Structural and functional connectivity changes in the brain associated with shyness but not with social anxiety

Abstract

Shyness and social anxiety are correlated to some extent and both are associated with hyper-responsivity to social stimuli in the frontal cortex and limbic system. However to date no studies have investigated whether common structural and functional connectivity differences in the brain may contribute to these traits. We addressed this issue in a cohort of 61 healthy adult subjects. Subjects were first assessed for their levels of shyness (Cheek and Buss Shyness scale) and social anxiety (Liebowitz Social Anxiety scale) and trait anxiety. They were then given MRI scans and voxel-based morphometry and seed-based, resting-state functional connectivity analysis investigated correlations with shyness and anxiety scores. Shyness scores were positively correlated with gray matter density in the cerebellum, bilateral superior temporal gyri and parahippocampal gyri and right insula. Functional connectivity correlations with shyness were found between the superior temporal gyrus, parahippocampal gyrus and the frontal gyri, between the insula and precentral gyrus and inferior parietal lobule, and between the cerebellum and precuneus. Additional correlations were found for amygdala connectivity with the medial frontal gyrus, superior frontal gyrus and inferior parietal lobule, despite the absence of any structural correlation. By contrast no structural or functional connectivity measures correlated with social or trait anxiety. Our findings show that shyness is specifically associated with structural and functional connectivity changes in cortical and limbic regions involved with processing social stimuli. These associations are not found with social or trait anxiety in healthy subjects despite some behavioral correlations with shyness.

Figure 1. Regions showing positive correlation between GM density and shyness scores without using anxiety scores as covariates.

Shyness scores are positively correlated with GM density in the bilateral superior temporal gyri and parahippocampal gyri, and also in the right insula and left cerebellum posterior lobe, when age, gender, and total intracranial volume are used as covariants (at a cluster lever with family wise corrected at p<0.05). Scatter plots show correlations between regional density in left cerebellum posterior lobe and right superior temporal gyrus and shyness and social anxiety scores. Images are presented in radiological orientation. Hot colors indicate brain regions with significant positive correlations with shyness.

Figure 2. Regions with GM changes showing positive and negative correlations between functional connectivity and shyness without other anxiety correction.

Shyness scores are significantly correlated with functional connectivity in left cerebellum (A), right insula (B), bilateral superior temporal gyri (C&D), and bilateral parahippocampal gyri (E & F) seeds. Images are presented in radiological orientation. Hot and cold colors indicate brain regions with significant positive (hot) and negative (cold) correlations with shyness.

Figure 3. Positive and negative correlations with shyness involving amygdala functional connectivity and without other anxiety correction.

Images are presented in radiological orientation. Hot and cold colors indicate brain regions with significant positive (hot) and negative (cold) correlations with shyness using the right (A) and left (B) amygdala as seeds.

Figure 4. Schematic representation of the functional connectivity associated with shyness.

(A) Regions showing positive correlations between functional connectivity and shyness (seeds located in right superior temporal gyrus and left cerebellum posterior lobe; (B) Regions showing negative correlations between functional connectivity and shyness (seeds located in bilaterally parahippocampal gyri); (C) Regions showing both positive and negative correlations between functional connectivity and shyness (seeds located in the bilateral amygdalae). Scatter plots on the right show correlations between regional functional connectivity (FC) value and shyness and social anxiety scores. Abbreviations: L-Cere, left cerebellum posterior lobe; R-Precu, right precuneus; R-STG, right superior temporal gyrus; R-SFG, right superior frontal gyrus; L-IFG, left inferior frontal gyrus; L-PHG, left parahippocampal gyrus; R-PHG, right parahippocampal gyrus; R-PCG, right postcentral gyrus; R-MFG, right middle frontal gyrus; L-AMG, left amygdala; R-AMG, right amygdala; R-IPL, right inferior parietal lobule; L-MedFG, left medial frontal gyrus; L-MidFG, left middle frontal gyrus.