followed an inverted U-shaped distribution.”
Quote in the paperSubstantial claim - Findingown data
In the last round of Experiment 1, one orangutan significantly reversed her choices (χ2 = 6, p = 0.014).
“We included one of the orangutans because in the last round of Experiment 1 she significantly reversed her choices (χ 2 = 6, p = 0.014; see table 1 for more details).”
Quote in the paperSubstantial claim - Interpretationnone given
Subjects' performance in Experiment 1 can only be explained by the recall of three types of information: what types of food were hidden, where they were hidden, and when they were hidden.
“Subjects’ performance can only be explained by the recall of three types of information: what types of food (frozen juice and grapes) were hidden, where they were hidden (in which box) and when (5 min or 1 h ago) they were hidden.”
Quote in the paperSubstantial claim - Premisecitation
Evidence from several studies on episodic memory in humans describes a symmetrical inverted U-shaped pattern of rising in childhood (3-4 years old) and declining in ageing (by the age of 25-30 years it begins a steady decline through adulthood).
“Evidence from several studies on episodic memory in humans describes a symmetrical inverted U-shaped pattern of rising in childhood (3–4 years old) and declining in ageing”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Tulving and Craik 2000 source
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- cites Craik and Salthouse 2000
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- cites Craik and Salthouse 2008
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- Premisecitation
A gorilla was able to hand over the card representing the type of food given to him and the card with the name of the trainer who had given him the food after delays of 10 min or 24 h.
“The gorilla was able to hand over the card that represented the type of food that was given to him and the card with the name of the trainer who had given him the food after the delay (Schwartz et al. 2002).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Schwartz et al. 2002 source
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- Premisenone given
None of these studies have shown that great apes can remember when the event occurred.
“Additionally, none of these studies have shown that great apes can remember when the event occurred.”
Quote in the paperSubstantial claim - Interpretationreasoning
In terms of purely behavioural criteria, the results provide evidence for episodic-like memory in great apes.
“In terms of purely behavioural criteria, our results provide evidence for episodic-like memory in great apes.”
Quote in the paperSubstantial claim - Premisecitation
The sole attempt to evaluate www-memory in non-human primates has been done with rhesus macaques (Hampton et al. 2005).
“The sole attempt to evaluate www-memory in non-human primates has been done with rhesus macaques (Hampton et al. 2005).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Hampton et al. 2005 source
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- Premisecitation
A chimpanzee correctly indicated to caretakers where a specific food item was hidden using a lexigram keyboard up to 16 h after observing baiting events.
“In a free recall experiment, a chimpanzee correctly indicated to the caretakers where a specific food item was hidden using a lexigram keyboard up to 16 h after observing baiting events (Menzel 2005).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Menzel 2005
Not checked in the free run.
- Interpretationcitation
Experiment 1 established that apes can remember the what, where and when of an event.
“Experiment 1 established that apes can remember the what, where and when of an event, although this does not indicate the structure of the memories that support subjects’ choices (Clayton and Dickinson 1999; Clayton et al. 2001, 2003a).”
Quote in the paperSubstantial claim0 of 3 sources checked - Premisecitation
The memory task that required no temporal encoding showed no dramatic changes in ability across ages in humans.
“We contrasted the www-memory task with a memory task that required no temporal encoding and showed no dramatic changes in ability across the ages in humans”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Tulving and Craik 2000 source
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- cites Craik and Salthouse 2000
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- cites Craik and Salthouse 2008
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- Premisecitation
Macaques were unable to remember the when component of an event in Hampton et al.'s study.
“In their study, Hampton and colleagues adapted the paradigm implemented by Clayton and Dickinson (1998) with the jays and they showed that macaques were unable to remember the when component of an event.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Hampton et al. 2005 source
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- Interpretationown data
In the absence of any noticeable forgetting, memory decay is an unlikely mechanism driving subjects' performance.
“Therefore, in the absence of any noticeable forgetting, we believe that memory decay is an unlikely mechanism driving subjects’ performance.”
Quote in the paperSubstantial claim - Interpretationreasoning
The binding between what-where-when allows subjects to discriminate between different episodes that share common features.
“The binding between what–where–when allows subjects to discriminate between different episodes that share common features.”
Quote in the paperSubstantial claim - Interpretationreasoning
A what-where-when structure supports the findings of Experiment 2 because the 'where' representation triggers both the 'what' and the 'when' representation of the baiting event.
“In contrast, a what–where–when structure supports our findings because the “where” representation triggers both the “what” but also the “when” representation of the baiting event.”
Quote in the paperSubstantial claim - Interpretationreasoning
Apes could not have learnt to choose the frozen juice when the platforms were relatively familiar and the grape when the platforms were unfamiliar because apes were exposed to both platforms for the same duration of time.
“Therefore, apes could not have learnt to choose the frozen juice when the platforms were relatively familiar and the grape when the platforms were unfamiliar because apes were exposed to both platforms for the same duration of time.”
Quote in the paperSubstantial claim - Interpretationreasoning
A where-what-when memory cannot support the results of Experiment 2.
“A where–what–when memory cannot support these results because the presence of either table should have retrieved the “what” representation of frozen juice cubes and grapes.”
Quote in the paperSubstantial claim - Interpretationreasoning
To solve the Experiment 2 task, the apes cannot rely on discrimination by relative familiarity because both platforms are always present during the entire trial.
“To solve this task the apes cannot rely on discrimination by relative familiarity because both platforms are always present during the entire trial.”
Quote in the paperSubstantial claim - Interpretationcitation
The age-dependent performance in the www-memory task is similar to the one reported for chimpanzees in the mirror self-recognition (MSR) task.
“First, this age-dependent performance is similar to the one reported for chimpanzees in the mirror self-recognition (MSR) task (Povinelli et al. 1993), a task typically used to assess the development of self-concept in human infants (Amsterdam 1972; Lewis and Brooks-Gunn 1979; Nielsen and Dissanayake 2004).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Povinelli et al. 1993 source
Not checked in the free run.
- Premisereasoning
A where-what-when memory structure does not explicitly encode information about how long ago the baiting event happened in a particular location.
“Therefore, this structure does not explicitly encode information about how long ago the baiting event happened in a particular location.”
Quote in the paperSubstantial claim - Interpretationown data
Familiarity cannot be the mechanism underlying apes' choices.
“However, we believe that familiarity cannot be the mechanism underlying apes’ choices.”
Quote in the paperSubstantial claim - Interpretationreasoning
Experiment 2 demonstrates that the encoded information about the what, where and when of an event occurred in an integrated representation.
“Additionally, Experiment 2 demonstrates that the encoded information about the what, where and when of an event occurred in an integrated representation.”
Quote in the paperSubstantial claim - Interpretationown data
Similar to other species, great apes encoded information about what was hidden, where and when (how long ago) in an integrated fashion.
“Similar to other species (Babb and Crystal 2005, 2006; Clayton and Dickinson 1998, Clayton et al. 2001, 2003b; Dere et al. 2005; Ergorul and Eichenbaum 2004; Ferkin et al. 2008; Henderson et al. 2006; Roberts et al. 2008; Zinkivskay et al. 2009), great apes encoded information about what was hidden, where and when (how long ago) in an integrated fashion.”
Quote in the paperSubstantial claim0 of 3 sources checked - Interpretationown data
Our data do not allow us to conclude that apes are actually recalling the baiting episode.
“However, note that our data do not allow us to conclude that apes are actually recalling the baiting episode.”
Quote in the paperSubstantial claim - Interpretationown data
The most direct form of forgetting (subjects forget the location of the food items) can be ruled out because apes chose empty boxes quite rarely.
“We consider that the most direct form of forgetting (i.e. subjects forget the location of the food items) can be ruled out because apes chose empty boxes quite rarely.”
Quote in the paperSubstantial claim - Interpretationreasoning
It is unlikely that the apes' behaviour was based on an instinctual predisposition to recover hidden caches or reject frozen juice after longer RI since none of the aspects is part of the ecology where apes evolved.
“However, we suggest that it is unlikely that the apes’ behaviour was based on a similar instinctual predisposition to recover hidden caches or reject frozen juice after longer RI since none of the aspects is part of the ecology where apes evolved.”
Quote in the paperSubstantial claim - Interpretationown data
Great apes took into account temporal information to choose a food item.
“Particularly important in the experiments presented here is the fact that great apes took into account temporal information to choose a food item.”
Quote in the paperSubstantial claim - Interpretationown data
Apes chose more often the grape in the platform baited first because the frozen juice hidden in that platform was baited 1 h earlier and had melted.
“Apes chose more often the grape in the platform baited first because the frozen juice hidden in that platform was baited 1 h earlier and, therefore, had melted.”
Quote in the paperSubstantial claim- Rests on an assumption: Frozen juice hidden 1 h earlier had melted and was not edible, while frozen juice hidden 5 min earlier was still edible.
- Interpretationreasoning
Subjects have to remember the two baiting events not only in terms of their time, but also in terms of the location of the food even though they both involved the same food items.
“Therefore, subjects have to remember the two baiting events not only in terms of their time, but also in terms of the location of the food even though they both involved the same food items.”
Quote in the paperSubstantial claim
- May combine two claims. 14
- The quote only partly states this claim. 1
- Classified as probably not a substantial claim. 30
May combine two claims.
Findingown dataSubjects' choices remained unchanged during testing in both the 5-min and 1-h conditions.
“Their choices remained unchanged during testing (Friedman tests: 5-min—χ 2 = 0.16, n = 12, p = 0.92; 1-h—χ 2 = 0.42, n = 12, p = 0.8).”
Quote in the paperNot a substantial claimThe quote only partly states this claim.
Findingown dataSubjects younger than 7 and older than 18 years of age showed much lower performance than adolescents and young adults on the what-where-when memory test.
“Subjects younger than 7 and older than 18 years of age showed a much lower performance than adolescents and young adults.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationClayton and colleagues have shown that scrub jays flexibly integrated memories for the what, where and when of an event.
“Clayton and colleagues have shown that scrub jays flexibly integrated memories for the what, where and when of an event (Clayton and Dickinson 1998, 1999; Clayton et al. 2001, 2003b).”
Quote in the paperNot a substantial claim0 of 3 sources checkedMay combine two claims.
Interpretationown dataThe apes' choices of the less preferred food after the 1-h delay were not simply due to memory lapses, because they rarely selected the empty boxes in the pre-test and test.
“Since subjects rarely selected the empty boxes in the pre-test and test (pre-test: less than 12% of the trials, test: less than 3% of the trials), this suggests that their choices of the less preferred food after 1-h delay were not simply due to memory lapses.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
InterpretationcitationOne weakness in Clayton's experimental approach is that it does not measure memory for unique experiences because they require training.
“Therefore, one weakness in Clayton’s experimental approach is that it does not measure memory for unique experiences because they require training.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Zentall et al. 2001 source
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Study design and conductnone givenThe apes did not have any previous experience with the frozen juice used in the experiment.
“It is important to mention that the apes did not have any previous experience with the frozen juice that we used in our experiment.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductown dataSubjects' general long-term memory was tested in a pre-test before the what-where-when memory test.
“In the pre-test, we tested individuals’ general long-term memory.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductnone givenIn each round and for each trial different baiting places were used and the three possible sites were counterbalanced.
“In each round and for each trial different baiting places were used and the three possible sites were counterbalanced.”
Quote in the paperNot a substantial claimMay combine two claims.
InterpretationreasoningHoffman et al.'s procedure is vulnerable to criticism because subjects were asked to remember what, where and when on separate occasions, raising doubts about the integration of the components.
“However, their subjects were asked to remember these three elements in separate occasions, raising doubts about the integration of the components.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Hoffman et al. 2009
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Study design and conductnone givenThe order in which subjects were presented in the 5-min and 1-h trials was counterbalanced.
“The order in which subjects were presented in the two types of trials was counterbalanced.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
PremisecitationRecent experimental studies have shown evidence for planning in chimpanzees, bonobos and orangutans.
“recent experimental studies have shown evidence for planning in chimpanzees, bonobos and orangutans”
Quote in the paperSubstantial claim0 of 3 sources checkedClassified as probably not a substantial claim. May combine two claims.
Study design and conductreasoningTo provide a unique baiting location on every trial within each round for each ape, the three baiting sites were covered with three different containers each, and these containers were different for each trial.
“To provide a unique baiting location on every trial within each round for each ape, the three baiting sites were covered with three different containers each. Additionally, these containers were different for each trial.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim. May combine two claims.
PremisecitationEacott et al. (2005) challenged the main role of the 'when' component in episodic-like memory, arguing that human episodic memory is poor in recalling timing and 'when' serves as a marker to distinguish events.
“An alternative approach suggested by Eacott et al. (2005) challenged the main role of the “when” component in episodic-like memory.”
Quote in the paperSubstantial claim0 of 2 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationRats were sensitive not only to the location of objects but also to the temporal order in which they were presented, leading authors to conclude that rats integrated what, where and when an event happened.
“The results from these experiments showed that rats were sensitive not only to the location of the objects, but also to the temporal order in which they were presented. These results led the authors to conclude that rats integrated what, where and when an event happened.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Kart-Teke et al. 2006 source
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Classified as probably not a substantial claim.
Study design and conductown dataFood preference for the two food items was established prior to the experiment.
“Prior to the experiment, we established the apes’ preference for two food items.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationOther bird and mammal species have also been shown to possess episodic-like memory (what, where, when).
“Other bird and mammal species have also been shown to possess such type of memory”
Quote in the paperNot a substantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationLongitudinal and cross-sectional studies in human memory have reported an inverted U-shaped curve as a function of age for episodic memory and no age effect for long-term memory.
“Interestingly, longitudinal and cross-sectional studies in human memory have reported an inverted U-shaped curve as a function of age for episodic memory and no age effect for long-term memory (Bialystok and Craik 2006 for a review).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Bialystok and Craik 2006 source
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PremisecitationHoffman et al. (2009) found positive evidence for episodic-like memory in rhesus monkeys using a computer task.
“Recently, Hoffman et al. 2009 examined working memory (Baddeley 2000) for what, where and when information in rhesus monkeys using a new paradigm based on a computer task and found positive evidence for episodic-like memory.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Hoffman et al. 2009
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PremisecitationThe trial-unique learning paradigm has been successfully implemented in rodents and birds.
“The trial-unique learning paradigm has been successfully implemented in rodents (rats: Kart-Teke et al. 2006; mice: Dere et al. 2005) and birds (Zentall et al. 2001).”
Quote in the paperNot a substantial claim0 of 3 sources checkedMay combine two claims.
PremisecitationThe unexpected question experiment by Zentall et al. (2001) only deals with short-time delays between encoding and question, whereas episodic memory is defined as a long-term memory system.
“However, as pointed out by Crystal (2009), episodic memory is defined as a long-term memory system and the unexpected question experiment carried out by Zentall et al. (2001) only deals with short-time delays between the encoding event and the experimental question.”
Quote in the paperNot a substantial claim0 of 2 sources checkedProbably not a substantial claim: may not pass S1 (asserted), S3 (load-bearing).
PremisecitationEpisodic memory and future planning depend on common processes.
“It has also been argued that episodic memory and future planning depend on common processes”
Quote in the paperNot a substantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationPigeons were able to report which action they performed in the past in a delayed-matching to sample task.
“The results from this experiment showed that pigeons were able to report which action they performed in the past.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Zentall et al. 2001 source
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Premisenone givenCompared to rodents and birds, non-human primates have received relatively little attention in episodic-like memory research.
“Compared to rodents and birds, non-human primates have received relatively little attention in episodic-like memory research.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationRats' success in Eacott et al.'s task allowed the authors to conclude that rats recollected the what, where and which of a past episode.
“Rats’ success in this task allowed the authors to conclude that rats recollected the what, where and which of a past episode.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Eacott et al. 2005 source
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Study design and conductown dataOur reduced sample size does not allow us to carry out more fine-grained analyses to tell apart differences between the great ape species included in this study and the developmental patterns in this memory system.
“It is precisely our reduced sample size that does not allow us to carry out more fine-grained analyses in order to tell apart differences between the great ape species included in this study and the developmental patterns in this memory system.”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationown dataApes chose more often the frozen juice in the platform baited last because the frozen juice was hidden 5 min ago and was still edible.
“Likewise, they chose more often the frozen juice in the platform baited last because the frozen juice was hidden 5 min ago and was, therefore, still edible.”
Quote in the paperSubstantial claim- Rests on an assumption: Frozen juice hidden 1 h earlier had melted and was not edible, while frozen juice hidden 5 min earlier was still edible.
Classified as probably not a substantial claim.
PremisecitationFamiliarity is a recognition process that provides a temporal cue for knowing which food item will be available without actually recollecting the past event.
“Familiarity is a recognition process that provides a temporal cue for knowing which food item will be available without actually recollecting the past event (Kort et al. 2005).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Kort et al. 2005 source
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Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductnone givenThe order of the 5 min and 1-h trials and the baited sites on the platform were counterbalanced across subjects.
“The order of the 5 min and 1-h trials and the baited sites on the platform were counterbalanced across subjects.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S4 (based).
PremisereasoningAn animal using a where-what-when representation would be unable to discriminate two episodes sharing the same 'what' because the 'where' and the 'when' components are not directly connected.
“As a consequence, an animal using this representation would be unable to discriminate two episodes sharing the same “what” because the “where” and the “when” components are not directly connected.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S4 (based).
Premisenone givenAn inverted U-shape distribution is a feature of episodic memory in humans.
“Second, an inverted U-shape distribution is a feature of episodic memory in humans.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationFriedman (1993) described three types of information that humans (but also animals) could process: temporal locations, temporal distances, and before-after relations or order of events.
“Friedman (1993) described three types of information that humans (but also animals) could process: temporal locations, which refer to when an event took place within a time pattern; temporal distances, implying how long ago an event occurred and before–after relations or order of events.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Friedman 1993 source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductreasoningThe statistical test in Experiment 2 was one-tailed given that we had an a priori prediction.
“The statistical test was one-tailed given that we had an a priori prediction.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenThe nature of Experiment 2 was confirmatory.
“The nature of this experiment was confirmatory.”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationown dataThe results of Experiment 2 confirmed the findings from the first experiment, that is, subjects' choices are mediated by the temporal information.
“The results of this experiment confirmed the findings from the first experiment, that is, subjects’ choices are mediated by the temporal information.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Interpretationnone givenThe mechanism that apes used to keep track of time and the nature of the temporal representation of past events remains undetermined.
“However, the mechanism that apes used to keep track of time and the nature of the temporal representation of the past events remains undetermined.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S1 (asserted), S4 (based).
Premisenone givenIf the three components occurred in an integrated representation, interrogating any episodic memory for any feature of the event will retrieve the other two features.
“If the three components occurred in an integrated representation, interrogating any episodic memory for any feature of the event will retrieve the other two features.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationResearch on memory for past events in humans has shown that there is no evidence that events are coded by the times of their occurrence or that memory is temporally organised.
“Research on memory for the past events in humans has shown that there is no evidence that events are coded by the times of their occurrence or that memory is temporally organised (Friedman 1993, 2004).”
Quote in the paperNot a substantial claim0 of 2 sources checked
The paper relies on this without support.
Frozen juice remains available/edible after 5 min but melts and becomes unobtainable after 1 h.
“The frozen juice was still available after 5 min but melted after 1 h and became unobtainable.”
“After 1 h, the frozen juice melted and became unobtainable, but it was still edible if chosen after 5 min.”
The paper relies on this without support.
The grape is a non-perishable food.
“less preferred but non-perishable food (grape)”
The paper relies on this without support.
Chimpanzees, bonobos and orangutans represent our closest and most distant great ape relatives, respectively.
“We tested chimpanzees, bonobos and orangutans because they represent our closest and most distant great ape relatives, respectively.”
The paper relies on this without support.
Frozen juice hidden 1 h earlier had melted and was not edible, while frozen juice hidden 5 min earlier was still edible.
“the frozen juice hidden in that platform was baited 1 h earlier and, therefore, had melted”
“the frozen juice was hidden 5 min ago and was, therefore, still edible”
The paper relies on this without support.
Apes prefer frozen juice over grapes when both are available.
“they should preferentially choose the frozen juice in the table baited last but the grape in the table baited first”
The paper relies on this without support.
The orangutan's significant reversal of choices in the last round of Experiment 1 indicates that her choices were based on how long ago the baiting event took place.
“We included one of the orangutans because in the last round of Experiment 1 she significantly reversed her choices (χ 2 = 6, p = 0.014; see table 1 for more details).”
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?
Studies using the what-where-when paradigm predominantly focus on the content criterion, and there is little evidence for the structure and flexibility criteria in the literature.
“these predominantly focus on the content criterion, and as a result, there is little evidence for the structure (but see [68,75]) and flexibility (but see [74]) criteria in the literature.”
From Is episodic-like memory <i>like</i> episodic memory? (2024) · cites this paper as [75]
Older dogs and apes show lower performances in an incidental encoding and what-where-when test, respectively, compared with younger conspecifics.
“Furthermore, older dogs and apes who were otherwise healthy showed lower performances in an incidental encoding and what–where–when test, respectively, compared with younger conspecifics [75,146].”
From Is episodic-like memory <i>like</i> episodic memory? (2024) · cites this paper as [75]
The same binding of multiple event features, permitting discrimination between two similar events, has also been demonstrated in rats and apes.
“The same binding of multiple event features, permitting the discrimination between two similar events, has also been demonstrated in rats and apes [68,75].”
From Is episodic-like memory <i>like</i> episodic memory? (2024) · cites this paper as [75]
Some studies use non-natural methodological elements to test for episodic-like memory, such as pecking or approaching shapes or coloured panels, or requiring subjects to recall their own or others' previous actions out of an array of behaviours.
“Some studies, however, use non-natural methodological elements to test for episodic-like memory [75], such as pecking or approaching certain shapes or coloured panels that are presented in front of the subjects [56,78–81], or requiring subjects to recall their own or others’ previous actions out of an array of behaviours [95,96].”
From Is episodic-like memory <i>like</i> episodic memory? (2024) · cites this paper as [75]
Statistics recomputed
Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.
- Consistentz = 3.12reported p = .002 · recomputed p = .002
“z = 3.12, p = .002”
- Consistentz = 2.55reported p = .011 · recomputed p = .011
“z = 2.55, p = .011”
- Consistentz = 1.79reported p = .037 · recomputed p = .073
“z = 1.79, p = .037”
The paper states a one-tailed test
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
The 24-hour pre-test was less accurate than the 2-minute pre-test
MajorTable 1 shows 100% accuracy at 2 minutes for every subject, but several subjects scored below 100% at 24 hours. The claim of equal accuracy underpins the paper's argument that there was no noticeable forgetting.
“they were as accurate at remembering where an item was hidden after 24 h as they were after 2 min.”
“| Fraukje | Pan troglodytes | 31 | 100 | 100 | 100 | 33.33 | 88.88 | 83.34 | 0.23 | NS | NT | NT | | Padanaa | Pongo pygmaeus | 10 | 100 | 100 | 100 | 66.66 | 100 | 77.23 | 0.58 | NS | 100 | 50 |”
Experiment 2 percentages for Fifi do not fit six trials
MinorEach Experiment 2 trial included a choice from both platforms, so six trials would yield six choices for each reported platform percentage. Fifi's reported 80% and 20% are not possible proportions of six choices; they correspond to proportions of five.
“Subjects received a total of 6 trials, 3 per condition.”
“| Fifi | Pan troglodytes | 14 | 100 | 100 | 100 | 66.66 | 83.33 | 44.45 | 5.9 | 0.035 | 80 | 20 |”
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Language, Memory, and Mental Time Travel: An Evolutionary Perspective
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Great ape foresight is looking great
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EPS Mid-Career Award 2013: Ways of thinking: From crows to children and back again
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Self-citationIs episodic-like memory <i>like</i> episodic memory?
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- Authors
- Martin-Ordas, G., Haun, D., Colmenares, F., & Call, J.
- Affiliations
- Max Planck Institute for Evolutionary Anthropology (DE)
- Universidad Complutense de Madrid (ES)
- Venue
- Animal Cognition
- Published
- 2009-09-27
- Volume
- 13
- Issue
- 2
- Pages
- 331-340
- ISSN
- 1435-9448 (ISSN-L)
- 1435-9456
- PMC
- PMC2822233
- OpenAlex
- W2165494708
- Semantic Scholar
- 448390e361ed5bf7a1a2721c8b62068b1f5cf1b0
- Cited by
- 244
- References
- 69
- Citations by year
- 2026: 14 · 2025: 9 · 2024: 11 · 2023: 14 · 2022: 12 · 2021: 22 · 2020: 14 · 2019: 35 · 2018: 8 · 2017: 23 · 2016: 6 · 2015: 14 · 2014: 17 · 2013: 10 · 2012: 12
- FWCI
- 15.04
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Animal Cognition (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- Max Planck Digital Library (submittedVersion, other-oa)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Social Sciences › Psychology › Developmental and Educational Psychology › Child and Animal Learning Development
- Keywords
- episodic-like memory, great apes, chimpanzees, bonobos, orangutans, temporal memory, temporal coding, age differences
- MeSH terms
- Animals, Pan troglodytes, Feeding Behavior, Female, Food Preferences, Male, Pongo pygmaeus, Mental Recall, Time Factors, Time Perception, Hominidae, Pan paniscus
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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.
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