Emotionally Aversive Cues Suppress Neural Systems Underlying Optimal Learning in Socially Anxious Individuals

J Neurosci. 2019 Feb 20;39(8):1445-1456. doi: 10.1523/JNEUROSCI.1394-18.2018. Epub 2018 Dec 17.

Abstract

Learning and decision-making are modulated by socio-emotional processing and such modulation is implicated in clinically relevant personality traits of social anxiety. The present study elucidates the computational and neural mechanisms by which emotionally aversive cues disrupt learning in socially anxious human individuals. Healthy volunteers with low or high trait social anxiety performed a reversal learning task requiring learning actions in response to angry or happy face cues. Choice data were best captured by a computational model in which learning rate was adjusted according to the history of surprises. High trait socially anxious individuals used a less-dynamic strategy for adjusting their learning rate in trials started with angry face cues and unlike the low social anxiety group, their dorsal anterior cingulate cortex (dACC) activity did not covary with the learning rate. Our results demonstrate that trait social anxiety is accompanied by disruption of optimal learning and dACC activity in threatening situations.SIGNIFICANCE STATEMENT Social anxiety is known to influence a broad range of cognitive functions. This study tests whether and how social anxiety affects human value-based learning as a function of uncertainty in the learning environment. The findings indicate that, in a threatening context evoked by an angry face, socially anxious individuals fail to benefit from a stable learning environment with highly predictable stimulus-response-outcome associations. Under those circumstances, socially anxious individuals failed to use their dorsal anterior cingulate cortex, a region known to adjust learning rate to environmental uncertainty. These findings open the way to modify neurobiological mechanisms of maladaptive learning in anxiety and depressive disorders.

Keywords: anterior cingulate cortex; decision-making; learning; reward; social anxiety.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Anger
  • Anxiety / physiopathology*
  • Anxiety / psychology
  • Bayes Theorem
  • Brain Mapping
  • Choice Behavior
  • Cues
  • Emotions / physiology*
  • Facial Expression*
  • Female
  • Gyrus Cinguli / physiology
  • Happiness
  • Humans
  • Learning / physiology*
  • Models, Psychological
  • Punishment
  • Reward