Slow to warm up: The role of habituation in social fear

Abstract

Neural habituation allows familiar information to be ignored in favor of salient or novel stimuli. In contrast, failure to rapidly habituate likely reflects deficits in the ability to learn that an environment is predictable, familiar and safe. Differences in habituation rate may underlie individual differences in the tendency to approach or avoid novelty; however, many questions remain unanswered. Given the importance of adaptive social functioning, here we tested whether habituation differences to social stimuli are associated with differences in social fearfulness, a trait that ranges from low social fear-the adaptive tendency to approach novel social stimuli-to high social fear-the maladaptive tendency to avoid novel social stimuli. Higher social fearfulness was associated with slower habituation across regions of the social brain, including the hippocampus, amygdala, ventromedial prefrontal cortex, medial orbitofrontal cortex, fusiformface area, primary visual cortex, and extrastriate visual cortex. Interestingly, habituation differences were driven by sustained amygdala-visual cortex interactions, but not deficient amygdala-prefrontal cortex interactions. Together, these findings provide evidence that a failure to filter social stimuli is associated with a key social trait. In light of the link between social fear and dysfunction, individual differences in habituation may provide an important neurobiological marker for risk for psychiatric illness, such as social anxiety disorder.