Reward Prediction Error Signaling during Reinforcement Learning in Social Anxiety Disorder is altered by Social Observation

Abstract

BACKGROUNDDysfunctional expectations of impending social or performance outcomes are core features of Social Anxiety Disorder (SAD) but often lack formal definition in clinical research. Reinforcement learning (RL) models offer a framework to define changes in outcome expectations in a formal way by computing the prediction error (PE). This study quantifies the updating of expectations by PEs in SAD and investigates alterations in RL regions associated with PE signaling.METHOD48 adult participants (24 diagnosed with SAD and 24 age-, gender-, and education- matched healthy controls (HC)) underwent event-related functional magnetic resonance imaging while learning from probabilistic feedback. Crucially, both groups completed two parallel versions of the task: one in which they learned under scrutiny (social observation) and one in which they learned without being overtly evaluated (non-social control condition).RESULTSCoupling to prediction errors in SAD was elevated in dorsomedial prefrontal cortex (DMPFC) when learning under observation. These findings provide the first evidence that PE signaling during social performance situations in SAD is associated with hypersensitive response signatures in DMPFC, a brain region associated with using others’ value standards as a proxy for one’s own value standards. Dynamic Causal Modelling further revealed that RPE-modulated connectivity from ventral pallidum to DMPFC during observation was reduced in SAD.CONCLUSIONSThe present results corroborate a crucial role of DMPFC in SAD, which corresponds to dysfunctional expectations about others’ alleged performance standards that play a prominent role in current models of the disorder.

You never get a chance to undo a negative first impression: Social anxiety is associated with impaired positive updating of social information

“…In these studies, SA has been consistently associated with enhanced learning of information that results in negative outcomes (Abraham & Hermann, 2015;social stimuli;Becker et al, 2019;Peterburs et al, 2021;non-social stimuli), whereas positive outcomes yielded mixed results (Khdour et al, 2016;Koban et al, 2017;Reilly et al, 2020). Importantly, these studies have used probabilistic tasks that imitate volatile and uncertain environments (Becker et al, 2019;Voegler et al, 2019), which require tolerance of uncertainty, a major difficulty for individuals with anxiety (Flores et al, 2018;Lamba et al, 2020). Therefore, it is difficult to disentangle the ramifications of the uncertain learning environments from the effects of learning negative and positive information in SA.…”

“…Several studies have examined the relationship between SA and the ability to learn new information with positive and negative outcomes (Abraham & Hermann, 2015;Becker et al, 2019;Peterburs et al, 2021). In these studies, SA has been consistently associated with enhanced learning of information that results in negative outcomes (Abraham & Hermann, 2015;social stimuli;Becker et al, 2019;Peterburs et al, 2021;non-social stimuli), whereas positive outcomes yielded mixed results (Khdour et al, 2016;Koban et al, 2017;Reilly et al, 2020).…”

“…Several studies have examined the relationship between SA and the ability to learn new information with positive and negative outcomes (Abraham & Hermann, 2015;Becker et al, 2019;Peterburs et al, 2021). In these studies, SA has been consistently associated with enhanced learning of information that results in negative outcomes (Abraham & Hermann, 2015;social stimuli;Becker et al, 2019;Peterburs et al, 2021;non-social stimuli), whereas positive outcomes yielded mixed results (Khdour et al, 2016;Koban et al, 2017;Reilly et al, 2020). Importantly, these studies have used probabilistic tasks that imitate volatile and uncertain environments (Becker et al, 2019;Voegler et al, 2019), which require tolerance of uncertainty, a major difficulty for individuals with anxiety (Flores et al, 2018;Lamba et al, 2020).…”

The impact of incidental anxiety on the neural signature of mentalizing

“…Anxiety is an emotion that is particularly prevalent for human behavior (Bandelow et al 2015), as its presence signals the occurrence of negative events that can be crucial for survival. Recent research has begun to investigate the effects of such incidental anxiety on cognitive processes including attention (Bar-Haim et al, 2007;Bradley et al, 2010;Cisler & Koster, 2010;MacLeod & Mathews, 1988), memory (Andreotti et al, 2011;Balderston et al, 2017;Bolton & Robinson, 2017;Vytal et al, 2013), and learning (Becker et al, 2019;Berghorst et al, 2013;Browning et al, 2015;Cavanagh et al, 2019;DeVido et al, 2009;Grupe, 2017;Robinson et al, 2013;Safra et al, 2018;Stevens et al, 2014;Ting et al, 2020). Despite this recent surge in the interest concerning the effects of incidental anxiety on cognitive processes and its neural correlates, relatively little is known about its impact on arguably one of the most important cognitive processes for human interaction, namely social cognitions such as mentalizing.…”