Abstract

Human cognition has usually been approached on the level of individual minds and brains, but social interaction is a challenging case. Is it best thought of as a self-contained individual cognitive process aiming at an “understanding of the other,” or should it rather be approached as an collective, inter-personal process where individual cognitive components interact on a moment-to-moment basis to form coupled dynamics? In a combined fMRI and eye-tracking study we directly contrasted these models of social cognition. We found that the perception of situations affording social contingent responsiveness (e.g., someone offering or showing you an object) elicited activations in regions of the right posterior temporal sulcus and yielded greater pupil dilation corresponding to a model of coupled dynamics (joint action). In contrast, the social-cognitive perception of someone “privately” manipulating an object elicited activation in medial prefrontal cortex, the right inferior frontal gyrus and right inferior parietal lobus, regions normally associated with Theory of Mind and with the mirror neuron system. Our findings support a distinction in social cognition between social observation and social interaction, and demonstrate that simple ostensive cues may shift participants' experience, behavior, and brain activity between these modes. The identification of a distinct, interactive mode has implications for research on social cognition, both in everyday life and in clinical conditions.

Highlights

  • Recent advances in evolutionary anthropology and experimental psychology suggest that one of the keys to the unique evolutionary trajectory of the human species can be found in our advanced capacities for reciprocal social interaction (Donald, 1991, 2001; Tomasello, 1999, 2008; Tomasello et al, 2005; Csibra and Gergely, 2009, 2011)

  • This approach departs from terms of mental inference (ToM) and MNS based frameworks, where interaction is founded on or extrapolated from individual processes of social observation, and it allows for specific predictions regarding individual brain activity during social interaction

  • The current study contrasted brain activity elicited by short videos, which evoked in the participants observational social cognition and interactive social cognition

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Summary

Introduction

Recent advances in evolutionary anthropology and experimental psychology suggest that one of the keys to the unique evolutionary trajectory of the human species can be found in our advanced capacities for reciprocal social interaction (Donald, 1991, 2001; Tomasello, 1999, 2008; Tomasello et al, 2005; Csibra and Gergely, 2009, 2011). The medial prefrontal and temporoparietal cortices consistently activate in tasks involving Theory of Mind/mentalizing (e.g., Castelli et al, 2000; Gallagher et al, 2000; German et al, 2004; Walter et al, 2004), while premotor areas and inferior parietal cortices seem to be involved in mental mirroring of others’ motor actions (e.g., Arbib et al, 2000; Rizzolatti et al, 2001; Stamenov and Gallese, 2002; Heiser et al, 2003; Kaplan and Iacoboni, 2006; Ocampo et al, 2011) While these studies make up an intriguing body of research on the neurobiological foundations of what we might term “social observation” (where no contingent response is afforded), it is disputable to which degree the findings can be generalized to account for processes underlying social interaction. We argue that the distinction between 3rd person social observation and 2nd person social interaction is an important conceptual and empirical distinction that has been somewhat neglected in the neurocognitive field (Roepstorff, 2001; Tylén and Allen, 2009; Schilbach, 2010; Hasson et al, 2012)

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