Potentiated perceptual neural responses to learned threat during Pavlovian fear acquisition and extinction in adolescents

Abstract

Adolescents' experience of heightened anxiety and increased vulnerability to develop anxiety disorders is believed to partly result from blunted fear extinction processes. However, whether this anxiety is mediated by adolescent-specific differences in perceptual responses to learned threat is not known. To investigate this, we used EEG to examine reinforcement-dependent changes in early visual event-related potentials in adolescents (N = 28, 13-14 years) and adults (N = 23, 25-26 years old) during a differential Pavlovian fear conditioning task, with one conditioned stimulus (CS+) paired with an aversive sound (unconditioned stimulus [US]) on 50% of trials, and another (CS-) never paired with the US. An immediate extinction phase followed, where both CSs were presented alone. We found age-dependent dissociations between explicit and implicit measures of fear learning. Specifically, both adolescents and adults demonstrated successful fear conditioning and extinction according to their explicit awareness of changes in CS contingencies and their evaluative CS ratings, and their differential skin conductance responses. However, for the first time we show age differences at the neural level in perceptual areas. Only adolescents showed greater visual P1 and N1 responses to the CS+ compared to the CS- during acquisition, a dissociation that for the N1 was maintained during extinction. We suggest that the adolescent perceptual hyper-responsivity to learned threat and blunted extinction reported here could be an adaptive mechanism to protect adolescents from harm. However, this hyper-responsivity may also confer greater vulnerability to experience pathological levels of anxiety at this developmental stage.

Keywords: adolescence; anxiety; event-related potentials; fear conditioning; fear extinction.