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  • The neural correlates of PE are typically investigated

    2018-10-25

    The neural correlates of PE are typically investigated using paradigms in which participants learn how arbitrary stimuli predict positive or negative outcomes. Such paradigms are well suited for examining general aspects of PE learning but may be less well suited for studying socially anxious adolescents, who have unimpaired performance on most such paradigms (Dickstein et al., 2010). The present study uses a paradigm known to elicit biased responding in socially anxious adolescents (Guyer et al., 2008) as a preliminary investigation of the relationship between age, social anxiety, and the neural correlates of PE amiodarone hcl in a social context. Relative to traditional PE paradigms, this novel approach may be better suited for capturing between-group differences in PE, but less well suited for examining general aspects of PE learning. Given past work, we hypothesized that striatal-mPFC engagement would be uniquely altered among socially anxious adolescents. To test this hypothesis, amiodarone hcl activity was assessed with functional magnetic resonance imaging (fMRI) as participants predicted, and then received, expected (accurately predicted) or unexpected (inaccurately predicted) positive and negative feedback from high and low-value peers. Brain activity was then related to performance on a surprise memory task in which participants were asked to recall feedback valence. Socially anxious and non-anxious adolescents and adults were studied to directly compare associations among these groups.
    Methods and materials
    Results
    Discussion This study replicates prior behavioral findings in adolescents (Guyer et al., 2008) and extends them to adults. We demonstrate that predicted feedback from peers is related to their initial value. Both adults and adolescents expected more positive feedback from high-, relative to low-value peers. However, we also found age-based differences such that adolescents predicted significantly lower levels of positive feedback from low-value peers. Unique fMRI findings also emerged. Socially-anxious adolescents were the only group to show patterns typical of PE processing: striatal engagement during unexpected, relative to expected, positive outcomes (Schultz et al., 1997). This finding may reflect unique reward-related behavior and learning (O’doherty, 2004; Yin et al., 2009) in response to unexpected positive social feedback. Alternatively, since striatal engagement has also been linked to various forms of arousal (e.g., Izuma et al., 2008; Miller et al., 2014; Schiller and Delgado, 2010), findings may reflect more complex influences, including a mixture of fear and excitement specific to anxious adolescents. Likewise, the positive social feedback provided in the context of the chatroom task may not have been sufficiently potent to engender the experience of reward among anxious adults, and healthy participants. This paradigm includes one-time social feedback, purportedly generated at a distinct time period, from unknown peers with whom they are unlikely to interact with in the future. Thus, it is possible that striatal engagement during unexpected, relative to expected positive outcomes was observed among anxious adolescents because they were the only ones who experienced the outcomes as salient. Future work that matches the salience of social outcomes across adults and adolescents is needed to tease apart this relationship. PE-based learning, which occurs when predictions are updated (Schultz et al., 1997), has been linked to striatal-mPFC connectivity (Haber et al., 2006; O’doherty, 2004). Here, we found that socially anxious adolescents were unique in exhibiting more negative striatal-mPFC functional connectivity for unexpected, relative to expected, positive feedback from high-value peers. Thus in adolescence, an important contributor to social anxiety may relate to dysfunctional communication between the striatum and mPFC in response to unexpected positive social feedback. Specifically, dysregulated striatal-mPFC functional connectivity may have a deleterious effect on the ability to learn from a pleasantly surprising social interaction. Support for this hypothesis comes from results in the current study linking striatal-mPFC functional connectivity to deficits in recall for social feedback among socially anxious adolescents. Group differences in striatal connectivity were also found in ventrolateral PFC. This brain region is not typically implicated in PE processing, and did not relate to PE-based learning. Thus, differential striatal-vlPFC connectivity may relate to other aspects of cognition engaged during the task. One shortcoming of our use of traditional, as opposed to generalized PPI (gPPI) methods is that functional connectivity can only be interpreted for one condition (i.e., unexpected positive feedback from high value peers), relative to another condition (i.e., expected positive feedback from high value peers). gPPI analyses, which can accommodate more than two conditions within a single model, allows for more flexibility in statistical analyses, and provides greater insight into directionality of results by contrasting connectivity in each condition of interest relative to an implicit or explicit baseline (McLaren et al., 2012). Such techniques could be very beneficial to future work in this area.