Fear extinction retention in children, adolescents, and adults

Abstract

Past results suggest that fear extinction and the return of extinguished fear are compromised in adolescents. However, findings have been inconclusive as there is a lack of fear extinction and extinction retention studies including children, adolescents and adults. In the present study, 36 children (6-9 years), 40 adolescents (13-17 years) and 44 adults (30-40 years), underwent a two-day fear conditioning task. Habituation, acquisition, and extinction were performed on the first day and an extinction retention test > 24 h later. Skin conductance responses were recorded during all phases of fear conditioning and functional magnetic resonance imaging (fMRI) was conducted during the fear retention test. All groups acquired and extinguished fear as measured with SCR, with no group differences in SCR during extinction retention. The groups had largely similar neural fear responses during the retention test, apart from adolescents displaying stronger amygdala fear response than children, with no differences between adolescents and adults. The findings do not support an adolescent extinction dip, and there was only marginal evidence of progressive changes in fear conditioning across development. In contrast to findings in rodents, fear conditioning in humans may elicit similar physiological responses and recruit similar neural networks from childhood to adulthood.

Keywords: Development; FMRI; Fear conditioning; Fear extinction; Fear retention; Threat conditioning.

Fig. 1

Illustration of the fear conditioning task. In session 1, participants underwent habituation, fear acquisition and extinction learning in the lab, and in session 2, > 24 h later, the extinction retention test was performed inside the magnetic resonance imaging (MRI) scanner. The conditioned stimulus (CS) that was paired with the unconditioned stimulus (US) scream (CS+) was counterbalanced across participants.

Fig. 2

Flow chart of inclusion/exclusion of participants.

Fig. 3

Square-root (sqrt) of skin conductance responses (SCR) to the conditioned stimulus paired with a scream (CS+) and never-paired (CS-) during the four phases of conditioning in children, adolescents, and adults. Error bars denote standard error.

Fig. 4

Fear ratings to conditioned stimuli. Ratings (1−5) of fear to the CS+ (red) and CS- (blue) before habituation, after fear acquisition, and after extinction learning in all age groups.

Fig. 5

Fear retention in the brain. Across age groups, fear retention (CS+>CS-) was detected mainly in the insula and the mid-cingulate region, but also included clusters in the anterior PFC, and the paracingulate gyrus. Statistical parametric maps thresholded at family-wise error corrected (FWE) p_FWE< .05 and overlaid on T1-weighted anatomical reference images. Color bar indicates Z scores. A: anterior, L: left.