Monkeys Monitor Human Goals in a Nonmatch-to-Goal Interactive Task Rossella Falcone, Emiliano Brunamonti, Stefano Ferraina, Aldo Genovesio* Department of Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy Abstract We designed a new task, called nonmatch-to-goal, to study the ability of macaque monkeys to interact with humans in a rule-guided paradigm. In this task the monkeys were required to choose one of two targets, from a list of three. For each choice, they were required to switch from their choice on the previous trial to a different one. In a subset of trials the monkeys observed a human partner performing the task. When the human concluded his turn, the monkeys were required to switch to a new goal discarding the human’s previous goal. We found that monkeys were very skillful in monitoring goals, not only of their own choice by also those of their human partner. They showed also a surprising ability to coordinate their actions, taking turns with the human partner, starting and stopping their own turn following the decision of the human partner in the task. Citation: Falcone R, Brunamonti E, Ferraina S, Genovesio A (2012) Monkeys Monitor Human Goals in a Nonmatch-to-Goal Interactive Task. PLoS ONE 7(2): e32209. doi:10.1371/journal.pone.0032209 Editor: Gonzalo G. de Polavieja, Cajal Institute, Consejo Superior de Investigaciones Cient´ıficas, Spain Received October 24, 2011; Accepted January 25, 2012; Published February 23, 2012 Copyright: 2012 Falcone 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. Funding: This work was supported by the ‘Sapienza’ University of Rome, Ricerca dell’Ateneo Federato di Scienze delle Politiche Pubbliche e Sanitarie (Protocol number: P288/09). 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: aldo.genovesio@uniroma1.it Introduction Very few studies have examined the ability of monkeys to interact with conspecifics or humans in a controlled situation. One influential line of research has shown that while observing human actions, monkeys display a shared neural representation of the action performed [1–3]. However, it is still debated whether these representations demonstrate that monkeys can fully understand human or conspecific actions [4]. Others studies have examined the ability of monkeys to interact by coordinating [5,6] or cooperating [7] with each other, and their sensitivity to the reward received by other monkeys [8]. In chimpanzees, Hiraka and Fuwa [9] showed not only cooperative behavior, but also the ability to select the most efficient partner. Very little work has been done to investigate the ability of monkeys to monitor others’ goals in a controlled experimental set up [6]. We wanted to test whether monkeys were able to use the active monitoring of human goals to make their own future choices. In a test of observational learning, Meunier et al. [10] showed that monkeys succeeded in learning by observing a monkey model solving discrimination learning problems, but failed with a human model. Therefore, it remains controversial whether monkeys can have the kinds of interaction with humans that they have with conspecifics. We wanted to test whether monkeys interact successfully with humans in a more controlled experimental setting. We measured the ability of monkeys to guide their choices based on a human’s previous choices. In line with our previous studies [11–14], we designed a nonmatch-to-goal task (NMTG) that required monkeys to switch either from their immediate previous goal or from the human partner’ s goal to a new goal, in order to receive a reward. We found that macaques were able to alternate roles with a human partner. They stopped their turns when the human intervened and promptly restarted when the human partner moved the arm away from the testing apparatus. The monkeys did not need any cue signal to instruct them that it was their turn. Instead, the monkeys monitored and adapted to the intervention of the human partner, stopping and restarting their turn accordingly. The monkeys showed high levels of performance in switching to a new goal after the human partner’s choice, which was comparable to that observed for switching their own goals. This study extends to human–monkey (H–M) pairs the opportu- nity to investigate social cognition in a controlled laboratory setup, opening a door to future behavioral, neuropsychological, and neurophysiological studies adopting similar paradigms. Materials and Methods Animals Animal care, housing, and experimental procedures were in conformity with the European (Directive 86/609/ECC) and Italian (D.L. 116/92) laws on the use of nonhuman primates in scientific research. The research protocol was approved by the Italian Health Ministry (Central Direction for the Veterinary Service, approval n. 199/2009-B). The housing conditions and the experimental procedures were in accordance with the European law on humane care and use of laboratory animals and complied with the recommendations of the Weatherall report (The use of non-human primates in research). Both monkeys were monitored daily by the researchers and the animal care staff, and every second day from the veterinarian, to check the conditions of health and welfare. PLoS ONE | www.plosone.org 1 February 2012 | Volume 7 | Issue 2 | e32209