Neural Responses During Trace Conditioning with Face and Non-Face Stimuli Recorded with Magnetoencephalography

Abstract

During fear conditioning a subject is presented with an initially innocuous stimulus like an image (conditioned stimulus; CS) that predicts an aversive outcome like a mild electric shock (unconditioned stimulus; UCS). Subjects rapidly learn that the CS predicts the UCS, and show autonomic fear responses (CRs) during the presentation of the CS. When the CS and the UCS coterminate, as is the case for delay conditioning, individuals can acquire CRs even if they are unable to predict the occurrence of the UCS. However when there is a temporal gap between the CS and the UCS, CR expression is typically dependent upon explicit awareness of the CS-UCS pairing. Research with non-human animals suggests that both the hippocampus and the prefrontal cortex are needed for trace but not delay fear conditioning, and that communication between these areas may help to maintain the CS during the trace interval. We tested this hypothesis by exposing subjects to differential delay and trace fear conditioning while we recorded their brain activity with magnetoencephalography. Faces and houses served as CSs and an aversive electrical stimulation served as the UCS. As predicted, subjects show evidence of conditioning on both implicit and explicit measures. In addition, there is a learning related increase in theta coherence between the left parahippocampal gyrus and several frontal and parietal cortical regions for trace but not delay conditioning. These results suggest that trace conditioning recruits a network of cortical regions, and that the activity of these regions is coordinated by the medial temporal lobe