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From muscles synergies and individual goals to interpersonal synergies and shared goals: Mirror neurons and interpersonal action hierarchies Comment on “Grasping synergies: A motor-control approach to the mirror neuron mechanism” by D’Ausilio et al. Matteo Candidi a,b,∗ , Lucia Maria Sacheli c , Salvatore Maria Aglioti a,b a Department of Psychology, Sapienza University of Rome, Italy b IRCCS Fondazione Santa Lucia, Rome, Italy c University of Milano-Bicocca, Italy
Received 29 December 2014; accepted 19 January 2015
Communicated by L. Perlovsky
D’Ausilio et al. [28] must be praised for bringing attention to the important question of how human Mirror Neurons (MNs) may contribute to action perception, prediction and understanding [1] and for linking their role with the granularity of the motor system as conceptualized in the domain of action control theories. Although we think that the Authors are right in saying that the granularity of the motor system constrains the granularity of the MN system, we speculate that the contribution of MNs to action perception, prediction and understanding is also constrained by the connections between MNs and other cortical and subcortical regions, and by the identity of MNs, i.e. whether they are interneurons or pyramidal cells [2]. In other words, the functional contribution of MS depends on whether they are connected to sensory, emotional and cognitive networks for the service of action perception, prediction and understanding. This said, we would like to develop an argument that may help to put the main ideas of this target article in a broader framework. We appreciate the relevance given by D’Ausilio et al. [28] to the link between MNs, synergies, actions’ goals and ecological behavior as we believe that MNs’ activity is inherently linked to motor goals, and that action goals are central for human behavior and mental life [3,4], especially when they are shared among individuals. Thus, on the one hand we acknowledge that MNs’ role in action prediction and understanding cannot be fully understood without taking into account the essential rules of motor control. On the other hand, we reckon that the same question needs to consider the sociality of actions, i.e. the sharing of common goals between co-agents [5–7], which is the natural condition where MNs might have developed. Since our motor goals are mostly interactive (social), it is crucial to study MNs’ activity during realistic, often non-imitative, interactions where an interpersonal goal must be (rapidly and flexibly) shared among individuals. This implies to ask the question of what happens to MNs’ activity when we DOI of original article: http://dx.doi.org/10.1016/j.plrev.2014.11.002. * Corresponding author at: Dipartimento di Psicologia, Università Sapienza, via dei Marsi 78, 00185, Rome, Italy.
E-mail address:
[email protected] (M. Candidi). http://dx.doi.org/10.1016/j.plrev.2015.01.023 1571-0645/© 2015 Elsevier B.V. All rights reserved.
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are actively engaged in the execution of an action while observing the very same (or a different) action performed by another individual. In this vein we propose that the activity of MNs is not only reflecting the representation of muscular synergies but it also implements the representation of interpersonal synergies at the service of shared goal coding. This can be done by including in the theoretical framework proposed by the authors the notion of “motor hierarchies” [8]. Indeed, in motor control theories, synergies are embedded in hierarchical action representations [9] where individual motor synergies are selected according to the desired end states. A hierarchical organization of actions (from goals to movements and muscular synergies) might be found during action observation too [3,8,10–12]. Thus, we suggest that MNs’ activity is not independent from this hierarchy and particularly from the desired state of an observer in relation to the observed movement. In keeping with a causal influence of higher level representation on individual action simulation, studies indicate that the social context in which actions take place shapes their motor representations, that different contexts may modify the actor’s intentions as inferred by the onlooker and that this effect has an impact on simulative processes [13,14]. Such notion becomes particularly important when motor interactions are taken into account. For example, representing individual sub-goals in the overarching representation of a common goal does change the activity of the simulative machinery the brain is equipped with. In other words, we posit that the role of MN (and their action representation level) changes depending on how much we represent the action of the others in relation to ours. Similarly, MNs functioning is not independent from the social context, as simulative mechanisms are modulated by the interpersonal links between observer and agent [15–18]. Studies of cortico-spinal modulations of individuals confronted with potential interaction alternatives indicate that we automatically and inevitably simulate what we see in others [19] and then simulate the complementary movement as soon as contextual cues specify what we should do [20,21]. In contrast, some scholars have argued that MNs’ reactivity may follow associative learning and may become associated to any kind of action (even incongruent ones) [22,23]. We think these forms of simulation, and MNs reactivity to others’ actions, are shaped by the extent to which we share goals with them. In other words, as much as the goal of an individual action constrains the synergies of the muscles used to achieve it, the representation of a shared goal determines if and how we will simulate the others’ behavior, and the consequent role of MNs activity in the perception, prediction and understanding of their actions. A slightly different approach to explore the level at which we simulate the action of others is to directly look at the effect of their actions on the kinematics of our own movements (visuo-motor interference effects, [24]) particularly when we are actively engaged in interactions. Action kinematics are crucial in the simulation of observed movements as they are what the observer sees. Within this framework, we have recently shown that sharing goals with others, while performing joint actions where partners have different roles, influences the degree to which simulation of the partner’s actions is reflected in the agent’s action kinematics [25]. We have also demonstrated that these effects are modulated by the interpersonal perception between interactive agents [26,27]. Thus we suggest that shared goals might carve individual kinematics and observed action simulation for the sake of coordination just as much as synergies do affect single muscles contractions. In other words, the “granularity” (i.e., the hierarchical structure) of our goal representation in conjunction with the behavior of a co-agent shapes the simulation of his movements. This process is possibly underpinned by MNs’ activity. In conclusion, we believe that the perspective proposed by D’Ausilio [28] and colleagues will help the field to move towards a better explanation of the motor mechanisms supporting the understanding of others’ action and interaction in the social world. However, the idea of granularity in the MNs needs to be included in the broader notion of hierarchical social motor representations. We submit that overarching, social goals modulate individual behaviors following similar organizational principles that allow one to cluster single muscles contractions in movement synergies. Thus, interpersonal synergies bind together individuals in their social encounters. References [1] Urgesi C, Candidi M, Avenanti A. Neuroanatomical substrates of action perception and understanding: an anatomic likelihood estimation meta-analysis of lesion–symptom mapping studies in brain injured patients. Front Human Neurosci 2014;8:344. [2] Kraskov A, Dancause N, Quallo MM, Shepherd S, Lemon RN. Corticospinal neurons in macaque ventral premotor cortex with mirror properties: a potential mechanism for action suppression? Neuron 2009;64:922–30. [3] Csibra G. Action mirroring and action understanding: an alternative account. In: Haggard P, Rossetti Y, Kawato M, editors. Sensorimotor foundations of higher cognition. Oxford: Oxford University Press; 2007. p. 435–59.
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[4] Huang JY, Bargh JA. The Selfish Goal: autonomously operating motivational structures as the proximate cause of human judgment and behavior. Behav Brain Sci 2014;37:121–35. [5] Sebanz N, Bekkering H, Knoblich G. Joint action: bodies and minds moving together. Trends Cogn Sci 2006;10:70–6. [6] Gallotti M, Frith CD. Social cognition in the we-mode. Trends Cogn Sci 2013;17:160–5. [7] Schilbach L, Timmermans B, Reddy V, Costall A, Bente G, Schlicht T, et al. Toward a second-person neuroscience. Behav Brain Sci 2013;36:393–414. [8] Grafton ST, Hamilton AF. Evidence for a distributed hierarchy of action representation in the brain. Hum Mov Sci 2007;26:590–616. [9] Wolpert DM, Ghahramani Z. Computational principles of movement neuroscience. Nat Neurosci 2000;3:1212–7. [10] Chersi F. Neural mechanisms and models underlying joint action. Exp Brain Res 2011;211:643–53. [11] Fogassi L, Luppino G. Motor functions of the parietal lobe. Curr Opin Neurobiol 2005;15:626–31. [12] Friston K, Kilner J, Harrison L. A free energy principle for the brain. J Physiol Paris 2006;100:70–87. [13] Ondobaka S, de Lange FP, Wittmann M, Frith CD, Bekkering H. Interplay between conceptual expectations and movement predictions underlies action understanding. Cereb Cortex 2014 [Epub ahead of print]. [14] Ondobaka S, Bekkering H. Conceptual and perceptuo-motor action control and action recognition. Cortex 2013;49:2966–7. [15] Molnar-Szakacs I, Wu AD, Robles FJ, Iacoboni M. Do you see what I mean? Corticospinal excitability during observation of culture-specific gestures. PLoS ONE 2007;2:e626. [16] Désy MC, Théoret H. Modulation of motor cortex excitability by physical similarity with an observed hand action. PLoS ONE 2007;2:e971. [17] Avenanti A, Sirigu A, Aglioti SM. Racial bias reduces empathic sensorimotor resonance with other-race pain. Curr Biol 2010;20:1018–22. [18] Gutsell JN, Inzlicht M. Empathy constrained: prejudice predicts reduced mental simulation of actions during observation of outgroups. J Exp Soc Psychol 2010;46:841–5. [19] Cattaneo L, Rizzolatti G. The mirror neuron system. Arch Neurol 2009;66:557–60. [20] Ubaldi S, Barchiesi G, Cattaneo L. Bottom-up and top-down visuomotor responses to action observation. Cereb Cortex 2013 [Epub ahead of print]. [21] Sartori L, Bucchioni G, Castiello U. When emulation becomes reciprocity. Soc Cogn Affect Neurosci 2013;8:662–9. [22] Catmur C, Walsh V, Heyes C. Sensorimotor learning configures the human mirror system. Curr Biol 2007;17(17):1527–31. [23] Cook R, Bird G, Catmur C, Press C, Heyes C. Mirror neurons: from origin to function. Behav Brain Sci 2014;37:177–92. [24] Kilner JM, Paulignan Y, Blakemore SJ. An interference effect of observed biological movement on action. Curr Biol 2003;13:522–5. [25] Sacheli LM, Tidoni E, Pavone EF, Aglioti SM, Candidi M. Kinematics fingerprints of leader and follower role-taking during cooperative joint actions. Exp Brain Res 2013;226:473–86. [26] Sacheli LM, Candidi M, Pavone EF, Tidoni E, Aglioti SM. And yet they act together: interpersonal perception modulates visuo-motor interference and mutual adjustments during a joint-grasping task. PLoS ONE 2012;7:e50223. [27] Sacheli LM, Christensen A, Giese M, Taubert N, Pavone EF, Aglioti SM, et al. Prejudiced interactions: implicit racial bias reduces predictive simulation during joint action with an out-group avatar. Sci Rep 2015. http://dx.doi.org/10.1038/srep08507 [in press]. [28] D’Ausilio A, Bartoli E, Maffongelli L. Grasping synergies: a motor-control approach to the mirror neuron mechanism. Phys Life Rev 2015. http://dx.doi.org/10.1016/j.plrev.2014.11.002 [in this issue].
