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      Preference Transitivity and Symbolic Representation in Capuchin Monkeys ( Cebus apella)

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          Abstract

          Background

          Can non-human animals comprehend and employ symbols? The most convincing empirical evidence comes from language-trained apes, but little is known about this ability in monkeys. Tokens can be regarded as symbols since they are inherently non-valuable objects that acquire an arbitrarily assigned value upon exchange with an experimenter. Recent evidence suggested that capuchin monkeys, which diverged from the human lineage 35 million years ago, can estimate, represent and combine token quantities. A fundamental and open question is whether monkeys can reason about symbols in ways similar to how they reason about real objects.

          Methodology/Principal Findings

          Here we examined this broad question in the context of economic choice behavior. Specifically, we assessed whether, in a symbolic context, capuchins' preferences satisfy transitivity - a fundamental trait of rational decision-making. Given three options A, B and C, transitivity holds true if A≥B, B≥C and A≥C (where ≥ indicates preference). In this study, we trained monkeys to exchange three types of tokens for three different foods. We then compared choices monkeys made between different types of tokens with choices monkeys made between the foods. Qualitatively, capuchins' preferences revealed by the way of tokens were similar to those measured with the actual foods. In particular, when choosing between tokens, monkeys displayed strict economic preferences and their choices satisfied transitivity. 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 increased when monkeys chose between the corresponding tokens.

          Conclusions/Significance

          These results indicate that indeed capuchins are capable of treating tokens as symbols. However, as they do so, capuchins experience the cognitive burdens imposed by symbolic representation.

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          Most cited references40

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          Neurons in the orbitofrontal cortex encode economic value.

          Economic choice is the behaviour observed when individuals select one among many available options. There is no intrinsically 'correct' answer: economic choice depends on subjective preferences. This behaviour is traditionally the object of economic analysis and is also of primary interest in psychology. However, the underlying mental processes and neuronal mechanisms are not well understood. Theories of human and animal choice have a cornerstone in the concept of 'value'. Consider, for example, a monkey offered one raisin versus one piece of apple: behavioural evidence suggests that the animal chooses by assigning values to the two options. But where and how values are represented in the brain is unclear. Here we show that, during economic choice, neurons in the orbitofrontal cortex (OFC) encode the value of offered and chosen goods. Notably, OFC neurons encode value independently of visuospatial factors and motor responses. If a monkey chooses between A and B, neurons in the OFC encode the value of the two goods independently of whether A is presented on the right and B on the left, or vice versa. This trait distinguishes the OFC from other brain areas in which value modulates activity related to sensory or motor processes. Our results have broad implications for possible psychological models, suggesting that economic choice is essentially choice between goods rather than choice between actions. In this framework, neurons in the OFC seem to be a good candidate network for value assignment underlying economic choice.
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            Monkeys reject unequal pay.

            During the evolution of cooperation it may have become critical for individuals to compare their own efforts and pay-offs with those of others. Negative reactions may occur when expectations are violated. One theory proposes that aversion to inequity can explain human cooperation within the bounds of the rational choice model, and may in fact be more inclusive than previous explanations. Although there exists substantial cultural variation in its particulars, this 'sense of fairness' is probably a human universal that has been shown to prevail in a wide variety of circumstances. However, we are not the only cooperative animals, hence inequity aversion may not be uniquely human. Many highly cooperative nonhuman species seem guided by a set of expectations about the outcome of cooperation and the division of resources. Here we demonstrate that a nonhuman primate, the brown capuchin monkey (Cebus apella), responds negatively to unequal reward distribution in exchanges with a human experimenter. Monkeys refused to participate if they witnessed a conspecific obtain a more attractive reward for equal effort, an effect amplified if the partner received such a reward without any effort at all. These reactions support an early evolutionary origin of inequity aversion.
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              Delay of gratification in children.

              To function effectively, individuals must voluntarily postpone immediate gratification and persist in goal-directed behavior for the sake of later outcomes. The present research program analyzed the nature of this type of future-oriented self-control and the psychological processes that underlie it. Enduring individual differences in self-control were found as early as the preschool years. Those 4-year-old children who delayed gratification longer in certain laboratory situations developed into more cognitively and socially competent adolescents, achieving higher scholastic performance and coping better with frustration and stress. Experiments in the same research program also identified specific cognitive and attentional processes that allow effective self-regulation early in the course of development. The experimental results, in turn, specified the particular types of preschool delay situations diagnostic for predicting aspects of cognitive and social competence later in life.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2008
                11 June 2008
                : 3
                : 6
                : e2414
                Affiliations
                [1 ]Unit of Cognitive Primatology and Primate Center, Institute of Cognitive Sciences and Technologies, Consiglio Nazionale delle Ricerche (CNR), Rome, Italy
                [2 ]University “La Sapienza”, Rome, Italy
                [3 ]Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, United States of America
                [4 ]Washington University School of Medicine, St Louis, Missouri, United States of America
                Yale University, United States of America
                Author notes

                Conceived and designed the experiments: EV EA AM LC. Performed the experiments: EA AM LC. Analyzed the data: EA AM LC CP. Wrote the paper: EV EA AM LC CP.

                Article
                08-PONE-RA-04212
                10.1371/journal.pone.0002414
                2409071
                18545670
                117ef542-d05b-4cef-8d20-285bbd768f01
                Addessi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 7 April 2008
                : 23 April 2008
                Page count
                Pages: 8
                Categories
                Research Article
                Neuroscience/Animal Cognition
                Neuroscience/Behavioral Neuroscience
                Neuroscience/Cognitive Neuroscience
                Neuroscience/Psychology
                Neuroscience/Experimental Psychology

                Uncategorized
                Uncategorized

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