An event-related examination of neural activity during social interactions

Jason R. Themanson 1 2 Stephanie M. Khatcherian 1 2 Aaron B. Ball 1 2 Peter J. Rosen 0 1 0 Washington State University 1 Received 22 September 2011; Accepted 2 May 2012 Advance Access publication 10 May 2012 This research was supported by a grant from the National Science Foundation (MRI 0722526) to Illinois Wesleyan University (PI: Joseph Williams) and a grant from Illinois Wesleyan University to J.R.T. University , P.O. Box 2900, Bloomington, IL 61702-2900, USA 2 Illinois Wesleyan University Social exclusion is known to cause alterations in neural activity and perceptions of social distress. However, previous research is largely limited to examining social interactions as a unitary phenomenon without investigating adjustments in neural and attentional processes that occur during social interactions. To address this limitation, we examined neural activity on a trial-by-trial basis during different social interactions. Our results show conflict monitoring neural alarm activation, indexed by the N2, in response to specific exclusionary events; even during interactions that are inclusionary overall and in the absence of self-reported feelings of social pain. Furthermore, we show enhanced attentional activation to exclusionary events, indexed by the P3b, during exclusionary, compared with inclusionary, interactions, and this P3b activation was associated with self-reported social distress following prolonged social exclusion. Finally, both the N2 and P3b showed larger amplitudes in the earlier stages of exclusion compared with later stages, suggesting heightened early sensitivity for both components. Together, these findings provide novel insights into the dynamic neural and perceptual processes of exclusion that exist during social interactions and the relationship between discrete events within interactions and the more general contexts of the social interactions. - INTRODUCTION Social exclusion gives rise to a diffuse pattern of behavioral and neural changes that can lead to severe emotional, cognitive, social and developmental impairments in targets of exclusion (Williams, 2001; Baumeister et al., 2002; Eisenberger et al., 2003; Masten et al., 2009). These effects include increases in aggressive social behavior, anxiety and depression (MacDonald and Leary, 2005; Williams et al., 2005) and decreases in self-esteem and the fulfillment of needs (Williams et al., 2001). Additionally, different patterns of neural activation are present during exclusion compared with inclusion, with enhanced activation of the anterior cingulate cortex (ACC) and right ventral prefrontal cortex (RVPFC) during exclusion (Eisenberger et al., 2003, 2007). In these studies, measures of neural activation were aggregated within blocks of social interactions, which show the overall patterns of activation for each type of interaction (i.e. inclusionary and exclusionary) but not the alterations in neural activation over the course of the interactions. This allows for general characterizations of the relationship between neural activation and self-reported feelings following exclusion but does not allow for the examination of adjustments in neural processes during social interactions. To address this issue, we conducted an event-related brain potential (ERP) study of social exclusion. ERP measurement allows for the examination of specific events within a larger social interaction due to the excellent temporal resolution of ERPs compared with other neuroimaging techniques and methodologies (e.g. functional magnetic resonance imaging; fMRI), which are temporally limited to examinations of social interactions at the level of the entire interaction. Therefore, we were able to examine specific patterns of neural activity in response to discrete events during ongoing social interactions, including neural alarm activation and related task-relevant attentional activations, within the larger contexts of different types of social interactions. Neural alarm and conflict monitoring The neural alarm is derived from conflict monitoring theory (Botvinick et al., 2001; Yeung et al., 2004), which describes the neural alarm as a conflict-based system implemented by the ACC that detects (or monitors) levels of conflict between actual outcomes and intended or desired outcomes during information processing. The activation of this ACC-based alarm then triggers adjustments in compensatory cognitive control to more successfully regulate thoughts and behaviors to obtain desired outcomes. Accordingly, conflict monitoring theory has suggested that there are at least two functionally linked but dissociable systems of cognitive control (see Botvinick et al., 2001, for review). The first is the ACC-based evaluative system, mentioned earlier and characterized as the neural alarm, which acts as a conflict monitor during information processing events (Botvinick et al., 2001; Yeung et al., 2004). Neuroimaging research has shown that the ACC is involved in the evaluative system by indicating when adjustments in control are warranted (MacDonald et al., 2000; Kerns et al., 2004). The second system is the regulative system, which exerts flexible adjustments in topdown control and attentional allocation during subsequent information processing. Available evidence indicates that this support is likely provided by the prefrontal cortex (MacDonald et al., 2000; Kerns et al., 2004), with different control processes associated with different regions within the prefrontal cortex. These control processes lead to compensatory activations in other attentional networks to improve subsequent behavioral outcomes during cognitive task execution or following a task when undesired or unwanted outcomes are perceived. Research has shown that the conflict-driven ACC activation is present during difficult tasks or task conditions (e.g. Stroop task) resulting in either correct or incorrect behavioral outcomes (Botvinick et al., 2001; Kerns et al., 2004; Yeung et al., 2004). This suggests that the neural alarm is not error or pain specific but is responsive to conflict regardless of response outcomes. Further, studies have indicated that ones neural alarm circuitry is responsive to the errors or negative outcomes of others (von Schie et al., 2004; Shane et al., 2008) independent of the individuals own behavioral or emotional responses. Conflict monitoring, then, is not solely reactive to personal negative outcomes. Rather, it is a constant and ongoing preconscious process that is present throughout environmental interactions that can be positive or negative in nature or can be personally experienced or observed. Alternatively, the regulation of conflict is a conscious process meant to modify behavior to achieve desired outcomes through the implementation of cognitive control, which adjusts the activation of attentional control networks to deal with the sources of the conflict or to cope with the consequences of the behavior. Therefore, conflict monitoring (...truncated)