Neurophysiological and Autonomic Dynamics of Threat Processing During Sustained Social Fear Generalization

Survival in rapidly changing environments requires that organisms learn to predict noxious outcomes based on situational cues. One key facet of successful threat prediction is generalization from a specific predictive cue to similar cues, ensuring that a cue-outcome contingency is applied beyond the original learning environment. Generalization has also been observed in laboratory studies of human aversive conditioning: Most behavioral and physiological processes generalize responses from a stimulus paired with threat, (the CS+), to unpaired stimuli, with response magnitudes varying as a function of stimulus similarity. In contrast, work focusing on sensory responses in visual cortex has found a sharpening pattern, in which responses to stimuli closely resembling the CS+ are maximally suppressed, potentially reflecting lateral inhibitory interactions with the CS+ representation. Originally demonstrated with simple visual cues, changes in visuocortical tuning have also been observed in threat generalization learning across facial identity cues. It is however unclear to what extent these visuocortical changes represent transient or sustained effects and if generalization learning requires prior conditioning to the CS+. The present study addressed these questions using EEG and pupillometry in a paradigm involving several hundreds of trials of aversive generalization learning along a gradient of facial identities. Visuocortical ssVEP sharpening occurred after dozens of trials of generalization learning without prior differential conditioning, but diminished as learning progressed further. By contrast, generalization of EEG alpha power suppression, pupil dilation, and self-reported valence and arousal ratings was seen throughout the experimental session. Findings are consistent with models of threat processing emphasizing the role of changing visucocortical and attention dynamics in the formation, curation, and shaping of fear memories as observers continue learning about stimulus-outcome contingencies.