Do non-human primates cooperate? Evidences of motor coordination during a joint action task in macaque monkeys

Visco-Comandini, Federica; Ferrari-Toniolo, Simone; Satta, Eleonora; Papazachariadis, Odysseas; Gupta, Rajnish Kumar; Nalbant, Laura E.; Battaglia-Mayer, Alexandra

doi:10.1016/j.cortex.2015.02.006

Cited by 28 publications

(35 citation statements)

References 49 publications

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“…One of the main challenges in this field is extending these studies to direct real-time interactions that would entail a broad spectrum of dynamic competitive and cooperative behaviours. In line with this, several recent studies also considered direct social interactions in humans and non-human primates [3][4][5][50][51][52][53][54][55] during dyadic games where players can monitor actions and outcomes of each other. Transparent games allow modelling the players' access to social cues, which is essential for the analysis of experimental data in the studies of this kind [21].…”

Section: Discussionmentioning

confidence: 83%

Emergence and suppression of cooperation by action visibility in transparent games

Unakafov

Schultze

Kagan

et al. 2018

Preprint

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Real-world agents, such as humans, animals and robots, observe each other during interactions and choose their own actions taking the partners' ongoing behaviour into account. Yet, classical game theory assumes that players act either strictly sequentially or strictly simultaneously (without knowing the choices of each other). To account for action visibility and provide a more realistic model of interactions under time constraints, we introduce a new game-theoretic setting called transparent game, where each player has a certain probability to observe the choice of the partner before deciding on its own action. Using evolutionary simulations, we demonstrate that even a small probability of seeing the partner's choice before one's own decision substantially changes evolutionary successful strategies. Action visibility enhances cooperation in a Bach-or-Stravinsky game, but disrupts cooperation in a more competitive iterated Prisoner's Dilemma. In both games, strategies based on the "Win-stay, lose-shift" and "Tit-for-tat" principles are predominant for moderate transparency, while for high transparency strategies of "Leader-Follower" type emerge. Our results have implications for studies of human and animal social behaviour, especially for the analysis of dyadic and group interactions.One of the most interesting questions in economics, biological, and social sciences is the emergence and maintenance of cooperation. A popular framework for studying cooperation (or the lack thereof) is Game Theory, which is frequently used to model interactions between "rational" decision-makers. In particular, a model for repeated interactions is provided by iterated games; two settings were previously used [1]:• Simultaneous games: players act at the same time without having any information about the current choice of the partners. Consequently, all players must make a decision under uncertainty concerning the choices of others.• Sequential games: players act in a certain order and the player acting later in the sequence is guaranteed to see the choices of the preceding players. Here the burden of uncertainty only applies to the first player or -if there are more than two players -becomes lighter with every turn in the sequence.Both settings place a simplifying restriction on the decisional context: either all players have no information about the choices of the partners (simultaneous game), or some players always have more information than others (sequential game). This simplification might be disadvantageous for modelling certain behaviours, since humans and animals usually act neither strictly simultaneously nor

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Section: Discussionmentioning

confidence: 83%

Emergence and suppression of cooperation by action visibility in transparent games

Unakafov

Schultze

Kagan

et al. 2018

Preprint

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“…The analysis of motor behavior of Monkeys S and K is shortly summarized here to favor comprehension of neural data. The details of this analysis have been reported in a previous behavioral study (Visco-Comandini et al, 2015), which included results from a larger dataset obtained from a total of three pairs of animals (monkey couples: S-K, C-D, B-K).…”

Section: Motor Behavior During Joint-action Vs Solo Action and Observmentioning

confidence: 99%

Two brains in action: Joint-action coding in the primate frontal cortex

2019

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Daily life often requires the coordination of our actions with those of another partner. After 50 years (1968 -2018) of behavioral neurophysiology of motor control, the neural mechanisms that allow such coordination in primates are unknown. We studied this issue by recording cell activity simultaneously from dorsal premotor cortex (PMd) of two male interacting monkeys trained to coordinate their hand forces to achieve a common goal. We found a population of "joint-action cells" that discharged preferentially when monkeys cooperated in the task. This modulation was predictive in nature, because in most cells neural activity led in time the changes of the "own" and of the "other" behavior. These neurons encoded the joint-performance more accurately than "canonical action-related cells", activated by the action per se, regardless of the individual versus interactive context. A decoding of joint-action was obtained by combining the two brains' activities, using cells with directional properties distinguished from those associated to the "solo" behaviors. Action observation-related activity studied when one monkey observed the consequences of the partner's behavior, i.e., the cursor's motion on the screen, did not sharpen the accuracy of joint-action cells' representation, suggesting that it plays no major role in encoding joint-action. When monkeys performed with a non-interactive partner, such as a computer, joint-action cells' representation of the other (non-cooperative) behavior was significantly degraded. These findings provide evidence of how premotor neurons integrate the timevarying representation of the self-action with that of a co-actor, thus offering a neural substrate for successful visuomotor coordination between individuals.The neural bases of intersubject motor coordination were studied by recording cell activity simultaneously from the frontal cortex of two interacting monkeys, trained to coordinate their hand forces to achieve a common goal. We found a new class of cells, preferentially active when the monkeys cooperated, rather than when the same action was performed individually. These "jointaction neurons" offered a neural representation of joint-behaviors by far more accurate than that provided by the "canonical action-related cells", modulated by the action per se regardless of the individual/interactive context. A neural representation of joint-performance was obtained by combining the activity recorded from the two brains. Our findings offer the first evidence concerning neural mechanisms subtending interactive visuomotor coordination between co-acting agents.

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“…The observer has the actual possibility to interfere with the grasping action and prevent it to happen, or cooperate to it. Cooperative behaviors are common in humans, but are also documented in monkeys ( Mendres and de Waal, 2000 ; Visalberghi et al, 2000 ; Visco-Comandini et al, 2015 ). If the mirror mechanism was only involved in action and intention understanding, the spatial location of the observed action and the vantage point of the observer would be irrelevant.…”

Section: The Mirror Mechanismmentioning

confidence: 99%

“…As mentioned above, the mirror mechanism in monkeys is considered to be involved in coding others’ actions in their social context ( Fujii et al, 2007 , 2008 ; Ishida et al, 2010 ; Visco-Comandini et al, 2015 ). The term “social context” encompasses a wide spectrum of settings and can refer to complex interactions, especially in human societies.…”

Section: The Mirror System In Humans An Anatomo-functional Perspectimentioning

confidence: 99%

Grasping actions and social interaction: neural bases and anatomical circuitry in the monkey

Rozzi

Coudé

2015

Front. Psychol.

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The study of the neural mechanisms underlying grasping actions showed that cognitive functions are deeply embedded in motor organization. In the first part of this review, we describe the anatomical structure of the motor cortex in the monkey and the cortical and sub-cortical connections of the different motor areas. In the second part, we review the neurophysiological literature showing that motor neurons are not only involved in movement execution, but also in the transformation of object physical features into motor programs appropriate to grasp them (through visuo-motor transformations). We also discuss evidence indicating that motor neurons can encode the goal of motor acts and the intention behind action execution. Then, we describe one of the mechanisms—the mirror mechanism—considered to be at the basis of action understanding and intention reading, and describe the anatomo-functional pathways through which information about the social context can reach the areas containing mirror neurons. Finally, we briefly show that a clear similarity exists between monkey and human in the organization of the motor and mirror systems. Based on monkey and human literature, we conclude that the mirror mechanism relies on a more extended network than previously thought, and possibly subserves basic social functions. We propose that this mechanism is also involved in preparing appropriate complementary response to observed actions, allowing two individuals to become attuned and cooperate in joint actions.

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Do non-human primates cooperate? Evidences of motor coordination during a joint action task in macaque monkeys

Cited by 28 publications

References 49 publications

Emergence and suppression of cooperation by action visibility in transparent games

Emergence and suppression of cooperation by action visibility in transparent games

Two brains in action: Joint-action coding in the primate frontal cortex

Grasping actions and social interaction: neural bases and anatomical circuitry in the monkey

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