Primate origins of corepresentation and cooperative flexibility: A comparative study with common marmosets (Callithrix jacchus), brown capuchins (Sapajus apella), and Tonkean macaques (Macaca tonkeana).

Abstract

Human joint action is generally facilitated by the tendency to represent not only one’s own task and behavior but also the partner’s. Yet, under some conditions, such as in the joint Simon task, corepresentation can cause interference and hampers, rather than facilitates, joint performance. A competent cooperator should thus also be able to flexibly inhibit corepresentation if that is conducive to cooperation success. To investigate the evolutionary origin of corepresentation, as well as the cooperative flexibility to inhibit it when necessary, we tested brown capuchins and Tonkean macaques in the joint Simon task and compared them with the previously tested marmosets. Corepresentation was present in all 3 species, but its strength and the cooperation success varied substantially. The cooperatively breeding marmosets showed the weakest corepresentation effect and, therefore, highest cooperation success, and they were the only ones to use mutual gaze when coordination with the partner was necessary. Cooperative flexibility was therefore not correlated with brain size but with the prevalence of cooperation in nature. This conclusion was corroborated by species differences in gazing patterns and suggests that the drivers of cooperative flexibility in humans were not solely cognitive.

A convergent interaction engine: vocal communication among marmoset monkeys

“…However, intriguing differences appeared when analysing gazing behaviour: marmosets, like human children, engaged in mutual gaze prior to acting in ambiguous trials when it was unclear whose turn it was, whereas in non-ambiguous trials mutual gaze was less frequent. The independently breeding capuchin monkeys and Tonkean macaques hardly engaged in mutual gaze at all during the entire study [38]. These interactions not only highlight the cooperative use of mutual gaze in marmosets but also suggest some proclivity towards turn-taking, to which we will now turn.…”

“…In this task, two individuals can work on an apparatus to obtain food for both of them, but this is only successful if only the partner whose turn it is actually works on the apparatus. The marmosets would co-represent each other when jointly engaged in this cooperative coordination task [37], as did those selected dyads of capuchin monkeys and Tonkean macaques that were sufficiently tolerant to engage in the task at all [38,39]. However, intriguing differences appeared when analysing gazing behaviour: marmosets, like human children, engaged in mutual gaze prior to acting in ambiguous trials when it was unclear whose turn it was, whereas in non-ambiguous trials mutual gaze was less frequent.…”

Individual differences in co-representation in three monkey species (Callithrix jacchus, Sapajus apella and Macaca tonkeana) in the joint Simon task: the role of social factors and inhibitory control

“…As a part of self–other (SO) integration, this co-representation presumably facilitates joint performance because it allows for immediate predictions of the partners’ behaviors and enables individuals to prepare their actions in anticipation of their partner’s actions, and therefore refines motor coordination (Sebanz et al 2006a ; Sommerville and Decety 2006 ; Vesper et al 2010 ; Butterfill 2012 ; Ruissen and de Bruijn 2016 ). Co-representation is involved in basic dyadic motor coordination requiring complementary actions, such as the joint Simon task (in humans: Sebanz et al 2003 ; Ruys and Aarts 2010 ; in primates [platyrrhine and catarrhine monkeys]: Miss et al 2022 ; Miss and Burkart 2018 ) or joint music performance (Novembre et al 2016 ; see also vocal turn-taking in cooperative communication in callitrichids: Takahashi et al 2013 ). Co-representation is particularly useful when individuals perform identical actions simultaneously and successful coordination increases with motor alignment through self-other (SO) integration, such as in joint grasping/lifting/pulling tasks or synchronization tasks (Newman-Norlund et al 2008 ; Vesper et al 2013 , 2014 ; Meyer et al 2016 ; Schmitz et al 2017 ; in primates [chimpanzees]: Melis et al 2006 ; Constable et al 2021 ).…”

“…Intriguingly, co-representation even emerged with an invisible co-actor, if the partner believed that the complementary motor responses came from a social, intentionally acting partner instead of being automatically generated by an algorithm (Tsai et al 2008 ; Sahaï et al 2019 ). A first goal of our study was therefore to investigate whether and how social variables predict the co-representation previously reported in dyads of common marmosets ( Callithrix jacchus ), capuchin monkeys ( Sapajus apella ) and Tonkean macaques ( Macaca tonkeana ) tested with a joint Simon task (Miss et al 2022 ; Miss and Burkart 2018 ).…”

“…It has the advantage of making co-representation visible and thus allowing a non-invasive, behavior-based quantification of co-representation (e.g. in nonhuman primates, Miss et al 2022 ; Miss and Burkart 2018 ). However, it is a joint interference task and therefore integrating the co-actor’s action and task requirements makes the distinction between one’s own and the partner’s task affordances more difficult.…”