Individual differences in social behavior predict amygdala response to fearful facial expressions in Williams syndrome

Abstract

Williams syndrome (WS) is a genetic condition often paired with abnormal social functioning and behavior. In particular, those with WS are characterized as being relatively hypersocial, overly emotional/empathic, and socially uninhibited or fearless. In addition, WS is associated with abnormal amygdala structure and function. Very little is known however about the relationship between specific social behaviors and altered amygdala function in WS. This study was designed to compare three models that relate abnormal social behavior with amygdala function in WS (indiscriminate sociability, emotional and empathic sociability and social fearlessness). We used a social behavior assessment procedure (Salk Institute Sociability Questionnaire), functional magnetic resonance imaging and an implicit emotion face processing task to test these models. Our findings provide support for a model of abnormal social fearlessness by showing that in WS, abnormal amygdala response to fear is paired with an increased tendency to approach strangers. Specifically, individuals with WS that exhibited less amygdala response to fearful facial expressions (compared to neutral) also exhibited an increased tendency to approach strangers. These findings contribute to our understanding of social and emotional functioning in neurodevelopmental conditions and provide evidence that in WS, amygdala response to fear modulates social behavior.

Figure 1

Model based hypotheses relating social behavior with amygdala function in WS. We predicted that if abnormal indiscriminate sociability is associated with amygdala function in WS (A), we would observe a relationship between Social Approach scores and amygdala response to facial expressions (fearful, happy and neutral combined) compared to scrambled images. We predicted that if abnormal emotional and empathic sociability is associated with amygdala function in WS (B), we would observe a relationship between Emotional/Empathic Sociability scores and amygdala response to emotional facial expressions (fear and happy, combined) compared to neutral. We predicted that if abnormal social fearlessness is associated with amygdala function in WS (C), we would observe a relationship between Social Approach Toward Strangers and amygdala response to fearful facial expressions compared to neutral.

Figure 2

Examples of stimuli used in the experimental paradigm. Participants were presented with photographs of faces conveying fearful, happy, neutral expressions and scrambled images. Participants were instructed to judge if each stimulus was either male, female or scrambled as quickly and as accurately as possible. Behavioral responses were collected within the 2000 ms following the onset of each stimulus.

Figure 3

Individual differences in Social Approach Toward Strangers scores associated with left amygdala response to fearful, compared to neutral, facial expressions in WS. Social Approach Toward Strangers scores are plotted on the x-axis. Contrast estimates within the left amygdala are plotted on the y-axis. Data were extracted from the peak voxel located at MNI coordinates: −20, −6, −6; (t = 6.41; p < .05 corrected). Cluster found to display a significant correlation is overlaid upon on a coronal slice of a representative WS brain normalized into standard stereotactic space.