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

Abstract

Rapid habituation to repeated presentations of stimuli that are neither threatening nor rewarding is crucial for effectively navigating the constantly changing environment. Failure to habituate has been proposed as a neuronal mechanism underlying social anxiety. In this study, we test the hypothesis that social fearfulness is associated with reduced neural habituation to social stimuli. Twenty-nine individuals representing the full dimension of social fearfulness (low to high) viewed repeated presentations (up to 7) of neutral social and nonsocial stimuli during an fMRI study. Percent signal change was extracted from a priori regions of interest—including the amygdala, hippocampus, medial orbitofrontal cortex (mOFC), ventromedial prefrontal cortex (vmPFC), fusiform face area (FFA), extrastriate cortex, and primary visual cortex (V1)—areas that have been previously implicated in social anxiety disorder. Social fearfulness was correlated with elevated initial response to faces in the hippocampus and vmPFC, and habituation differences to faces in the amygdala, hippocampus, mOFC, vmPFC, extrastriate, and V1 (p < .05). Higher social fear was associated with a sustained response relative to individuals with low social fear, who showed rapid habituation to repeated social stimuli. Social fearfulness was also correlated with sustained functional connectivity between the amygdala and two visual cortex regions—the extrastriate cortex and V1. Importantly, social fearfulness findings were similar when controlling for neural response to non-social stimuli (objects), suggesting that differences were specific to social stimuli. Individual differences in habituation to social stimuli may provide an important neurobiological marker for risk for psychiatric illness, such as social anxiety disorder.