Determining the memory systems that support nonhuman animals’ capacity to remember distant past events is currently the focus an intense research effort and a lively debate []. Comparative psychology has largely adopted Tulving’s framework by focusing on whether animals remember what-where-when something happened (i.e., episodic-like memory) []. However, apes have also been reported to recall other episodic components [] after single-trial exposures []. Using a new experimental paradigm we show that chimpanzees and orangutans recalled a tool-finding event that happened four times 3 years earlier (experiment 1) and a tool-finding unique event that happened once 2 weeks earlier (experiment 2). Subjects were able to distinguish these events from other tool-finding events, which indicates binding of relevant temporal-spatial components. Like in human involuntary autobiographical memory, a cued, associative retrieval process triggered apes’ memories: when presented with a particular setup, subjects instantaneously remembered not only where to search for the tools (experiment 1), but also the location of the tool seen only once (experiment 2). The complex nature of the events retrieved, the unexpected and fast retrieval, the long retention intervals involved, and the detection of binding strongly suggest that chimpanzees and orangutans’ memories for past events mirror some of the features of human autobiographical memory.

Results and Discussion

10 Proust M. På Sporet Efter Den Tabte Tid [A la Recherce du Temps Perdu/Remembrance of Things Past]. 11 Tulving E. Elements of Episodic Memory. 12 Rubin C. Autobiographical Memory. 13 Conway M.A.

Pleydell-Pearce C.W. The construction of autobiographical memories in the self-memory system. 14 Berntsen D.

Staugaard S.R.

Sørensen L.M. Why am I remembering this now? Predicting the occurrence of involuntary (spontaneous) episodic memories. 11 Tulving E. Elements of Episodic Memory. 13 Conway M.A.

Pleydell-Pearce C.W. The construction of autobiographical memories in the self-memory system. 15 Mulcahy N.J.

Call J.

Dunbar R.I.M. Gorillas (Gorilla gorilla) and orangutans (Pongo pygmaeus) encode relevant problem features in a tool-using task. 16 Girndt A.

Meier T.

Call J. Task constraints mask great apes’ ability to solve the trap-table task. 17 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. 18 Manrique H.M.

Gross A.N.

Call J. Great apes select tools on the basis of their rigidity. 19 Barsalou L.W. The content and organization of autobiographical memories. 20 Berntsen D. Involuntary autobiographical memories. Figure 1 Experimental Setup Show full caption Setup for the experiment with the chimpanzees (orangutans’ rooms consisted of only four compartments). Locations A and B represent the locations where the boxes to hide the tools were placed (experiment 1). Locations C and D represent the locations where the trays to hide the tool was placed (experiment 2). Room 1 is the room where the task was placed, as well as where the subjects were when experimenter gave them access to the tool locations. See also Figures S1 and S2 In Remembrance of Things Past, Marcel Proust [] described how the unique taste of a petite madeleine dipped in lime tea spontaneously brought to his mind a childhood memory of visiting his aunt Leonie in the mornings and always being offered a madeleine dipped in lime tea. This example nicely illustrates that the activation of autobiographical memories [] can be cue dependent [] and serves to frame our research question. Although some authors emphasize the aspect of conscious experience of the self (i.e., autonoetic awareness) in autobiographical memory [], our study does not address this aspect because this feature cannot be measured in nonhuman animals. Thus, the main goal of experiment 1 was to investigate whether, like in Proust’s example, chimpanzees’ and orangutans’ memories for a complex remote event (i.e., problem solving situation) could be triggered by relevant cues in terms of distinctly overlapping features of the past event. Three years prior to the present study, apes were exposed to a task composed of two events: apes observed an experimenter hiding two different tools in two locations, one tool in each location (tool-hiding event), and later they were presented with an out-of-reach food task (task-presentation event) ( Figure 1 and Figure S1 available online). In order to successfully obtain the reward, apes had to remember the location where the useful tool was hidden, go retrieve it, and use it. Note that chimpanzees and orangutans are proficient at using tools to obtain out-of-reach rewards []. Autobiographical memory research makes a distinction between general and unique events. Whereas unique events refer to events specific in time and place (e.g., your first talk at a conference), general events are considered to be summaries of similar repeated events or events extended in time (e.g., what you normally do and experience when you give talks at conferences) []. Since the event that we are testing here took place four times for a particular task (i.e., platform task) and for a particular set of tools (i.e., length condition) (see the Experimental Procedures ), we refer to it as a general event.

14 Berntsen D.

Staugaard S.R.

Sørensen L.M. Why am I remembering this now? Predicting the occurrence of involuntary (spontaneous) episodic memories. Figure 2 Schematic Representation of Previous Use of the Platform Task Show full caption Illustration of some of the different experiments in which the platform task has been used, the different situations in which the tools have been presented, and some of the experimenters that have used this task. The solid line represents the associative links that subjects had to make in order to successfully search for the tools when they saw the platform task in experiment 1. The dotted lines represent the associations that subjects had to disregard. Research on autobiographical memory has also shown that memories for past events can happen strategically through goal-directed retrieval or involuntarily through associative cueing (henceforth, cued recall). The latter is normally triggered by features of the context present at retrieval, which match distinctive features of the memory []. Thus, in order to activate a memory, a cue is needed that is sufficiently distinct to discriminate a past event from alternatives through association. In our experiment, the unique combination of the rooms where subjects were tested, the experimental setup, and the experimenter provided a unique feature overlap with a past event and thus a highly discriminable cue. This is so because subjects had been tested in the exact same location, with the exact same setup, and with the same experimenter as 3 years earlier. However, in order for this cue combination to activate the relevant memory, subjects had to be able to bind these elements together and ignore a number of irrelevant associative links. Note that the experimenter has tested the apes in other tasks (e.g., tool use, object choice paradigms) and that the rooms are used on daily basis to test the apes by other experimenters in other experimental setups (e.g., cooperation tasks, tool-use tasks), and different experimenters in different experiments have used the present platform task. Thus, individually, each cue had been previously associated with other experimental contexts; only in combination did the features provide high discriminability ( Figure 2 ).

21 Martin-Ordas G.

Atance C.M.

Call J. Remembering in tool-use tasks in children and apes: The role of the information at encoding. We tested 15 chimpanzees and four orangutans ( Table S1 ). Subjects were distributed into two groups: an experimental group (with previous experience in Martin-Ordas, Atance, and Call’s experiment [] and a control group (with no previous experience). Subjects only received one trial. We predicted that if the cues provided at retrieval triggered subjects’ memories for a general event (e.g., in this context tools used to be hidden in locations A and B), apes in the experimental group would search for the tool in those locations.

Our results showed that except for one subject (Pini), the ten remaining subjects in the experimental group searched for the tools in the boxes placed in locations A and B (binomial test, p = 0.012) and none of the control subjects did so (Fisher’s exact test, p < 0.001). Since apes did not witness the tool-hiding event and in the previous experiment the location of the two tools was counterbalanced across the four trials, they could not know where each tool was hidden. We found that subjects’ responses varied depending on which tool they found first (Fisher’s exact test, p = 0.005). Four subjects found the correct tool first and went directly to the platform to use it. Six subjects found first the incorrect tool, rejected it, immediately went to search for the other tool in the second location, and used it. We also analyzed latency to find the tools. Overall, subjects went to retrieve the tools within the first 5 s (median = 4.5; Q1 = 2; Q3 = 38.50), and none of the control subjects did so after 5 min.

Experiment 1 established that chimpanzees and orangutans recalled a general event that happened 3 years ago. However, it still remains an open question whether apes can remember tool-finding events that happened only once and distinguish them from another similar tool-finding events. Experiment 2 examined this possibility by presenting 16 chimpanzees and five orangutans with a unique tool-hiding event (see the Experimental Procedures ). Whereas half of the subjects (experimental group) experienced the tool-hiding and task-presentation events once, the other half (control group) lacked such experience. Two weeks later, all subjects were shown only the task-presentation event. Similar to experiment 1, we predicted that if the cues provided at retrieval triggered subjects’ memories for a unique event, apes in the experimental group would search for the tool in locations C or D ( Figures 1 and S2 ). In addition, experiment 2 helped us to further investigate the issue of binding. If apes encode the relation between the elements of an event and form an integrated representation of the event, interrogating a memory for a distinctive feature of the event (e.g., task) will activate the other features (e.g., where to search for the tools). The binding between the task and where to search for the tools would allow subjects to discriminate between different episodes (i.e., experiment 1 and experiment 2) that share common features (e.g., the location, experimenter). In order to test this possibility, we controlled for subjects’ experience with the tool-finding event in experiment 1 ( Supplemental Experimental Procedures ).

Nine out of ten subjects in the experimental group searched and found the tools in the trays placed in locations C and D (binomial test, p = 0.021), and none of the control subjects searched for the tools (Fisher’s exact test, p < 0.001). Seven out of the nine successful subjects went to the correct location first (binomial test, p = 0.180), and the other two went to the empty location first, then went to the second location, found the tool, and used it. Having more experience with tasks involving tool searching (i.e., tool finding general event in experiment 1) did not affect subjects’ performance (Fisher’s exact test, p = 0.400). Overall, experimental subjects went to retrieve the tools within the first 21 s (median = 21; Q1 = 10; Q3 = 28.50), and none of the control subjects did so after 5 min. Thus, experiment 2 established that subjects remembered a unique tool-hiding event that happened 2 weeks earlier when presented with the relevant cues.

Exploratory behavior cannot explain our results; otherwise, control subjects would also have been able to find the tools during the 5 min that the trials lasted. Additionally, successful subjects went directly (without any exploration) to retrieve the tools immediately after the experimenter gave them access to the rooms where the tools were hidden. Learning to respond to a particular stimulus configuration without having any recollection of the past event is also unlikely because the experimenter, the task used in experiment 1, and the testing rooms had been used in numerous other studies. Furthermore, subjects were exposed only four times (experiment 1) and only once (experiment 2) to those particular stimuli configurations.

22 Eichenbaum H. How does the brain organize memories?. 23 Newcombe N.S.

Lloyd M.E.

Ratliff K.R. Development of episodic and autobiographical memory: a cognitive neuroscience perspective. 24 Chalfonte B.L.

Johnson M.K. Feature memory and binding in young and older adults. The performance of those subjects who had experienced the general event in experiment 1 but not the unique event in experiment 2 is particularly revealing. Contrary to what one would expect according to an explanation based on learning to respond to a particular stimuli configuration, subjects directed their searches toward neither the location where the boxes used to be in experiment 1 nor the trays in experiment 2. Likewise, experimental subjects with experience in both experiments did not direct their searches toward both locations. One could still argue that since the two tasks used in the present experiments required different tools, subjects could have identified the tool they needed for each particular task and then search their memory for the location where such tool was found in the past. However, this explanation does not account for the results from experiment 1 because the same task had been used on several occasions in the same room and the location of the tools varied with the experimenter. Instead, our results suggest that subjects relied on a binding of specific aspects (i.e., experimenter, tool location) of two very similar tool-finding events in a way that allowed them to distinguish between those events. Such binding is often regarded as a constituting component of autobiographical memory in humans [].

4 Babb S.J.

Crystal J.D. Discrimination of what, when and where: implications for episodic-like memory in the rat. 5 Clayton N.S.

Dickinson A. Episodic-like memory during cache recovery by scrub jays. 6 Martin-Ordas G.

Haun D.

Colmenares F.

Call J. Keeping track of time: evidence for episodic-like memory in great apes. 7 Schwartz B.L.

Colon M.R.

Sanchez I.C.

Rodriguez I.A.

Evans S. Single-trial learning of “what” and “who” information in a gorilla (Gorilla gorilla gorilla): implications for episodic memory. 8 Menzel C.R. Unprompted recall and reporting of hidden objects by a chimpanzee (Pan troglodytes) after extended delays. 9 Menzel C.R. Progress in the study of chimpanzee recall and episodic memory. 25 Crystal J.D.

Alford W.T.

Zhou W.

Hohmann A.G. Source memory in the rat. 26 Zentall T.R.

Clement T.S.

Bhatt R.S.

Allen J. Episodic-like memory in pigeons. 8 Menzel C.R. Unprompted recall and reporting of hidden objects by a chimpanzee (Pan troglodytes) after extended delays. The present work differs in important ways of previous studies of long-term memory in nonhuman animals. With regard to the recall of past events [], there are three important differences between previous studies and the current one. First, previous research typically used delays of a week maximum, whereas in our study apes remembered events that happened 2 weeks or 3 years earlier. Second, while most of the previous research investigated the recall a series of repeated unique events, we tested cued recall of a unique and a general event. An important limitation of using repeated trials is that at encoding, subjects could anticipate that they would be tested later and, thus, encode the information semantically []. We negated this possibility to our subjects by assessing their memories unexpectedly, for a general tool-finding event that occurred 3 years earlier. Third, in a free-recall experiment, a chimpanzee remembered what (i.e., food) was where for periods of up to 16 hr []. While our results are consistent with these findings, there are two important differences between the two studies. First, in Menzel’s study, the chimpanzee could have monitored the area in which the food had been hidden but she could not retrieve the food during the retention interval (RI). In contrast, if our subjects had checked the target locations during the RIs (3 years or 2 weeks, depending of the experiment), they would have found no tools there. This is important because it demonstrates that tool retrieval in the memory assessment phases was based on remembering the general or unique event. Second, our results show that apes bound the information about the experimenter-task-tool location and distinguished between similar tool-finding events ( Figure 2 ). This binding hypothesis was not directly tested in Menzel’s study.

27 Beran M.J.

Pate J.L.

Richardson W.K.

Rumbaugh D.M. A chimpanzee’s (Pan troglodytes) long-term retention of lexigrams. 28 Patterson T.L.

Tzeng O.J.L. Long-term memory for abstract concepts in the lowland gorilla. 29 Adachi I.

Anderson J.R.

Fujita K. Reverse-reward learning in squirrel monkeys (Saimiri sciureus): retesting after 5 years, and assessment on qualitative transfer. With regard to long-term retention [], previous studies have only addressed whether subjects have long-term retention for general rules that they may be able to apply in other contexts besides the experimental context in which those rules were acquired. Therefore, a successful response in these experiments did not necessarily require remembering the elements of the context in which that particular task took place. In contrast, in the current study subjects not only remembered how to solve the problem, but also remembered contextual elements. Thus, in order to succeed, subjects had to recall elements of the context in which this particular cue constellation was previously presented and differentiate it from other situations that shared some of those same cues.