Behavioural Research 215 (2010) 292–298

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Behavioural Brain Research

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Research report Behavioural evidence for mental travel in nonhuman animals

Thomas Suddendorf ∗, Michael C. Corballis

School of , University of Queensland, Brisbane, Qld 4072, Australia article info abstract

Article history: If episodic is an adaptation, it must have evolved to benefit present or future survival and repro- Received 25 September 2009 duction, rather than to provide an accurate record of the past per se. Recent research has documented Received in revised form various links between the ability to construct episodes of the past and imagine potential future episodes, 25 November 2009 and it has been argued that the former may be a design feature of the latter. Thus, claims about the exis- Accepted 27 November 2009 tence of in non-verbal organisms may be evaluated by examining behavioural evidence Available online 3 December 2009 for foresight. Here we review recent data on foresight in animals and conclude that the evidence to sug- gest episodic memory so far is equivocal. We suggest specific experimental criteria that could provide Keywords: Episodic memory stronger evidence. We maintain that there must be uniquely traits for which there are no animal Episodic-like memory models and it remains possible that depends on several such traits. Identification of Foresight what precisely is unique about the human capacity and what is not, can inform us about the nature and Memory systems evolution of the human capacities. Mental time travel © 2009 Elsevier B.V. All rights reserved. Planning www-memory

1. Introduction 2. Looking to the future as evidence for memory

Can nonhuman animals imagine the world of tomorrow? Can Memory research typically involves a study phase and the main they regret what they did last month and envision doing it better dependent variable is accuracy of retrieval. From an evolutionary next year? Research is beginning to address whether nonhuman perspective, however, memory capacities can only be selected on animals might be able to travel mentally in time, and if so, to the basis of what they contribute to survival and reproduction, what extent. Although this special issue is dedicated to the study whether or not they accurately reflect the past [1]. This perspective of episodic memory, we will focus here on evidence for thinking might explain why our memory of past events is frequently inaccu- about future events. Foresight requires some memory capacities, rate; subject to bias, decay and suggestion [9,10]. It may even be the and memory systems have been shaped, in part, by natural selection case that episodic memory is merely an adaptive design feature of for better prediction [1]. Thus, future-directed actions may repre- the ability to conceive of future events [11,10]. In other words, we sent behavioural expressions for certain memory capacities. The may be able to recollect past events only because this mechanism current interest in studying “episodic-like” memory in nonhuman allows us to imagine future events. But that proposal is difficult animals, in particular, has brought to the fore the need to estab- to assess and there are other ways in which episodic memory may lish behavioural indicators of episodic memory. Here we discuss increase fitness (e.g., allowing us to learn from the same event more the logic of this approach and review the state of the current evi- than once [12]). Be that as it may, there is a strong case for the so- dence. Recent work on food-caching birds [2,3] and on great apes called Janus hypothesis [13,14], the idea that mentally conceiving [4,5] suggests that they might have some capacity for flexible fore- of past events and imagining future events are closely linked in sight. However, there is an ongoing debate about what precisely mind and brain [15,1,10,16,17]. these studies have so far demonstrated [6–8]. We respond to this Amnesic patients who cannot recall personally experienced debate, review recent evidence from primate studies and suggest events have been found to have parallel problems with future specific experimental criteria that could help overcome the current events [18–21]. There are also conditions characterised by milder impasse. disturbances in mental access to both past and future events [22,23]. Studies of impairments may of course be misleading; for instance, deficits in episodic memory may be due to a gist- based recall strategy rather than a memorial deficit per se [24]. ∗ Corresponding author. Tel.: +61 7 33658341; fax: +61 7 33654466. However, commonalities between episodic memory and fore- E-mail address: [email protected] (T. Suddendorf). sight are increasingly documented in other contexts. Mental time

0166-4328/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.bbr.2009.11.044 T. Suddendorf, M.C. Corballis / Behavioural Brain Research 215 (2010) 292–298 293 travels into past and future have phenomenological similarities Furthermore, Clayton and colleagues refer to “episodic-like [25,26] and share various distribution characteristics [27]. Imag- memory” in acknowledgment of the fact that these paradigms do ining more distant events typically leads to more abstract and not test the subjective feel (i.e., autonoetic ) that is de-contextualized scenarios than events closer in time [26,28]. essential to meet the current definition of human episodic memory There are links in how young children acquire episodic memory [21]. One reason human episodic memory is no longer charac- and episodic future thinking [29–31], and there is a parallel decline terised as memory for what where and when information is that in past and future mental time travel detail with advanced age [32]. there is a double dissociation here [11]. People can report what, Finally, there is growing evidence for a strong overlap in the brain where and when information about events (e.g., the shooting of areas implicated in episodic memory retrieval and imagining future Abraham Lincoln; one’s birth) without being able to mentally relive events. FMRI and PET studies point to regions of the medial pre- the events. Conversely, because episodic retrieval is based on active frontal cortex, and lateral and medial parts of the parietal cortex reconstruction and is characterised by various biases and errors, and temporal lobes (e.g. [33–36]). veracity of what, where and when information is not its hallmark. The fact that these links are there does not of course mean that That is, one may recall a particular event and yet be factually wrong there are no profound differences. Obviously, episodic memory in its www specifics. Evidence for retention of accurate www infor- refers to events that have happened whereas the future has not mation is not equivalent to evidence for episodic memory. For this, yet eventuated, and in fact may often never eventuate the way it and some other reasons, convincing evidence for episodic memory was imagined. Not surprisingly, there must be important differ- in nonhuman animals has remained elusive [1]. ences in the cognitive processes involved in mental time travel If researchers find it difficult to establish clear signs of episodic into the past and future (see [37], for review). Nonetheless, if the memory in animals, then how could natural selection have differ- Janus hypothesis is correct, then evidence for the latter may also entiated between an individual that has semantic or procedural be regarded as evidence for the former. This opens up an unusual memory and one that has episodic memory? Unless episodic mem- way of behaviourally examining episodic memory in nonhuman ory is a mere side product, or spandrel, there must be something animals [38,16]. enhancing fitness for it to be selected and it is difficult to conceive that this is merely the subjective feel at retrieval (i.e., autonoetic consciousness). What could be a tangible, demonstrable effect on 3. Testing episodic memory survival or reproduction? As foreshadowed at the beginning, a memory system can be selected on the basis of what it contributes In adult episodic memory is generally assessed through to future survival and reproduction—foresight can offer serious -reports. Much of human conversation involves recounting past adaptive advantages [38,11]. episodes and planning future events. Tulving [21] argued that retrieval from episodic memory is accompanied with self-knowing, or “autonoetic”, consciousness (“this happened to me”). This intro- 4. Foresight in nonhuman animals spective experience of remembering past events, according to Tulving, is the key defining characteristic of episodic recall. While Current behaviour can not only influence current fitness, but such a phenomenological approach has led to useful research with also increase or decrease future survival and reproduction chances. human participants who, for example, can be asked to report if Thus, there is a range of future-directed capacities evident in the they remember or merely know something [39,40], it is not read- animal kingdom. Mechanisms that can track significant regular- ily transferable to non-linguistic subjects. Thus, without language ities such as when and where food or reproductive partners are there may be little hope of ever establishing evidence for autonoetic available are adaptive. Some species have adapted to fundamen- consciousness and hence, by this definition, episodic memory in tal long-term regularities such as severe seasonal changes through animals [41]. This may not be entirely impossible though. Sudden- profound, but relatively fixed, future-directed instincts (e.g., hiber- dorf and Busby [11] pointed out some ways in which nonhuman nation). For instance, E. coli bacteria travel through the human animals could in principle have the means to report past experi- digestive tract from a lactose-rich to a maltose-rich environment ences, but no convincing evidence has yet emerged. Nevertheless, and it has recently been documented that they, when in the for- it is not clear whether nonhuman animals do not have autonoetic mer, prepare for the latter by activating genes for digesting maltose consciousness, or whether some of them do have it and researchers [54]. This does not mean that each individual bacterium plans have not yet been able to demonstrate this. ahead. Natural selection has shaped this behaviour in all E. coli. In light of these difficulties, many comparative researchers have It is an innate response to recurrent, long-term regularities of returned to Tulving’s discarded initial definition of episodic mem- the order of significant events. But the temporal orders of signif- ory: memory for what happened where and when [42]. Clayton icant events are not always sufficiently regular for an organism and Dickinson showed that it is possible to examine memory for to adapt to. Some change quickly (e.g., some food sources) and this kind of information in non-verbal paradigms with food-caching an organism that can adjust its behaviour accordingly would have scrub jays [43]. They showed that these birds adjust their behaviour an advantage. Thus, mechanisms differ in the degree of flexibility according to what food was stored where and when. Many studies they impute on individuals. Critical periods for parameter setting, [44–47,1,48] have since adopted this approach arguing for what, imprinting, and indeed all forms of may be regarded as where, when memory in species ranging from mice [49] to bees future-oriented mechanisms that allow individuals, rather than [50]. In spite of this prolific spread of what we might call the populations, to adapt to local regularities. Different memory sys- www-memory approach there are reasons to be cautious with the tems may enable different future-directed potential and episodic comparison to human episodic memory [51,52,11]. One important memory is arguably the most flexible [1]. issue is the question of whether the “when” information in these Mental time travel enables humans to re-experience and pre- paradigms represents the time of a past event or whether sim- experience virtually any possible event. We can imagine future pler mechanisms, such as the decaying strength of a memory trace, situations and deduce the consequences for current choices. We may be sufficient to explain the behaviour [47,53,1]. Rats have been can escape our current state and imagine a different state of the shown to record how long ago food was found, rather than when world and of ourselves. Much of human success depends on our it was found, a process that need not imply mental travel into the foresight and this capacity may have been a key survival strategy past [53]. [55]. To what extent other organisms use this strategy is beginning 294 T. Suddendorf, M.C. Corballis / Behavioural Brain Research 215 (2010) 292–298 to attract serious study. It may be that only humans have a mental and hence ultimately control what happens to the food. Finally, we time travel faculty [10]. Alternatively, it could be that other species [7] note that all reported competence in jays so far is restricted to are somehow constrained in their ability. For example, they may the domain of food caching and retrieval, and shows none of the anticipate future events only to the extent that the future relates to domain general flexibility characteristic of humans foresight. Like the satisfaction of current drives and needs. This idea is known as other nonhuman animals, they appear to display what Cheney and the Bischof-Köhler hypothesis [56,57,10]. There may be a range of Seyfarth [60] called a “laser-beam intelligence”. other limits and different species may be limited in different ways Still, within the domain of caching and retrieving scrub jays have [1]. It is of course also possible that some other species share the been demonstrated to have surprising future-directed capacities ability to travel mentally in time. If so, however, then we would still and we suspect that other caching specialist will have similar skills. need to explain why only humans seem to take radical advantage Regardless of how much they do or do not resemble human fore- of this foresight? sight, the mechanisms underlying such future-directed capacities deserve greater empirical attention [1,46]. 4.1. Scrub jays 4.2. Primates Caching food, as scrub jays and many other animals do, is inher- ently a future-directed activity. But it remains unclear to what Homologues of the human capacity, however, are more likely to extent these animals think about the future retrieval when they be found in our closest primate relatives. One study with squirrel are engaged in caching. Correia et al. [2] have recently claimed to monkeys suggested that these new world monkeys might be able have refuted the Bischof-Köhler hypothesis by demonstrating that to anticipate future thirst. Naqshbandi and Roberts [61] gave two scrub jays cache food specifically for an anticipated future need. The monkeys a choice between 1 and 4 pieces of dates. When the sub- authors took advantage of specific satiety – when eating a lot of one jects chose 4 pieces they were not given access to water for 3 h and if type of food the desire for more of this food declines – to show that they selected 1 piece water supply was available after half an hour. jays, while not desiring a certain food now cache this food for a Eating dates induces thirst. Over repeated trials the monkeys, but future desire. Scrub jays were prefed with one type of food (A) for not rats, began to choose 1 piece rather than 4 pieces. The authors 3 h and then allowed to cache this prefed food and a different kind claim that this contradicts the Bischof-Köhler hypothesis because of food (B). Next, the birds were prefed with food B before being the monkeys took their future thirst into account. However, the allowed to recover what they had originally cached. After two and repeated exposure and gradual change suggests associative learn- three such rounds the jays were said to cache so as to “maximize the ing [62]. Furthermore, if they did imagine their future states, it satisfaction of their future motivational state over the current one”, remains unclear why they did not continue to select 4 pieces and thereby arguably refuting the Bischof-Köhler hypothesis. A closer simply not eat them all until water was available [14]. look at the data, however, showed that the birds had not stored Paxton and Hampton [63] recently failed to replicate this finding more of the food that was to become more desirable in the future with 6 rhesus monkeys. Over 4 experiments they did not find any (i.e., of food A) as such an interpretation suggests [7]. The average evidence that these old-world monkeys would change their choice number of items stored for the future stayed at about a mere 1 in light of the availability of future water. The authors thus decided item across the trials (i.e., specifically 0.7; 1.2 and 0.8 respectively). to drop the delay altogether for one of the choices and contrast Clayton et al. [6] responded that the relative number of these items this with a larger choice that would lead to water in 3 h. Only in stored increased when compared to the number of items cached of this experiment did the monkeys learn to select the smaller num- food B, and that this relative change is in contrast to an incentive ber of date pieces. The authors conclude, perhaps with tongue in learning account which would predict that both foods should be cheek, that this technically violates the Bischof-Köhler hypothesis stored equally. However, this change in proportional caching was because, in spite of the very short interval between selection and driven solely by the fact that the birds stopped caching food B, and water supply, the monkeys were not thirsty at selection. However, not by an increase in caching food A, and there may be any number the choice the monkeys faced was between 1 date piece and water of reasons why they might have done so. Although thinking about versus 4 date pieces and no water, and thus their behaviour can the future might be one of them, there is no evidence here that the easily be explained in terms of operant conditioning. Indeed, the birds increasingly cached the food that would become desirable in authors concede that a learning account can explain these find- the future. ings as well as the un-replicated results of Naqshbandi and Roberts There were other methodological problems that have been [61]. It is not clear whether the rhesus monkeys failed because of raised about this and similar recent studies [7]. But we agree that not being able to imagine their future thirst, or because they sim- the use of specific satiety might be a promising avenue of study ply could not learn the association between their choice and the even if the current data are not entirely convincing. Another study delayed availability of water. As Paxton and Hampton note, tradi- in which jays allegedly “plan” breakfast [3] was criticized for lump- tional learning theory emphasizes temporal contiguity. ing together the performance of the four birds that did have reason Humans, however, clearly can learn to form associations to expect to be given breakfast the next day and those four birds between events that are temporally far removed from each other. that did not [7]. In response, Clayton and colleagues state that “The And human behaviour often reflects considerations of long-term birds had only had three experiences of each condition and there- future consequence. For instance, humans regularly forgo an fore it is highly unlikely that they would have learnt a specific instant reward in favour of a more desirable long-term future goal alternation pattern in that time.” (p. e10) [6]. In other words, the (though this is by no means an easy feat, as anyone who has been on authors concede that the birds did not have a specific expectation a diet can attest). Recent comparative research has demonstrated about what will happen tomorrow. Instead, their clever behaviour that great apes, humans’ closest living relatives, also have at least may be based on simpler caching heuristics [58]. It may even be some competence in this regard. When given the choice between questioned more generally to what extent the caching and pilfer- a small reward now and a larger reward later, monkeys, like most ing avoidance strategies of jays make sense in a laboratory, given other animals, find it difficult to wait if the delay is more than a that humans, not other jays, control food and caches [7]. It is true few seconds, but recent studies on great apes have demonstrated (contrary to what we claimed [7]) that some of the birds have seen that they can delay gratification in the order of minutes [64–66].In other birds pilfer their caches [59], but it remains the case that one study, waited for up to 8 min to receive a reward it is always humans who provide and remove the caching trays that was 40 larger than the other reward [65]. Thus, humans’ T. Suddendorf, M.C. Corballis / Behavioural Brain Research 215 (2010) 292–298 295 closest relatives do seem to share some unusual future-directed suggest that even in modest foresight situations in which the right capacities. However, it also needs to be acknowledged that humans future-directed selection is always the same object, great apes do can be observed delaying gratification for months, years and even surprisingly poorly. life-times (e.g., consider celibacy). Dufour and Sterck [68], for example, although reporting a par- Wolfgang Köhler pioneered work on the possibility that chim- tial replication of the Mulcahy and Call finding with chimpanzees, panzees may solve problems in their minds rather than only failed to find evidence for simple planning in a series of four ded- through associative trial and error learning. Nonetheless his icated studies. They trained 10 chimpanzees to exchange a token research compelled him to conclude that: “The time in which the for a food reward over 20 consecutive days to clearly establish the lives’ is limited in past and future” [67], p. 272). Ninety relationship. Subjects were then given the opportunity to collect years later, researchers at the Wolfgang Köhler Primate Research the tokens in anticipation of an exchange session an hour later. Center in Leipzig produced the best evidence yet that some great Given the results discussed above one would expect at least some of apes may be able to plan up to 14 h ahead. Mulcahy and Call them to prepare for the future situation. However, the chimpanzees [4] trained 3 bonobos and 3 orangutans to use a tool to obtain a did not collect and bring the token to the test compartment for the food reward from a feeder apparatus. A plexi-glass panel was then exchange any more than any of the distracter items that were avail- installed to block access to the apparatus. The target tool and other able. The few occasions on which they did bring a token, and hence distracter items were present in the room and the subjects could were rewarded, were not followed by subsequent successes, sug- take any of these objects with them when they were ushered into gesting that the behaviour was due to chance rather than learning a waiting room. The objects not carried out of the test room were or foresight. If foresight, even extending only a few hours into the then removed by the experimenter. Subjects were let back into the future were commonplace, one would expect to see frequent and testing room after an hour and the plexi-glass panel was removed. consistent evidence for this in experiments and in the field. Yet, On almost half of the trials subjects carried the target tool to the there has been a marked scarcity of such accounts. waiting room and returned with it an hour later to obtain the food Thus, an unusual recent observation suggesting that a chim- reward. There were large individual differences in performance. panzee might have planned several hours in advance led to great The best performing orangutan and bonobo were given another excitement. Osvath [69] interviewed three zoo keepers who had such test with the waiting being extended over night and they suc- observed a male chimpanzee apparently planning for future dom- ceeded in returning with the target tool. Although this does not inance displays. The keepers reported that he calmly collected prove that Köhler was wrong and that there is no limit to the time objects into piles early in the morning and a few hours later used that apes live in, it does suggest that these apes could think about them as projectiles to hurl at gathering zoo visitors. The author a more remote future than previously evident. argues that this demonstrates future-need anticipation. However, However, because the apes had to select the same tool on all in the absence of systematic studies, it is difficult to assess what has trials, it is not clear whether they anticipated a specific future sit- caused the behaviour. The report of past observations alone can- uation or whether their behaviour can be explained in terms of not conclusively establish whether the chimpanzee had in mind more general learning principles. The authors report a control con- future throwing when he collected the objects. Controlled experi- dition given to 4 naïve subjects that did not have any learning ments (e.g., systematically contrasting situations when there will history of which tool is useful. Their performance, however, was be visitors and those when it can be predicted that there will not not informative because two of them did not get an opportunity be) are required to determine the nature of the cognitive processes to learn the contingencies, and the other two performed exactly involved. Nonetheless, this is a curious report that has drawn a as did two individuals in the experimental condition [55]. Ideally, lot of international attention. Nothing quite like it has as yet been a learning account would be circumvented by using single trials reported from the wild, nor, for that matter, from any other cap- with novel items, rather than using the same problem and solu- tive chimpanzees. If such foresight capacities are part of the normal tion over repeated trials given to the same subjects (see below). cognitive repertoire of great apes, one would expect to hear about However, that is difficult to do without large numbers of subjects. many more such examples. Perhaps this is indeed what awaits us One way to improve the case for a richer interpretation would be in the future and this report will trigger an avalanche of similar to include control conditions to show that the apes do not always accounts from zoos and field stations. select the tool, but do so only for specific anticipated future situa- It would, of course, not be too surprising to find that our closest tions. For example, one of the distracter items could be made the living relatives have at least some of the capacity that we humans target tool in some trials. Without such controls it remains unclear employ to such great effect. Limited evidence from nonhuman what drove the performance of those apes that returned with the species may imply a continuum, echoing Darwin’s [70] remark that target tool [55]. “... the difference in mind between man and the higher animals, Repetition of the same tool-problem relationship also is a con- great as it is, certainly is one of degree and not of kind” (p. 126). cern for a subsequent study on two chimpanzees and one orangutan This may turn out to be the case, but the evidence so far suggests by Osvath and Osvath [5]. These authors found that the apes could to us that there is something uniquely human about mental time select a straw tool that was needed 70 min later to suck up fruit travel. If more such reports emerge it is to be hoped that they will be juice. However, prior to testing, all three subjects were given an followed up with controlled experiments to determine the mech- opportunity to learn this relationship. Hence, experimental sub- anisms involved. Given the critiques of earlier experiments, this jects went into test trials with experience of associating the straw raises the question of how experiments could establish that great and half a litre of fruit juice, whereas three control subjects were not apes have the kind of foresight that implies episodic memory. given this same initial learning experience [8]. The observed differ- ence between the choices of the experimental and control groups 5. Experimental criteria may hence be due to this difference in learning history. Difficul- ties associated with control conditions also afflict their subsequent Tulving [16] and Suddendorf [71,38] have discussed experi- experiments in which the experimental apes selected tools that mental criteria and proposed behavioural tests. Building on these allowed them later to drink fruit juice [8]. Together with the results considerations, as well as on the critiques of the innovative animal from Mulcahy and Call [4], however, these studies do raise the pos- studies that have been conducted thus far, we suggest that future sibility that great apes can think about what will happen in the research consider the following four criteria in designing future relatively near future. Other results, on the other hand, continue to studies. 296 T. Suddendorf, M.C. Corballis / Behavioural Brain Research 215 (2010) 292–298

Firstly, we recommend the use of single trials. This avoids have mental time travel, one could use them as animal models to repeated exposure to the same stimulus-reward relationships and study neurophysiology, impairments and so forth. However, if the hence critiques related to this. It also is crucial in establishing that initial assumption is not correct, such work will miss its intended behaviour is driven by memory for a single specific event, and not target. based on generalisations. Secondly, we advocate the use of novel problems. This avoids the influence of potential innate response tendencies as well as poten- 6. Animal models tially relevant individual learning histories. Success on single, novel trials substantiates the claim that cognitive processes are driving This special issue is testament to the recent surge in stud- the action. This is important both for studies on test naïve animals, ies examining animal models of human episodic memory. No as it is usually impossibly to know what the animal in question has doubt some essential components of human episodic memory and experienced in the past, as well as for studies on animals that are foresight have animal parallels. For instance, there are probably part of a research colony, and who thus typically have extensive homologue characteristics of the hippocampus that humans and experience in similar experiments. other mammals share [84]. Recent studies on hippocampal place Thirdly, we advise the use of clear temporal–spatial separation cells suggest a role not only just in memory but also in prediction. between the future-directed action and its consequence. Spatial Recordings from rats in a familiar maze suggest that at decision separation is important to avoid any potential cuing. Sufficient tem- points place cells fire as if the rat were mentally sweeping ahead to poral separation is necessary to ensure that the behaviour draws examine the options [85,86]. The potential prospection here is of on long-term memory, rather than on working memory. course only seconds into the future, but may well be a fundamen- Finally, we suggest that problems from a range of domains are tal building block that humans use when envisioning future events. employed. This can counter arguments that innate behavioural pre- Nonetheless, these successes should not blind us to the possibility dispositions drive the action. And diverse contexts are necessary that other important components of the human capacity may not to demonstrate the flexibility that is so characteristic of human have any nonhuman parallels [1]. foresight. There must be some characteristics of the human mind that are Experiments that employ these criteria could provide strong uniquely human and these traits may be called human’s cognitive behavioural evidence for foresight and episodic memory. A recent autapomorphies [87]. These are traits that set us apart and define developmental study has demonstrated such evidence in children us. Syntactic language is often considered to be the prime example from age 4 who remembered single, novel problems sufficiently to (e.g. [88]). Mental time travel may be another example and human secure their future solution [72]. These suggestions do not mean language seems ideally adapted to allow us to communicate these to imply, however, that behaviours that do not reflect these crite- travels [89,90]. Indeed, language may have evolved precisely for ria are not based on mental time travel. They may well be. Indeed, this purpose, since it includes symbolic representations to allow it has been rightly argued that much of human planning may not reference to non-present events, marker to indicate space and time, meet the strict criteria that have been suggested for animal studies and recursive rules to allow elements to be combined in different [46,63]. The reason to be so conservative about the animal data is ways. The flexibility and generativity of both mental time travel that in the absence of language it is much more difficult to establish and language are fundamental to human culture and civilisation. what goes on in an animal’s mind. As yet no other animals have been shown to demonstrate anything The ongoing thirty-year-old debate about whether nonhuman comparable. And thus, animal models of these faculties may only animals have a illustrates this difficulty. Recent ever be of limited use. research efforts at the Wolfgang Köhler Primate Research Centre In setting criteria for demonstrating mental time travel in non- suggest that great apes understand something about others’ minds, human species, it may appear that we have neglected to provide including goals [73], intentions [74], seeing [75] and knowing [76]. appropriate criteria for humans. But language provides the evi- Yet, some researchers remain entirely unconvinced that great apes dence in countless ways. Each time you agree with another that you have anything like a theory of mind [77,78]. The reason these crit- will do something (e.g. “Let’s meet next Tuesday at your place to dis- ics can remain sceptical is that great apes have not as yet met the cuss the progress”), and you end up doing it, it is clear behavioural strict behavioural criteria necessary for distinguishing action that evidence. This is not to claim that we are perfect at it, that we is based on reasoning about minds from those of reasoning about are making the right decisions or that it is easy. Moreover, future other regularities. When Premack and Woodruff [79] proposed the behaviour is not always established in this way. We sometimes do possibility that chimpanzees might have a theory of mind, three not follow up on planned intentions, and foresight can fail to pre- independent commentators [80–82] immediately realized that to vent us from reverting to bad habits, like smoking or drinking too behaviourally demonstrate that someone is acting on the basis of a much. Our point is simply that mental time travel provides a novel, theory of mind one really needs to show that they appreciate that powerful mechanism for fine-tuning our lives, but it is by no means others may mis-represent the world. Tests of apparent understand- the only driver of future behaviour. ing of true beliefs (just as tests of goals, intentions or perceptions), Studying the future-directed capacities of other species is cannot rule out the possibility that subjects behave on the basis of important in its own right. They have been neglected for too long. As some observable contingencies (as true beliefs and reality match). noted above, even if mental time travel is unique to humans many Only the attribution of false beliefs can therefore unequivocally species probably possess other sophisticated mechanisms that reveal an understanding of the representational nature of mind. track regularities and guide future-directed behaviour (e.g., natal It is of course possible that great apes have some theory of mind, homing in turtles). These may even offer solutions for human engi- just not what it takes to pass the false-belief task. Indeed, we think neering problems, just as the study of bee navigation has produced they might do [83]. But it is true that experiments have not yet simple but effective approaches to aircraft navigation [91,92]. And unequivocally demonstrated that great apes have a theory of mind. such research efforts can also indirectly provide vital information Something similar might be in store for our much younger to our understanding of the human capacities. A systematic com- debate. It is important to think carefully about what criteria need parative approach mapping the extent to which humans and their to be met to ascribe episodic memory or foresight. It is tempting close relatives share homologous memory and foresight capacities, to accept initial empirical evidence as conclusive proof and move and what precisely is distinctly human can inform us not only about on. For example, once one accepts that certain nonhuman animals the evolutionary history of these traits, but also about the genetic T. Suddendorf, M.C. Corballis / Behavioural Brain Research 215 (2010) 292–298 297 and neurological underpinnings. Those traits that are unique to [25] D’Argembeau A, Van der Linden M. 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