Symbolic Manipulation in Monkeys

ResearchBlogging.orgOne of the most interesting aspects of human behavior is our nearly infinite capacity to arrange and coordinate symbols. Think of the symbols that permeate our existence. Paper money has no value in and of itself. A wedding ring is just a band of metal. The progress of the science might even be seen as the creation of an incredibly elaborate super-abstraction from which we can derive novel and testable predictions. Humans beings, in short, are into symbols.

We know, however, that we are not the only animals capable of symbolic thinking. For example, I could argue that whenever I teach a rat that a treat can be found under a particular toy, the toy comes to symbolize the treat for that rat. There have been neuronal recordings done for a similar experiment that show the formation of a stimulus-reward pairing in rat brains. (These recordings were done in the orbitofrontal cortex for odor-reward pairings. See Schoenbaum et al.) However, this sort of stimulus response learning is not really symbolic in the sense that we understand the term.

The real hallmark of symbolic reasoning is the ability to compare and manipulate symbols. On this ground, we have evidence that chimpanzees are capable of symbolic logic. Chimpanzees can be trained to use linguistic symbols to ask for certain items, and two similarly trained chimps can conduct simple conversations with one another on the basis of these symbols.

Moving down the evolutionary ladder, though, experiments with symbols in non-apes are not as common. We know that capuchin monkeys are capable of forming economic associations with tokens as symbols for possible rewards. But are they capable of manipulating such symbols? Addessi et al. publishing in PLoS One show that they are.

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Image by atbaker on Flickr

Addessi et al. wanted to know whether symbolic thinking in capuchin monkeys showed transitivity. Transitivity is the property that the indirect associations between the values of symbols follow what you would infer from the direct associations between the values of symbols. For example, if the value of symbol A is greater than symbol B and the value symbol B is greater than symbol C, than we would expect the value of symbol A to be greater than symbol C -- even if those values have never been directly compared.

You do this experiment by training capuchin monkeys to associate food rewards with particular tokens A, B, and C. Then you establish the various values that the animals have for each of the food reward by comparing how much of A you would need to equal how much of B. In a forced choice, how much of A relative to B is required for the monkey to pick each with equal frequency? (The authors call this the Food condition.)

After you establish the value of the food and associate each with a token, you subject the monkeys to a number of forced choice experiments where they have to choose between different numbers of tokens A, B, and C. (The authors call this the Token condition.) This experiment allows you to establish whether because the food reward associated with A is bigger than that associated with C, the animals will pick A over C. Furthermore -- and this is important -- it allows you to determine whether the relative value of the food equals exactly the relative value of the tokens. How would you figure that out? Well, say that food A is worth four times as much as food B; you have to offer the monkey four times as much B as A to get them to pick each with equal frequency. Well, then you ask: how many tokens of B must be offer to equal how many tokens of A? Is it the same ratio of 4:1?

The authors found when they performed the experiment that the animals consistently picked the more valuable tokens: their responses showed transitivity. However, when tokens were substituted for actual food, the animal's preferences for more valuable tokens were magnified to be greater than their preference for the actual food. What would that look like? Take my example above. Say you discover that the animal prefers food A to food B at a ratio of 4:1. Then when you do the experiments with the tokens, you note that the animal always picks A -- that no quantity of B tokens is sufficient for them to not pick A tokens. This is would suggest a magnification of the preference for A.

Here is what the authors have to say about their results:

Our results can be summarized as follows. Qualitatively, preferences revealed by the way of tokens were similar to those measured with the actual foods. Specifically, when choosing between tokens, capuchins displayed strict economic preferences and choices satisfied transitivity since the first session for all subjects but one. These results confirm and extend previous findings obtained in non-human primates faced with choices between real foods or juices and with relative numerousness judgments between food or tokens. Quantitatively, however, values measured by the way of tokens differed systematically from those measured with the actual foods. In particular, for any pair of foods, the relative value of the preferred food tended to increase when monkeys chose between the corresponding tokens. (Italics in original. Emphasis mine. Citations removed.)

The authors speculate that the reason for the disconnect between the evaluation of food and the evaluation of the tokens might have to do with trouble comparing a "dual representation." In this sense, the monkeys are making evaluations in a manner very similar to human children:

Finally, the different results obtained in the Token condition compared to the Food condition could reflect a difficulty to achieve a dual representation. Specifically, capuchins may find it difficult to grasp the dual nature of tokens as it is the case for young children. In humans, the understanding and use of symbolic artifacts develops slowly because simultaneously representing both the concrete object itself and its abstract relation to what it stands for is complex. DeLoache and colleagues have extensively investigated how young children use scale models (i.e., realistic miniature models of a familiar playroom) as a source of information for solving a retrieval problem. In a typical trial, children observed an experimenter hide a miniature toy in the model and were then asked to find the larger toy in the analogous location of the playroom. Children understanding of the model-playroom relation and the ability to successfully find the corresponding larger toy in the playroom developed between 2.5 and 3.0 years of age. In chimpanzees tested in a similar version of this task, only a few individuals could inhibit perseverative object-oriented responses and successfully retrieved the hidden item.

Young children seem to fail in the scale model task because they are attentive to the real object rather than to what it stands for. When the salience of the model is decreased (for example substituting the scale model with a video clip), or when there is no need for dual representation (children are told that a "shrinking machine" transformed the playroom into the miniature model), performance improves. In contrast, performance declines when the physical salience of the scale model is increased by allowing children to play with the model before performing the task. A similar phenomenon might explain our results. In the Token condition capuchins might have focused on the quality of the preferred token disregarding the quantities of the two alternatives, thus choosing this token more often than the corresponding food in the Food condition. Future studies should assess whether preventing the physical interaction with tokens by eliminating the exchange procedure modifies capuchins' performance. (Emphasis mine. Citations removed.)

The comparison between the behavior of capuchins and children is fascinating because it explains the evolutionary leap that has allowed for humans to engage in more symbolic thinking. Part of that evolutionary leap appears to be the ability to disconnect the very present object/symbol from the value that it represents. If you aren't obsessing over the tokens that are actually in your hands, you can focus on comparing their true values. In many ways, this "long-term thinking" is a defining feature of human thought, and it is a feature conspicuously lacking in capuchins and often in young children.

There is a particular experiment that I would suggest to help to clarify matters. I mentioned before that we think that stimulus-reward pairings are formed in the orbitofrontal cortex -- among other places...it is a complicated subject. I would be interested in finding the neurological substrate that allows for the direct comparison of the tokens values. You could probably do this by doing neuronal recordings in the monkey's orbitofrontal cortex during the performance of this task. That would let you find out whether the representation of the food's value and the representation of the token's value are the same or different. The prediction for this experiment would be that they are different. (I have talked about this issue of transitivity in value for monkeys before in relation to monkeys willingness to trade food for sex in the wild.)

All told some very interesting work on a very interesting subject!

Hat-tip: Science Daily

Addessi, E., Mancini, A., Crescimbene, L., Padoa-Schioppa, C., Visalberghi, E., Santos, L. (2008). Preference Transitivity and Symbolic Representation in Capuchin Monkeys (Cebus apella). PLoS ONE, 3(6), e2414. DOI: 10.1371/journal.pone.0002414

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