- Email: [email protected]
From One to Many: Representing Not Only Actions, but Interactions in the Brain
TICS 1859 No. of Pages 2
Spotlight
From One to Many: Representing Not Only Actions, but Interactions in the Brain Leonhard Schilbach1,* Observing others is a pervasive way of learning about the social world, but little is known about the neural correlates of observing more than one individual. A recent neuroimaging study demonstrates that activity in the human motor system tracks multiple actions and that anterior cingulate cortex is involved to monitor motor conflict. Social encounters shape our lives in a multitude of ways and are crucial for physical and mental health. The field of social neuroscience investigates the neurobiology that underlies social perception and communication, but has so far largely focused on how an individual brain processes the actions observed in another individual. This line of research has produced evidence that observing an action activates the same motor areas of the brain that are engaged when generating the action oneself. This, in turn, has given rise to the idea of a ‘mirror neuron’ system in the human brain (cf. [1]). The finding that there is a commonality in the response profiles of motor regions during observation and execution has been interpreted by some as evidence that observation-related motor activation has a causal role in subserving an individual's ‘understanding’ of another individual’s actions, while others have argued that motor activation is the consequence of action perception or that it contributes to action perception in a domain-general fashion (cf. [2]).
generate a more complete characterization of the contribution and functional role of the motor system (and other brain networks) for everyday life social encounters, it is necessary to take steps toward a truly social (or ‘second-person’) neuroscience that focuses on the neurobiology of social interactions rather than on the observation of individual actions [3]. Social interactions that can be observed in real life (e. g., when we observe a group of people who are having dinner together in a restaurant) typically involve multiple interaction partners whose actions are reciprocally related to one another in space and time. In the context of action observation, this raises different questions: does it matter for the brain whether an observed action is directed towards myself or another person? Is it possible to represent the actions of two or multiple persons when observing a social interaction or does the mirror mechanism break down when there is no one-to-one mapping between observer and the observed? Does it matter whether these are the same or different, such as complementary actions, which often occur in real-life situations? Which other bodily signals, such as facial expressions and gaze cues, are relevant and how does the context provided by a social situation influence how multiple actions are represented in the brain [4,5]?
Several of these important new questions have been addressed in a recent functional neuroimaging study by Cracco and colleagues [6], who used videos of not only one, but two hands, both, just one, or neither of which performed gestures. When two hands were performing gestures, these gestures could either be identical or different, but were not related to one another. While not explicitly stated in the paper, the video images suggest that the videos of the two hands shown While the interpretation of these specific were the right hand of the same person findings is still a matter of controversy, to shown twice. Results demonstrated that
observing two right hands performing different gestures activated the motor system of the brain more strongly than observing two hands perform the same gesture. Furthermore, using multivariate analysis techniques, the gestures could be related to brain activity in visual and parietal cortex. This was true regardless of whether the two gestures were the same or different. However, observing two different actions compared with two identical actions led to differential effects in the anterior cingulate cortex (ACC), a region that has repeatedly been shown to be involved in error monitoring. The latter could be taken to suggest that, in general, the brain is sensitive to conflicts in information processing. In the context of action observation, this might mean that deviations from (even minimal) social group norms are detected to ensure social alignment [7]. Furthermore, ACC has been shown to have a crucial role in understanding others’ motivation for social exchange, which is important to assess possible costs and benefits of social interactions, thereby also shaping social behavior [8]. These findings by Cracco et al. are important because they demonstrate that previously reported effects in the motor system extend to the perception of multiple actions. In addition, they show that the perception of several actions engages additional brain regions relevant for error monitoring and motor conflict to account for the fact that multiple observed actions may not be executed simultaneously. Here, an interesting avenue for future research may involve investigating the conditions in which other brain regions (such as the so-called ‘mentalizing network’, which has been related to processing the intentions that may motivate an action) are engaged automatically during action observation and may interact with the motor system when observing multiple actions [9].
Trends in Cognitive Sciences, Month Year, Vol. xx, No. yy
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TICS 1859 No. of Pages 2
Importantly, future studies should build on brain regions beyond the motor system the findings of Cracco and colleagues by will also need to be considered. enriching the relatively simple paradigm 1 Max Planck Institute of Psychiatry, Kraepelinstr. 2–10, used in this study to include additional 80804 Munich, Germany cues that usually characterize naturalistic social interactions. Here, not only well- *Correspondence: [email protected] (L. Schilbach). controlled full-body stimuli could be useful https://doi.org/10.1016/j.tics.2018.10.007 (cf. [10]), but also approaches that measure and quantify freely forming social References interactions and allow for systematic 1. Rizzolatti, G. and Sinigaglia, C. (2010) The functional role of the parieto-frontal mirror circuit: interpretations and mismanipulation of the timing and reciprocity interpretations. Nat. Rev. Neurosci. 11, 264–274 of multiple actions. These future studies 2. Catmur, C. et al. (2017) Sensorimotor training alters action understanding. Cognition 171, 10–14 will help to elucidate whether the results 3. Schilbach, L. et al. (2013) Toward a second-person neuobserved in this study can, indeed, be roscience. Behav. Brain Sci. 36, 393–414 interpreted as evidence for ‘interaction 4. Pierno, A.C. et al. (2006) When gaze turns into grasp. J. Cogn. Neurosci. 18, 2130–2137 representation’ or whether additional
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Trends in Cognitive Sciences, Month Year, Vol. xx, No. yy
5. Schilbach, L. et al. (2011) Eyes on me: an fMRI study of the effects of social gaze on action control. Soc. Cogn. Affect Neurosci. 6, 393–403 6. Cracco, E. et al. (2018) Representing multiple observed actions in the motor system. Cereb. Cortex Published online October 6, 2018. http://dx.doi.org/10.1093/cercor/bhy237 7. Fairhurst, M.T. et al. (2013) Being and feeling in sync with an adaptive virtual partner: brain mechanisms underlying dynamic cooperativity. Cereb. Cortex 23, 2592–2600 8. Apps, M.J. et al. (2016) The anterior cingulate gyrus and social cognition: tracking the motivation of others. Neuron 90, 692–707 9. Ciaramidaro, A. et al. (2014) Do you mean me? Communicative intentions recruit the mirror and the mentalizing system. Soc. Cogn. Affect Neurosci. 9, 909–916 10. von der Lühe, T. et al. (2016) Interpersonal predictive coding, not action perception, is impaired in autism. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371, 20150373
Spotlight
From One to Many: Representing Not Only Actions, but Interactions in the Brain Leonhard Schilbach1,* Observing others is a pervasive way of learning about the social world, but little is known about the neural correlates of observing more than one individual. A recent neuroimaging study demonstrates that activity in the human motor system tracks multiple actions and that anterior cingulate cortex is involved to monitor motor conflict. Social encounters shape our lives in a multitude of ways and are crucial for physical and mental health. The field of social neuroscience investigates the neurobiology that underlies social perception and communication, but has so far largely focused on how an individual brain processes the actions observed in another individual. This line of research has produced evidence that observing an action activates the same motor areas of the brain that are engaged when generating the action oneself. This, in turn, has given rise to the idea of a ‘mirror neuron’ system in the human brain (cf. [1]). The finding that there is a commonality in the response profiles of motor regions during observation and execution has been interpreted by some as evidence that observation-related motor activation has a causal role in subserving an individual's ‘understanding’ of another individual’s actions, while others have argued that motor activation is the consequence of action perception or that it contributes to action perception in a domain-general fashion (cf. [2]).
generate a more complete characterization of the contribution and functional role of the motor system (and other brain networks) for everyday life social encounters, it is necessary to take steps toward a truly social (or ‘second-person’) neuroscience that focuses on the neurobiology of social interactions rather than on the observation of individual actions [3]. Social interactions that can be observed in real life (e. g., when we observe a group of people who are having dinner together in a restaurant) typically involve multiple interaction partners whose actions are reciprocally related to one another in space and time. In the context of action observation, this raises different questions: does it matter for the brain whether an observed action is directed towards myself or another person? Is it possible to represent the actions of two or multiple persons when observing a social interaction or does the mirror mechanism break down when there is no one-to-one mapping between observer and the observed? Does it matter whether these are the same or different, such as complementary actions, which often occur in real-life situations? Which other bodily signals, such as facial expressions and gaze cues, are relevant and how does the context provided by a social situation influence how multiple actions are represented in the brain [4,5]?
Several of these important new questions have been addressed in a recent functional neuroimaging study by Cracco and colleagues [6], who used videos of not only one, but two hands, both, just one, or neither of which performed gestures. When two hands were performing gestures, these gestures could either be identical or different, but were not related to one another. While not explicitly stated in the paper, the video images suggest that the videos of the two hands shown While the interpretation of these specific were the right hand of the same person findings is still a matter of controversy, to shown twice. Results demonstrated that
observing two right hands performing different gestures activated the motor system of the brain more strongly than observing two hands perform the same gesture. Furthermore, using multivariate analysis techniques, the gestures could be related to brain activity in visual and parietal cortex. This was true regardless of whether the two gestures were the same or different. However, observing two different actions compared with two identical actions led to differential effects in the anterior cingulate cortex (ACC), a region that has repeatedly been shown to be involved in error monitoring. The latter could be taken to suggest that, in general, the brain is sensitive to conflicts in information processing. In the context of action observation, this might mean that deviations from (even minimal) social group norms are detected to ensure social alignment [7]. Furthermore, ACC has been shown to have a crucial role in understanding others’ motivation for social exchange, which is important to assess possible costs and benefits of social interactions, thereby also shaping social behavior [8]. These findings by Cracco et al. are important because they demonstrate that previously reported effects in the motor system extend to the perception of multiple actions. In addition, they show that the perception of several actions engages additional brain regions relevant for error monitoring and motor conflict to account for the fact that multiple observed actions may not be executed simultaneously. Here, an interesting avenue for future research may involve investigating the conditions in which other brain regions (such as the so-called ‘mentalizing network’, which has been related to processing the intentions that may motivate an action) are engaged automatically during action observation and may interact with the motor system when observing multiple actions [9].
Trends in Cognitive Sciences, Month Year, Vol. xx, No. yy
1
TICS 1859 No. of Pages 2
Importantly, future studies should build on brain regions beyond the motor system the findings of Cracco and colleagues by will also need to be considered. enriching the relatively simple paradigm 1 Max Planck Institute of Psychiatry, Kraepelinstr. 2–10, used in this study to include additional 80804 Munich, Germany cues that usually characterize naturalistic social interactions. Here, not only well- *Correspondence: [email protected] (L. Schilbach). controlled full-body stimuli could be useful https://doi.org/10.1016/j.tics.2018.10.007 (cf. [10]), but also approaches that measure and quantify freely forming social References interactions and allow for systematic 1. Rizzolatti, G. and Sinigaglia, C. (2010) The functional role of the parieto-frontal mirror circuit: interpretations and mismanipulation of the timing and reciprocity interpretations. Nat. Rev. Neurosci. 11, 264–274 of multiple actions. These future studies 2. Catmur, C. et al. (2017) Sensorimotor training alters action understanding. Cognition 171, 10–14 will help to elucidate whether the results 3. Schilbach, L. et al. (2013) Toward a second-person neuobserved in this study can, indeed, be roscience. Behav. Brain Sci. 36, 393–414 interpreted as evidence for ‘interaction 4. Pierno, A.C. et al. (2006) When gaze turns into grasp. J. Cogn. Neurosci. 18, 2130–2137 representation’ or whether additional
2
Trends in Cognitive Sciences, Month Year, Vol. xx, No. yy
5. Schilbach, L. et al. (2011) Eyes on me: an fMRI study of the effects of social gaze on action control. Soc. Cogn. Affect Neurosci. 6, 393–403 6. Cracco, E. et al. (2018) Representing multiple observed actions in the motor system. Cereb. Cortex Published online October 6, 2018. http://dx.doi.org/10.1093/cercor/bhy237 7. Fairhurst, M.T. et al. (2013) Being and feeling in sync with an adaptive virtual partner: brain mechanisms underlying dynamic cooperativity. Cereb. Cortex 23, 2592–2600 8. Apps, M.J. et al. (2016) The anterior cingulate gyrus and social cognition: tracking the motivation of others. Neuron 90, 692–707 9. Ciaramidaro, A. et al. (2014) Do you mean me? Communicative intentions recruit the mirror and the mentalizing system. Soc. Cogn. Affect Neurosci. 9, 909–916 10. von der Lühe, T. et al. (2016) Interpersonal predictive coding, not action perception, is impaired in autism. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371, 20150373