Contingency awareness shapes neural responses in fear conditioning

TL;DR

The study shows that fear conditioning in the brain requires awareness of the relationship between stimuli.

Contribution

This study provides empirical evidence that fear conditioning depends on contingency awareness.

Findings

Only participants aware of the stimulus relationship showed neural learning signs.

Aware participants had stronger theta responses and attention-related brain activity.

Anxiety and personality traits did not predict contingency awareness.

Abstract

Contingency awareness refers to an observer’s ability to identify the association between a conditioned and an unconditioned stimulus (US). A widely held belief in human fear conditioning is that this form of associative learning may occur independently of contingency awareness. To test this hypothesis, in this preregistered study (https://osf.io/vywq7), we recorded electroencephalography during a task, where participants were presented with compounds of a word (drawn from two semantic categories) and tactile stimulation (vibration), followed by either a neutral sound (US−) or a loud noise (US+). Based on interviews, participants were divided into an aware (N = 50) and an unaware (N = 31) group. Only the aware group showed evidence of learning at the neural level, notably a larger stimulus-preceding negativity developing before US+ and a stronger theta response to vibrations predicting the US+. The aware group also showed stronger alpha and beta suppression around the vibrations and a weaker theta response to US+, possibly indicating heightened attention to the cue and the violation/confirmation of expectation. Group differences in alpha and beta suppression were already present before the aversive learning began, suggesting that elevated attention may precede and facilitate awareness. Personality tests showed that elevated anxiety, neuroticism, higher intolerance of uncertainty, or harm avoidance is not predictive of the acquisition of contingency awareness. Our findings support the notion that fear conditioning, as reflected in cortical measures, cannot occur without contingency awareness.

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