Editor’s Note: Today’s post, coming appropriately after yesterday's post on human intuitions about memory, comes from Felicity Muth who blogs at Not Bad Science, and tweets as @FelicityMuth. This post, while it can certainly stand alone, is meant to be read after reading Felicity's contribution to The Guest Blog.

We have known for a number of years now that it is possible for animals to have memories for past events or episodes in their lives as we do. This ‘episodic-like memory’ was originally shown through a series of innovative experiments with scrub jays (see my post today on The Guest Blog!).

The key trait of the western scrub jays used by Clayton and Dickinson in their influential experiments was that the birds had a natural tendency to store food and dig it up at a later date. This was useful for testing them, as this natural behaviour could be used to determine whether the birds remembered what they had stored in the past, where they had stored it, and when they had stored it. This ‘what-where-when’ triad has become somewhat of a gold standard for proving episodic-like memory in animals.

Since the scrub jays, people have looked to see if other animals also possess episodic-like memory. A lot of animals have been shown to be able to also remember what, where and when an event happened, including chimpanzees, orangutans, bonobos, meadow voles and magpies. However, other studies have failed to show episodic memory in animals like rhesus monkeys and rats. Is it really the case that some animals can remember, whereas others just cannot? What seems more likely is that the way in which we ‘ask’ the animals if they remember gives us different results.

In trying to find out whether rhesus monkeys could remember past events, researchers tested the monkeys in a similar way to how the scrub jays had been tested. First the monkeys were given a range of foods to see which ones they liked the most. Each monkey was then assigned two foods: one they liked a lot, and one they liked less so, but would still eat. They then explored a room and found where these two foods were hidden (in two of three possible hiding places). After this, they were kept out of the room for either one hour, or twenty-five hours. After one hour, both foods were still fresh. However, after twenty-five hours the monkey’s preferred food had ‘decayed’ (been replaced with a rotten version by the researcher). The monkeys quickly learned to search for their favourite food first, and to avoid the empty hiding place. However, they were not able to learn that a long delay meant that their favourite food had gone rotten, and they continued to go to the place where this food was hidden. So, it seems that they learned the ‘what’ (their favourite food), the ‘where’ (it was hidden) but not the ‘when’ part of episodic memory. However, even though the monkeys did not remember what happened in this context does not mean that in other contexts they might. In the words of Carl Sagan: absence of evidence is not evidence of absence (although I should point out that he actually said this as an argument against this way of thinking; it’s still a catchy line though).

One of the possible reasons that the rhesus monkeys in this experiment could not remember when the food was hidden could be because these monkeys do not naturally store foods that do and do not decay. Given that all animals are (mostly) adapted to the environments in which they live, the fact that these monkeys do not need to remember these things in the wild is a good reason why they might not be able to do it in the lab. Whilst the experiments with scrub jays showing that they had episodic-like memory were excellent for that species, they may not be entirely suitable for looking at memory in other animals. New original ways of looking for episodic memory are now being designed for other animals, taking advantage of their pre-existing natural behaviours. As the rhesus monkey experiment highlighted, one of the most problematic components of episodic memory is the ‘when’ aspect. What we mean by ‘when?’ might seem obvious at first, but if we actually think about it, it can mean a lot of different things. To take an example, think about when you last ate pasta. You might be remembering ‘when’ as a period of time (like three days ago). However, you might also be thinking about it in relation to other events (when you had dinner with your mum in Pizza Hut, which was a week ago). This other type of ‘when’ has been dubbed ‘in which context’, or just ‘which’, giving us the new catchy definition: ‘what-where-which’.

Among others, Eacott and colleagues have used this definition to look for episodic memory in rats. Just as Nicola Clayton and her colleagues showed episodic memory in scrub jays through using a natural behaviour (their food-storing behaviour), so they used a rat’s natural behaviour to investigate whether it had episodic memory. Rats have a strong tendency to explore novel objects. This means that if they go into a room where they have seen most of the objects there before, but one of them is new, they will go to this object and explore it (mainly through sniffing) more so than any other object. An important aspect of our episodic memory is that we remember events spontaneously, without having to be trained to do so. What is useful about a rat’s behaviour to explore novel objects is that it is also spontaneous, and rats do not have to be trained to do it beforehand.

To test for episodic-like memory in these rats, the scientists placed different objects (‘what’) in different locations in a room (changing the ‘where’), as well as changing the background colour of the room (‘which context’). I’m not entirely sure which objects they used, and since it is not the point of the study, for illustrative purposes let’s say it was a Jesus figurine and a Chewbacca doll. First rats explored a room (for example, an orange room with Jesus on the left and Chewbacca on the right). They then saw the objects again in a different context (for example, a blue room) and switched over (so that Jesus is now on the right). The rats were then put in a context they had experienced previously with two of the same objects. So in my example, this could be an orange room with two Jesuses. The rat has experienced this object (‘what’), these locations (‘where’), and this room (‘which’) before, so by themselves none of these stimuli are novel. However, whilst they had seen Jesus on the left of an orange room before, they had not seen him on the right of an orange room. So, the object on the right is the most novel, and what the rats should explore if they remember what they have previously seen. The rats did indeed do this, integrating the ‘what’, ‘where’ and ‘which’ components into an episodic-like memory.

One limitation of this experiment was that the rat could always see all the components of it’s memory, and could use these cues as a reminder of what it had seen previously. To make sure the rats really were recollecting past experiences, the scientists went on to test the rats again in a similar set-up, but this time one where they could not see the objects. In this new set-up, rats were trained in two different ‘which’ contexts (a maze that was smooth and black, or covered in wire mesh) where there were two different objects hidden. During the training, the rats learned where each object was in each context (for example, ‘In the black maze Jesus is hidden to the left and Chewbacca is hidden to the right, and in the wire-mesh maze Jesus is hidden to the right and Chewbacca to the left’). The rats were then taken out of the maze and put in their holding cage with one of the objects, for example the Jesus figurine, for eight minutes. If the rat was not converted to Christianity in this time, it would have at least become habituated to the object. This meant that when the rat was put back into the maze (say the black maze), its natural tendency was to want to explore the other object (Chewbacca), as it was more novel. In order to do this, they had to recollect that in the black maze, Chewbacca was hidden on the right and to run to this location to find it. In other words, the rats had to remember ‘where’ the (‘what’) object was, in this (‘which’) context.

The rats were indeed able to do this. This is an exciting finding as it another example of episodic-like memory in other animals apart from ourselves, discovered using a behaviour spontaneously produced by the animal. This finding is also exciting as rats are a model organism for human diseases like Alzheimer’s, which affect episodic memory. Now that we have a way of testing for episodic memory in the rat, it means that we can see how it is affected when different parts of the brain are damaged (as they are by disease). The neurological side of this behaviour is already being looked into in depth, and I am looking forward to seeing the new discoveries in this field in the coming years.

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Bird, L.R., Roberts, W.A., Abroms, B., Kit, K.A. & Crupi, C. (2003) Spatial memory for food hidden by rats (Rattus norvegicus) on the radial maze: Studies of memory for where, what, and when. Journal of Comparative Psychology 117(2): 176-187.

Clayton, N., Yu, K. & Dickinson, A. (2001) Scrub jays (Aphelocoma coerulescens) form integrated memories of the multiple features of caching episodes. Journal of experimental psychology. Animal behavior processes 27(1): 17.

Clayton, N., Yu, K. & Dickinson, A. (2003) Interacting Cache memories: evidence for flexible memory use by Western Scrub-Jays (Aphelocoma californica). Journal of experimental psychology. Animal behavior processes 29(1): 14.

Clayton, N.S. & Dickinson, A. (1998) Episodic-like memory during cache recovery by scrub jays. Nature 395(6699): 272-274.

Eacott, M.J. & Easton, A. (2010) Episodic memory in animals: Remembering which occasion. Neuropsychologia 48(8): 2273-2280.

Eacott, M.J., Easton, A. & Zinkivskay, A. (2005) Recollection in an episodic-like memory task in the rat. Learning & Memory 12(3): 221.

Eacott, M.J. & Norman, G. (2004) Integrated memory for object, place, and context in rats: a possible model of episodic-like memory? The Journal of neuroscience 24(8): 1948.

Ferkin, M.H., Combs, A., Delbarco-Trillo, J., Pierce, A.A. & Franklin, S. (2008) Meadow voles, Microtus pennsylvanicus, have the capacity to recall the “what”,“where”, and “when” of a single past event. Animal Cognition 11(1): 147-159.

Hampton, R.R., Hampstead, B.M. & Murray, E.A. (2005) Rhesus monkeys (Macaca mulatta) demonstrate robust memory for what and where, but not when, in an open-field test of memory. Learning and Motivation 36(2): 245-259.

Martin-Ordas, G., Haun, D., Colmenares, F. & Call, J. (2010) Keeping track of time: evidence for episodic-like memory in great apes. Animal Cognition 13(2): 331-340.

Raby, C. & Clayton, N. (2009) Prospective cognition in animals. Behavioural Processes 80(3): 314-324.

Zinkivskay, A., Nazir, F. & Smulders, T.V. (2009) What–where–when memory in magpies (Pica pica). Animal Cognition 12(1): 119-125.

Rhesus monkey: Flickr/Christina Hoheisel. Rat: Flickr/Kathy Keatley Garvey, UC Davis Department of Entomology.

Felicity Muth is a PhD student, researching animal behaviour and cognition. She believes strongly that the scientific community should be more communicative about their work, as there is a lot of misinformation and misunderstanding about science and scientists. Also, science is just damn interesting.

She writes a regular blog called Not Bad Science about the most exciting new findings in animal behaviour and cognition. You can also keep up with her on twitter.