Emotion regulation in social anxiety disorder: behavioral and neural responses to three socio-emotional tasks

Michal Ziv, Philippe R Goldin, Hooria Jazaieri, Kevin S Hahn, James J Gross, Michal Ziv, Philippe R Goldin, Hooria Jazaieri, Kevin S Hahn, James J Gross

Abstract

Background: Social anxiety disorder (SAD) is thought to involve deficits in emotion regulation, and more specifically, deficits in cognitive reappraisal. However, evidence for such deficits is mixed.

Methods: Using functional magnetic resonance imaging (fMRI) of blood oxygen-level dependent (BOLD) signal, we examined reappraisal-related behavioral and neural responses in 27 participants with generalized SAD and 27 healthy controls (HC) during three socio-emotional tasks: (1) looming harsh faces (Faces); (2) videotaped actors delivering social criticism (Criticism); and (3) written autobiographical negative self-beliefs (Beliefs).

Results: Behaviorally, compared to HC, participants with SAD had lesser reappraisal-related reduction in negative emotion in the Beliefs task. Neurally, compared to HC, participants with SAD had lesser BOLD responses in reappraisal-related brain regions when reappraising faces, in visual and attention related regions when reappraising criticism, and in the left superior temporal gyrus when reappraising beliefs. Examination of the temporal dynamics of BOLD responses revealed late reappraisal-related increased responses in HC, compared to SAD. In addition, the dorsomedial prefrontal cortex (DMPFC), which showed reappraisal-related increased activity in both groups, had similar temporal dynamics in SAD and HC during the Faces and Criticism tasks, but greater late response increases in HC, compared to SAD, during the Beliefs task. Reappraisal-related greater late DMPFC responses were associated with greater percent reduction in negative emotion ratings in SAD patients.

Conclusions: These results suggest a dysfunction of cognitive reappraisal in SAD patients, with overall reduced late brain responses in prefrontal regions, particularly when reappraising faces. Decreased late activity in the DMPFC might be associated with deficient reappraisal and greater negative reactivity.

Trial registration: ClinicalTrials.gov identifier: NCT00380731.

Figures

Figure 1
Figure 1
The three socio-emotional tasks. (a) Looming harsh faces (Faces); (b) Social criticism (Criticism); (c) Negative self-beliefs (Beliefs). Each task was composed of ‘React’ and ‘Reappraise’ trials, which consisted of: (1) a 1.5-s ‘Cue’; (2) a socio-emotional stimulus (a looming harsh face/ a video-clip of an actor delivering social criticism/ an autobiographical sentence + negative self-beliefs); and (3) a negative emotion rating scale. Participants were instructed to either react normally to the stimuli without any attempt to control, modify, or regulate their reactions (‘React’), or to try and down regulate negative emotion reactions by actively reinterpreting the meaning of the emotion inducing stimulus (‘Reappraise’).
Figure 2
Figure 2
Faces task: brain responses during Reappraise versus React in SAD and HC. (a) Differential BOLD responses in patients with SAD versus healthy controls (HC > SAD). 1 = left inferior frontal gyrus, 2 = dorsal ACC, 3 = left lateral orbitofrontal cortex. (b) Common BOLD responses in patients with SAD and healthy controls. 1 = left cuneus, 2 = left lingual gyrus, 3 = left parahippocampus, 4 = left middle temporal gyrus, 5 = left precentral gyrus, 6 = dorsomedial PFC. Statistical threshold for BOLD responses: t-value threshold ≥2.93, voxel P <0.005, minimum cluster volume threshold ≥244 mm3 (6 voxels × 3.438 mm3), cluster-wise P <0.01.
Figure 3
Figure 3
Faces task: temporal dynamics of the BOLD response during Reappraise versus React in SAD and HC. Asterisks represent a significant between-group difference in the average of the first three time points (early) or last three time points (late) BOLD responses. (a) Left inferior frontal gyrus; (b) Dorsal ACC; (c) Left lateral orbitofrontal cortex.
Figure 4
Figure 4
Criticism task: brain responses during Reappraise versus React in SAD and HC. (a) Differential BOLD responses in patients with SAD versus healthy controls (HC > SAD). 1 = left fusiform gyrus, 2 = right fusiform gyrus, 3 = left putamen, 4 = left lingual gyrus, 5 = right cerebellum. (b) Common BOLD responses in patients with SAD and healthy controls. 1 = right precuneus, 2 = dorsomedial PFC, 3 = left dorsolateral PFC. Statistical threshold for BOLD responses: t-value threshold ≥2.93, voxel P <0.005, minimum cluster volume threshold ≥244 mm3 (6 voxels × 3.438 mm3), cluster-wise P <0.01.
Figure 5
Figure 5
Criticism task: temporal dynamics of the BOLD response during Reappraise versus React in SAD and HC. Asterisks represent a significant between-group difference in the average of the first three time points (early) or last two time points (late) BOLD responses. (a) Left fusiform gyrus; (b) Right fusiform gyrus; (c) Left lingual gyrus; (d) Left putamen; (e) Right cerebellum.
Figure 6
Figure 6
Beliefs task: brain responses during Reappraise versus React in SAD and HC. (a) Differential responses in patients with SAD versus healthy controls (HC > SAD). 1 = left superior temporal gyrus. (b) Common BOLD responses in patients with SAD and healthy controls. 1 = dorsomedial PFC. Statistical threshold for BOLD responses: t-value threshold ≥2.93, voxel P <0.005, minimum cluster volume threshold ≥244 mm3 (6 voxels × 3.438 mm3), cluster-wise P <0.01.
Figure 7
Figure 7
Beliefs task: temporal dynamics of the left STG BOLD responses during Reappraise versus React in SAD and HC. Asterisks represent a significant between-group difference in the average of the last three time points (late) BOLD responses.
Figure 8
Figure 8
Dorsomedial PFC BOLD responses during the three socio-emotional tasks. The dorsomedial PFC (DMPFC) showed increased activity in both patients with SAD and HC, during reappraisal of faces, criticism, and beliefs.
Figure 9
Figure 9
Temporal dynamics of the dorsomedial PFC BOLD responses during Reappraise versus React Faces (a), Criticism (b), and Beliefs (c) in SAD and HC. No significant between-group differences were found in early or late DMPFC activity when reappraising faces and criticism. A significant between-group difference was found in late DMPFC activity when reappraising beliefs (P <0.04).
Figure 10
Figure 10
Beliefs task: association between dorsomedial PFC BOLD responses during Reappraise versus React and percent reduction in negative emotion ratings. When reappraising beliefs, DMPFC BOLD responses were positively correlated with % reduction in negative emotion ratings in SAD patients (r = 0.42, P <0.04).

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