Fear conditioning prompts sparser representations of conditioned threat in primary visual cortex

Repeated exposure to threatening stimuli alters sensory responses. We investigated the underlying neural mechanism by recording simultaneous EEG-fMRI from human participants viewing oriented gratings during Pavlovian fear conditioning. In acquisition, one grating (the CS+) was paired with a noxious noise, the unconditioned stimulus (US). The other grating (CS-) was never paired with US. In habituation, which preceded acquisition, and in final extinction, the same two gratings were presented without the US. Using fMRI-BOLD multivoxel patterns in primary visual cortex during habituation as reference, we found that during acquisition, aversive learning selectively prompted systematic changes in multivoxel patterns evoked by the CS+. Specifically, CS+ evoked voxel patterns in V1 became sparser as aversive learning progressed, and the sparse pattern was preserved in extinction. Concomitant with the voxel pattern changes, occipital alpha oscillations were increasingly more desynchronized during CS+ (but not CS-) trials. Across acquisition trials, the rate of change in CS+-related alpha desynchronization was correlated with the rate of change in multivoxel pattern representations of the CS+. Furthermore, alpha oscillations co-varied with BOLD in the right temporal-parietal junction, but not with BOLD in the amygdala. Thus, fear conditioning prompts persistent sparsification of threat cue representations, likely mediated by attention-related mechanisms.