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, fusiform face 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.

Keywords: amygdala; functional connectivity; hippocampus; social anxiety disorder; visual cortex.

Fig. 1.

Repeated faces task design. There were a total of 32 neutral face stimuli presented in this task. Each stimulus was presented either 1 time, 3 times, 5 times, or 7 times. Stimuli were presented in pseudo-random order for 1 s followed by a black screen for 2–4 s.

Fig. 2.

Differences in neural response to faces. (A) Social fearfulness was correlated with higher initial amplitudes to first face presentations in the hippocampus and vmPFC. (B) Social fearfulness was also correlated with higher b′ slope values between the third and fifth face exposure, indicating a slower rate of habituation, in the amygdala, hippocampus, vmPFC, mOFC, V1 and extrastriate cortex.

Fig. 3.

Differences in habituation of amygdala functional connectivity. Social fearfulness was correlated with sustained signaling between the amygdala and two visual cortex regions, the extrastriate cortex and V1, between the third and fifth face exposure.