Forgetting the best when predicting the worst: Preliminary observations on neural circuit function in adolescent social anxiety

Abstract

Social anxiety disorder typically begins in adolescence, a sensitive period for brain development, when increased complexity and salience of peer relationships requires novel forms of social learning. Disordered social learning in adolescence may explain how brain dysfunction promotes social anxiety. Socially anxious adolescents (n = 15) and adults (n = 19) and non-anxious adolescents (n = 24) and adults (n = 32) predicted, then received, social feedback from high and low-value peers while undergoing functional magnetic resonance imaging (fMRI). A surprise recall task assessed memory biases for feedback. Neural correlates of social evaluation prediction errors (PEs) were assessed by comparing engagement to expected and unexpected positive and negative feedback. For socially anxious adolescents, but not adults or healthy participants of either age group, PEs elicited heightened striatal activity and negative fronto-striatal functional connectivity. This occurred selectively to unexpected positive feedback from high-value peers and corresponded with impaired memory for social feedback. While impaired memory also occurred in socially-anxious adults, this impairment was unrelated to brain-based PE activity. Thus, social anxiety in adolescence may relate to altered neural correlates of PEs that contribute to impaired learning about social feedback. Small samples necessitate replication. Nevertheless, results suggest that the relationship between learning and fronto-striatal function may attenuate as development progresses.

Keywords: Development; Learning; Medial prefrontal cortex; Peer feedback; Prediction error; Striatum.

Fig. 1

Depiction of “Chatroom Task”. (A) On the initial visit, participants selected peers they wanted to chat with (high-value) and rejected those they did not want to chat with (low-value). (B) On the second visit, participants underwent an fMRI scan. During the first run of fMRI data acquisition, participants predicted the social feedback they would receive from high- and low-value peers (ratings 0–50 = negative feedback predicted; ratings 51–100 = positive feedback predicted). (C) During the second run of fMRI data acquisition, participants received expected (accurately predicted) or unexpected (inaccurately predicted) social feedback from peers. Neuroimaging results were constrained to this functional run. (D) After scanning, participants were unexpectedly asked to recall the social feedback they received from each peer.

Fig. 2

Flow-chart depicting definition of events. Three within subject factors are depicted in columns across the bottom. Peer valuation (column 1): Participants selected age-matched peers they wanted to chat with (high-value) and rejected those they did not want to chat with (low-value) in a pre-scan visit. Predict social feedback (column 2): Participants predicted whether high- and low-value peers would provide them with positive or negative social feedback. Receive social feedback (column 3): Participants received unexpected (inaccurately predicted) or expected (accurately predicted) social feedback from peers. This column depicts the eight task-specific regressors that were modeled for individual level fMRI analyses. For example, a participant may have predicted negative feedback from a high value peer. If they received positive feedback, that event would be characterized as unexpected (inaccurately predicted). However, if the participant predicted positive feedback, and then received positive feedback, that event would be characterized as expected (accurately predicted). Brain activity associated with prediction error was calculated by subtracting expected from unexpected social feedback from high-value peers [(A) positive and (B) negative feedback] and from, low-value peers [(C) positive and (D) negative feedback].

Fig. 3

Predicted social feedback measured by behavioral responding. (A) Average predicted social feedback for high- and low-value peers across all groups. (B) An age group × peer value interaction was driven by adolescents predicting lower levels of positive feedback from low-value peers than adults. (C) Anxious participants had a trend towards predicting lower levels of positive feedback from peers than non-anxious participants. ***p < .005; ∼p < .06.

Fig. 4

Brain regions differentially engaged by prediction errors. (A) Bilateral striatal activity for prediction errors varied by age group and anxiety, depending on peer value and feedback. This reflects a significant 5-way interaction between social anxiety (anxious/non-anxious) × age group (adult/adolescent) × peer value (high/low) × actual social feedback (positive/negative) × prediction error (expected/unexpected peer feedback) interaction. (B) Activation from right caudate was extracted and plotted to facilitate interpretation. Brain activity associated with prediction error (reflected by each bar) was calculated by subtracting inaccurate predictions from accurate predictions. ***p < .005.

Fig. 5

Functional connectivity and recall for positive feedback from high-value peers. (A) Results from psychophysiological interaction analyses, using a 6 mm sphere in right caudate as a seed (centered at 14, 14, 6), demonstrate group differences in functional connectivity between the striatum and mPFC during unexpected, relative to expected, positive feedback. (B) Activity from right caudate was extracted for each participant and plotted to facilitate interpretation. On the y-axis: negative values reflect more negative mPFC-striatal functional connectivity during unexpected (inaccurately predicted) relative to expected (accurately predicted) feedback, positive values reflect more positive mPFC-striatal functional connectivity during unexpected (inaccurately predicted) relative to expected (accurately predicted) feedback. (C) Recall of social feedback. Dotted line represents chance (probability of recall = .50). (D) Among adolescents, but not adults, negative mPFC-striatal functional connectivity was associated with worse recall for unexpected feedback, relative to expected positive feedback. On the x-axis: negative values indicate worse recall for unexpected than expected positive feedback; positive values indicate better recall for unexpected than expected positive feedback; 0 values indicate equal recall for expected and unexpected positive feedback. *p < .05; **p < .01; ***p < .005.