In the eye of the beholder: individual differences in perceived social isolation predict regional brain activation to social stimuli

Abstract

Prior research has shown that perceived social isolation (loneliness) motivates people to attend to and connect with others but to do so in a self-protective and paradoxically self-defeating fashion. Although recent research has shed light on the neural correlates of social perception, cooperation, empathy, rejection, and love, little is known about how individual differences in loneliness relate to neural responses to social and emotional stimuli. Using functional magnetic resonance imaging, we show that there are at least two neural mechanisms differentiating social perception in lonely and nonlonely young adults. For pleasant depictions, lonely individuals appear to be less rewarded by social stimuli, as evidenced by weaker activation of the ventral striatum to pictures of people than of objects, whereas nonlonely individuals showed stronger activation of the ventral striatum to pictures of people than of objects. For unpleasant depictions, lonely individuals were characterized by greater activation of the visual cortex to pictures of people than of objects, suggesting that their attention is drawn more to the distress of others, whereas nonlonely individuals showed greater activation of the right and left temporo-parietal junction to pictures of people than of objects, consistent with the notion that they are more likely to reflect spontaneously on the perspective of distressed others.

Figure 1

Results from 2(Valence: unpleasant, pleasant) × 2(Content: nonsocial, social) × UCLA (continuous) GLMs conducted on participants’ valence ratings (top panel) and arousal ratings (bottom panel). Estimates at 1 SD above and below the mean UCLA score in our sample are presented; error bars represent one SE.

Figure 2

A cluster of voxels centered in the ventral striatum, but extending to the amygdala and portions of the anterior thalamus, showed an inverse relationship between loneliness and activation in the Pleasant Social – Pleasant Nonsocial contrast. The scatterplots demonstrate the association between loneliness and activity in this cluster in response to pleasant social pictures, r(21) = −.46, p < .05, and in response to pleasant nonsocial pictures, r(21) = .69, p < .001. Estimated impulse response functions and mean percent signal change AUC for participants lower and higher in loneliness (estimates at 1 SD above and below the mean UCLA score in our sample are presented) shows a crossover interaction for the relationship between loneliness and brain responses to pleasant social and pleasant nonsocial stimuli, such that nonlonely participants exhibit greater activation to pleasant pictures that contain social content and lonely participants exhibit greater activation to pleasant nonsocial pictures.

Figure 3

(a) Clusters of voxels in the left and right visual cortices exhibited a positive relationship between loneliness and activation in the Unpleasant Social – Unpleasant Nonsocial contrast; whereas clusters of voxels in the left and right TPJ exhibited a negative relationship between loneliness and activation in the Unpleasant Social – Unpleasant Nonsocial contrast. (b) The scatterplot depicts the relationship between loneliness and activation of the left visual cortex in response to Unpleasant Social – Unpleasant Nonsocial pictures, r(21) = .83, p < .001. Estimated IRFs (and AUC values) show that individuals with higher loneliness showed greater activation to unpleasant social pictures. Results were comparable for the right visual cortex. (c) The scatterplot shows the inverse relationship between loneliness and activation of the right temporoparietal junction (TPJ) in response to Unpleasant Social – Unpleasant Nonsocial pictures, r(21) = −.58, p < .01. Estimated IRFs show that individuals lower in loneliness showed greater activation of the right TPJ to unpleasant social pictures in particular. Results were comparable for the left TPJ.