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UMD BIOL 608W - Cognitive and Motivational Requirements for the Emergence of Cooperation in a Rat Social Game

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Cognitive and Motivational Requirements for theEmergence of Cooperation in a Rat Social GameDuarte S. Viana1, Isabel Gordo2,E´lio Sucena3,4., Marta A. P. Moita1.*1 Fundac¸a˜o Champalimaud Neuroscience Program at Instituto Gulbenkian de Cieˆncia, Oeiras, Portugal, 2 Instituto Gulbenkian de Cieˆncia, Oeiras, Portugal,3 Departamento de Biologia Animal, Faculdade de Cieˆncias da Universidade de Lisboa, Lisboa, Portugal, 4 Centro de Biologia do Desenvolvimento, Instituto Gulbenkiande Cieˆncia, Oeiras, PortugalAbstractBackground:Game theory and the Prisoner’s Dilemma (PD) game in particular, which captures the paradox of cooperativeinteractions that lead to benefits but entail costs to the interacting individuals, have constituted a powerful tool in the studyof the mechanisms of reciprocity. However, in non-human animals most tests of reciprocity in PD games have resulted insustained defection strategies. As a consequence, it has been suggested that under such stringent conditions as the PDgame humans alone have evolved the necessary cognitive abilities to engage in reciprocity, namely, numericaldiscrimination, memory and control of temporal discounting.Methodology/Principal Findings:We use an iterated PD game to test rats (Rattus norvegicus) for the presence of suchcognitive abilities by manipulating the strategy of the opponent, Tit-for-Tat and Pseudo-Random, or the relative size of thetemptation to defect. We found that rats shape their behaviour according to the opponent’s strategy and the relativeoutcome resulting from cooperative or defective moves. Finally, we show that the behaviour of rats is contingent upon theirmotivational state (hungry versus sated).Conclusions/Significance:Here we show that rats understand the payoff matrix of the PD game and the strategy of theopponent. Importantly, our findings reveal that rats possess the necessary cognitive capacities for reciprocity-basedcooperation to emerge in the context of a prisoner’s dilemma. Finally, the validation of the rat as a model to studyreciprocity-based cooperation during the PD game opens new avenues of research in experimental neuroscience.Citation: Viana DS, Gordo I, Sucena E´, Moita MAP (2010) Cognitive and Motivational Requirements for the Emergence of Cooperation in a Rat Social Game. PLoSONE 5(1): e8483. doi:10.1371/journal.pone.0008483Editor: Sarah Frances Brosnan, Georgia State University, United States of AmericaReceived July 1, 2009; Accepted November 23, 2009; Published Jan uary 13, 2010Copyright: ß 2010 Viana et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.Funding: This work was supporte d by Fundac¸a˜o Champalimaud, Instituto Gulbenkian de Cieˆncia and Fundac¸a˜o para a Cieˆncia e a Tecnologia, Portugal (POCTI/0664/2004). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Competing Interests: The authors have declared that no competing interests exist.* E-mail: [email protected] These authors contributed equally to this work.IntroductionA central feature of the human species is its seeminglyevolutionarily unprecedented capacity to establish cooperativeinteractions between non-related individuals. However, manyexamples describing similar behaviours in other animals revealedthat this capacity is not exclusive to our species [1], questioning asimple Darwinian competition scenario for the evolution ofcooperation. Over the last decades, several models have beenput forward to solve this adaptive paradox such as kin selection,mutualism and reciprocity [2–5]. Nevertheless, when tested innatural populations and in laboratory conditions, some types ofcooperation have been difficult to validate. In particular, evidencefor reciprocity has not been free from controversy despite theabundance of reported cases including vampire bats [6], treeswallows [7], sticklebacks [8], impala [9], blue jays [10], cotton-toptamarin monkeys [11], red-winged blackbirds [12] and piedflycatchers [13].Several mechanistic causes for the emergence of reciprocity-based cooperation, during the interaction between two individuals,have been put forward. One of these emphasizes pro-socialpropensity of the interacting individuals, in that a cooperative actconstitutes a truly altruistic behaviour emerging from a rewardvalue attributed to the perception of benefit to others [14].Alternatively, from a strictly economic perspective, it is proposedthat animals cooperate whenever it entails a benefit, eitherimmediate or in the future, regardless of the consequence of itsaction to the other interacting individual [15]. These twoapparently opposing views may both explain to some degree theemergence of cooperation. Indeed, cooperation in humans issensitive to both pro-social and economic factors [16,17].Game Theory has proven to be instrumental in the study ofsocial behaviour, as it formalizes mathematically the outcomesassociated with the decisions of two or more interactingindividuals, framing in economic terms the conditions forreciprocity [17,18]. In the prisoner’s dilemma (PD), the moststudied game, cooperation leads to benefits but entails costs to theinteracting individuals [19–21]. In the PD game, players can eithercooperate or defect. If both cooperate they receive a higher payoff(Reward, R) than if they both defect (Punishment, P), but if onePLoS ONE | 1 January 2010 | Volume 5 | Issue 1 | e8483defects when the other cooperates, the defector receives thehighest payoff (Temptation, T) whereas the cooperating individualreceives the lowest (Sucker, S). The resulting payoff matrix followsthe rule T.R.P.S. If the game is played only once the beststrategy is defection, however cooperation can be stable if PD isplayed repeatedly (iterated PD). Several strategies have proven tolead to stable cooperation in the iPD game, of which Tit-for-Tat,the winning strategy in the now classical Axelrod’s iPDtournament [18,19], has been extremely successful. In thisreciprocating strategy players start by cooperating and subse-quently repeat the choice of the opponent on the previous gameiteration.The success of reciprocating strategies in theoretical models ofiPD games has been corroborated experimentally by numerousreports on the emergence of

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