Impact of observational and direct learning on fear conditioning generalization in humans

Abstract

Humans gain knowledge about threats not only from their own experiences but also from observing others' behavior. A neutral stimulus is associated with a threat stimulus for several times and the neutral stimulus will evoke fear responses, which is known as fear conditioning. When encountering a new event that is similar to one previously associated with a threat, one may feel afraid and produce fear responses. This is called fear generalization. Previous studies have mostly focused on fear conditioning and generalization based on direct learning, but few have explored how observational fear learning affects fear conditioning and generalization. To the best of our knowledge, no previous study has focused on the neural correlations of fear conditioning and generalization based on observational learning. In the present study, 58 participants performed a differential conditioning paradigm in which they learned the associations between neutral cues (i.e., geometric figures) and threat stimuli (i.e., electric shock). The learning occurred on their own (i.e., direct learning) and by observing other participant's responses (i.e., observational learning); the study used a within-subjects design. After each learning condition, a fear generalization paradigm was conducted by each participant independently while their behavioral responses (i.e., expectation of a shock) and electroencephalography (EEG) recordings or responses were recorded. The shock expectancy ratings showed that observational learning, compared to direct learning, reduced the differentiation between the conditioned threatening stimuli and safety stimuli and the increased shock expectancy to the generalization stimuli. The EEG indicated that in fear learning, threatening conditioned stimuli in observational and direct learning increased early discrimination (P1) and late motivated attention (late positive potential [LPP]), compared with safety conditioned stimuli. In fear generalization, early discrimination, late motivated attention, and orienting attention (alpha-event-related desynchronization [alpha-ERD]) to generalization stimuli were reduced in the observational learning condition. These findings suggest that compared to direct learning, observational learning reduces differential fear learning and increases the generalization of fear, and this might be associated with reduced discrimination and attentional function related to generalization stimuli.