Familiarity promotes the blurring of self and other in the neural representation of threat

0 Received 16 September 2011; Accepted 16 April 2012 Advance Access publication 3 May 2012 The authors acknowledge the support of Alexander Tatum , Amanda LeTard, Casey Brown, Matthew Allen, Thomas Hale-Kupiec, Caroline Trower, Priyanka Banjeree, Joe Allen, Jon Haidt , James Morris and Jeff Simpson. They also thank Joe Allen for access to the KLIFF sample. This project was supported by a grant issued by the National Institute of Mental Health. The project described was supported by Award Number R01MH080725 to J.A.C. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Mental Health or the National Institutes of Health. Gilmer Hall, Charlottesville, VA 22904 , USA 1 Department of Psychology, University of Arizona , Tucson, AZ , USA 2 Department of Psychology, University of Virginia , Charlottesville, VA , USA Neurobiological investigations of empathy often support an embodied simulation account. Using functional magnetic resonance imaging (fMRI), we monitored statistical associations between brain activations indicating self-focused threat to those indicating threats to a familiar friend or an unfamiliar stranger. Results in regions such as the anterior insula, putamen and supramarginal gyrus indicate that self-focused threat activations are robustly correlated with friend-focused threat activations but not stranger-focused threat activations. These results suggest that one of the defining features of human social bonding may be increasing levels of overlap between neural representations of self and other. This article presents a novel and important methodological approach to fMRI empathy studies, which informs how differences in brain activation can be detected in such studies and how covariate approaches can provide novel and important information regarding the brain and empathy. - INTRODUCTION Empathy may be critical for understanding others and motivating altruism (Batson and Shaw, 1991). de Vignement and Singer (2006, p. 435) define empathy as having occurred when . . . (i) one is in an affective state; (ii) this state is isomorphic to another persons affective state; (iii) this state is elicited by the observation or imagination of another persons affective state; (iv) one knows that the other person is the source of ones own affective state. Studies suggest a consistent set of neural regions similarly responsive to both self- and other-directed cues of threat and pain (Decety, 2011). These regions include the anterior insula (AI), prefrontal cortex (PFC), orbitofrontal cortex (OFC), various subcortical affective regions and the anterior cingulate cortex (ACC). Moreover, activations in these regions are frequently characterized as overlapping across self and others, or as providing evidence of self-other overlap (Decety and Sommerville, 2003; de Vignement and Singer, 2006;). Despite their consistency, these effects are moderated by other variables (cf. Hein and Singer, 2008). For example, physicians have generally weaker responses to vicarious pain (Cheng et al., 2007), and men respond less to the pain of unfair individuals (Singer et al., 2006). Furthermore, similar pain in targets produces stronger responses than dissimilar pain (Lamm et al., 2010). In this article, we compare degrees of selfother overlap in threat-responsive brain regions as a function of familiarity and add to traditional data analytic approaches to these questions an alternative strategy designed to highlight individual differences in selfother overlap and its moderation by familiarity. Simulation theory and conjunction analysis Neuroimaging studies suggest that empathy involves simulating the experience of others using neural circuits dedicated to perceiving the state of ones own body (e.g. Carr et al., 2003; Singer et al., 2004; Lamm et al., 2007, 2010; Ochsner et al., 2008; Keysers and Gazzola, 2007), a pattern broadly predicted by simulation theory (Gallese and Goldman, 1998). For example, Singer et al. (2004) discovered that neural circuits supporting affective responses to ones own pain are similarly active during anothers pain. Moreover, activation intensity in these circuits during other-directed pain varies in part as a function of self-reported empathy. Researchers typically use conjunction analysis to indentify shared neural networks. Conjunction analysis determines brain regions that are active in two or more conditions. In the typical empathy study, these would be areas that are active when researchers apply an aversive stimulus both to the participant and to someone else the latter of which putatively indicates an empathic response. Activations during empathic responding that mirror self-focused responses are interpreted as reflecting the use of ones own experience to simulate the others psychological state, a process that Singer et al. (2004) have suggested implies a breach of individual separateness. Indeed, conjunction analysis is frequently interpreted as suggesting that self-related brain activation is correlated with other-related brain activity when people engage in empathy. For example, Decety (2011, p. 104) argues that . . . similar neural networks mediate the simulation of pain for self and other. Such a perceptionaction coupling mechanism offers an interesting foundation for intersubjectivity because it provides a functional bridge between first-person information and third-person information, grounded on selfother equivalence . . .. Although these interpretations imply correlation between self and other, conjunction analysis does not.1 There may be no intra-individual correlation in a given region between the representation of self and of other even when overall average group activity in both conditions is similar. For 1There may be little or no intra-individual correlation in a given region between the representation of self and other even when overall average activity in both conditions is similar across many individuals. Conversely, there may be a high selfother correlation in a given region even when overall average activity in both conditions is quite different when averaged across individuals. This is because the general order and relative magnitude of each persons data points are independent of the overall group mean. For example, a vector composed of the numbers 2 4 3 5 1 6 is perfectly correlated with a vector composed of the numbers 12 14 13 15 11 16, but the means of each vector are dramatically different. This analytical difference may have important implications for the construct that our measures are tapping. For example, conjunction analysis likely tells us quite accurately which regions are normatively involved in empathic processing of vicariously experienced negative events, whereas correlation in this case likely reflects the tendency to treat the other person as if they were the self or just like the self, a pattern that may suggest an altogether different (...truncated)