Neural activity to positive expressions predicts daily experience of schizophrenia-spectrum symptoms in adults with high social anhedonia

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1 1 Neural activity to positive expressions predicts daily experience of schizophrenia-spectrum symptoms in adults with high social anhedonia Christine I. Hooker, Taylor L. Benson, Anett Gyurak, Hong Yin, Laura M. Tully, Sarah Hope Lincoln Harvard University Methods fmri Task and Stimuli Supplemental Materials The Mind Reading Library is a commercially available CD developed by Simon Baron- Cohen (2003) has 408 short videos expressing a range of emotions including basic emotions (e.g. happy, angry) as well as complex and social emotions (e.g. jealous, loving). The developers provide verbal labels for each emotion based on consensus ratings. Because the aim of this study is to measure emotion regulation specifically, the regulation of positive feelings from a social encounter, the priority was to choose facial expression videos that elicited feelings of social acceptance, rejection (or neutrality). Research staff viewed all facial expression videos and selected videos that could be broadly categorized as interpersonally accepting (e.g. loving, caring, accepting, empathic, encouraging), interpersonally rejecting (e.g. contemptuous, annoyed, disgusted, angry), and neutral. The Mind Reading Library did not label any videos as neutral, per se, but expressions with low valence and low intensity were chosen. (Labels included calm, relaxed, composed, blank, and indifferent). Selection of the final stimuli considered whether the expressions fit the designated category (accepting, rejecting or neutral), whether they were realistic (e.g. had appropriate intensity), and whether face identity and gender (of the actors) could be balanced across conditions. The final selection included facial expression

2 2 videos from 10 different actors (5 females, 5 males). Each actor appears an equal number of times in each condition (accepting, rejecting, and neutral). All videos were edited to 3 seconds each. To verify that the facial expression videos elicited the target emotions, all facial expression stimuli that were used in the task were rated by an independent group of participants (N= 29) recruited from the Psychology Department study pool at Harvard University. The participants answered three questions about each facial expression video: 1) How accepted or rejected do you feel?; 2) How realistic is the expression?; 3) How does it affect your attention level? Mean(SD) [range] and paired t-tests are reported below. Results show that the facial expression stimuli elicited the target feelings. Accepted/Rejected ratings were on a 5 point scale (1=Highly Rejected; 3= Neutral; 5=Highly Accepted). As expected, participants reported that they felt accepted when viewing Positive expressions (4.27(0.38) [ ]), rejected when viewing Negative expressions (1.91(0.44) [ ]), and neutral when viewing Neutral expressions (3.02(0.25) [ ]) Positive, Negative, and Neutral expressions were significantly different from each other in the expected directions [Positive vs. Neutral: t= 17.52, p<.001); Negative vs. Neutral: t= 12.37, p<.001); Positive vs. Negative, t= 17.78, p<.001), and ratings for Positive and Negative expressions deviated from neutral ratings an equal amount i.e. there was no difference in how intensely participants felt accepted when viewing Positive expressions and rejected when viewing Negative expressions. In addition, participants rated the Positive, Negative, and Neutral facial expressions as moderately to extremely realistic (5 point scale: 1 = Not at all; 3=Moderately; 5= Extremely).

3 3 These ratings provide additional confidence about the validity of the task. Realism ratings: Positive: 4.22(0.52) [ ]; Negative: 3.86(0.54) [ ]; Neutral: 4.26(0.55) [ ]. Positive expressions and Neutral expressions were equally realistic (t= 0.41, p =0.68), and Negative faces were rated as slightly less realistic than both Positive (t= 4.90, p <.001), and Neutral expressions (t= 4.62, p <.001). We also wanted to ensure that the Positive and Negative expressions were intense enough to elicit emotional response and that the emotional intensity of both Positive and Negative expressions were significantly greater than Neutral expressions. Intensity was measured as the degree of arousal elicited when viewing each face. Anchors were taken from commonly used likert scales for emotional stimuli (Scale: 1= sleepy/sluggish; 5=alert/stimulated). As expected both Positive and Negative expressions were rated as more alerting and stimulating than Neutral expressions [Neutral: 2.96(0.57) [ ]; Positive: 3.92(0.60) [ ], t= 10.24, p<.001; Negative: 3.53(0.59) [ ], t= 4.76, p<.001]. Positive expressions were also more alerting and stimulating then Negative expressions (t=2.70, p<.05).

4 4 fmri Activity for Main Contrasts in Each Group One sample t-tests were conducted in each group to show task related activity. Statistical threshold was t(14)= 3.79, p<.001 with cluster extent of 5 voxels. As expected, regions for both emotion processing and face processing were significantly active for Positive>Neutral Expressions and Negative > Neutral expressions, including the superior temporal cortex, fusiform gyrus, amygdala, and anterior cingulate cortex. Regions for reward processing were significantly more active for Positive> Negative, including the orbital frontal cortex, ventral medial prefrontal cortex, and caudate. Both groups had similar activity patterns for the main contrasts. The findings verify that the primary conditions activated the appropriate emotion and face processing networks. Supplemental Table 1. Brain regions for Low SA. Anatomical Region R/L BA volume in voxels/mm 3 MNI Coordinates x, y, z T value β Low Social Anhedonia Positive > Neutral Middle Occipital Gyrus R / Inferior temporal gyrus R Fusiform gyrus R Superior temporal gyrus% R Middle Occipital Gyrus L / Superior occipital gyrus L Middle occipital gyrus L Fusiform gyrus L /

5 Middle occipital gyrus L 18 - Middle temporal gyrus L Superior temporal gyrus# L Superior temporal sulcus# L Insula (anterior) R 48 18/ Amygdala- Hippocampal Complex R 20 50/ Amygdala-Hippocampal Complex L / Hippocampus - Posterior L Amygdala L Anterior cingulate cortex R 24 11/ Superior temporal sulcus - anterior L 22 72/ Precentral gyrus R 6 8/ Posterior hippocampus R 27 26/ Thalamus R n/a Posterior hippocampus R Anterior cingulate cortex L 24,32 18/

6 6 Middle cingulate cortex L 23 36/ Superior temporal gyrus R 22 23/ Temporal pole L 21, 38 6/ Negative > Neutral Middle temporal gyrus R / Middle temporal sulcus R Superior temporal gyrus R Superior temporal sulcus# R Inferior occipital gyrus/fusiform gyrus L / Middle occipital gyrus L Middle temporal sulcus L Superior temporal sulcus# L Thalamus (posterior) R n/a 35/ Thalamus (posterior) L Precentral gyrus R 6 15/ Superior occipital gyrus L 17 24/ Amygdala R 34 40/

7 7 Hippocampus L 20 36/ Amygdala L Superior temporal sulcus R 18/ Lingual gyrus L 18 6/ Fusiform L 37 20/ Middle occipital gyrus R 19 7/ Positive > Negative Superior occipital gyrus R / Lingual gyrus R Fusiform gyrus R Superior frontal gyrus L 9 38/ Middle occipital gyrus L 18 52/ Middle occipital gyrus L Anterior cingulate cortex L 10, / Anterior orbital gyrus L Anterior cingulated cortex L Caudate (Head) L 25 12/

8 8 Anterior cingulate cortex R 10, 32 25/ Anterior cingulate cortex R Superior frontal gyrus medial portion R 10 7/ Superior frontal gyrus medial portion R Negative > Positive No significant findings Dash (-) in the volume column indicates that the region is included in the cluster listed above % Threshold was raised to p<.00001, t(14) = 6.29 so that peaks of STS would be separated from large occiptal/temporal cluster # Included in middle occipital gyrus cluster.

9 9 Supplemental Table 2. Brain regions for High SA. Anatomical Region R/L BA volume in voxels/mm 3 MNI Coordinates x, y, z T value β High Social Anhedonia Positive > Neutral Middle occipital gyrus R / Middle temporal gyrus R Middle occipital gyrus R (Cluster extends to and includes entire STS) - Superior temporal sulcus posterior % R 22, Superior temporal sulcus (middle) % R Superior temporal sulcus anterior % R Middle occipital gyrus L / Middle occipital gyrus L Inferior occipital gyrus L Superior temporal gyrus % L Superior temporal sulcus posterior % L Thalamus (pulvinar) R n/a 35/

10 10 Temporal pole L 38 21/ Temporal pole L Amygdala L 34 47/ Amygdala L Amygdala/parahippocampal gyrus L Middle temporal gyrus - anterior L / Superior temporal sulcus - anterior L Superior temporal sulcus anterior L Fusiform gyrus L 37 49/ Fusiform gyrus L Precuneus/posterior cingulate R/L 23,26 38/ Gyrus rectus L 11 19/ Gyrus rectus R 11 10/ Thalamus (pulvinar) L n/a 5/ Negative > Neutral Superior temporal sulcus R / Middle temporal gyrus R

11 11 Superior temporal gyrus R Middle occipital gyrus L / Middle temporal gyrus L Middle temporal gyrus L Superior temporal sulcus # L Fusiform R 37 25/ Amygdala L 34 6/ Middle occipital gyrus L 18 12/ Superior temporal sulcus L 20 11/ Inferior frontal gyrus triangularis R 45 5/ Positive >Negative Cuneus/Superior occipital gyrus R 18 65/ Middle temporal gyrus (anterior) L 21 11/ Precuneus R 23 7/ Negative > Positive Postcentral gyrus R 43 27/ Central sulcus R 4 13/

12 Dash (-) in the volume column indicates that the region is included in the cluster listed above % Threshold was raised to p<.00001, t(14) = 6.29 so that peaks of STS would be separated from large occiptal/temporal cluster # Included in middle occipital gyrus cluster.

13 13 Reliability Analyses Supplemental Table 3. Test-retest reliability was examined by correlating diary ratings for the first half and second half of the diary (i.e. days 1 11 and days 12 21). Pearson correlations listed in table. Diary Variable All Participants High Social Anhedonia Low Social Anhedonia Cognition 0.92** 0.94** 0.87** Paranoia 0.89** 0.87** 0.63* Odd Experiences 0.92** 0.92** -- Motivation/Productivity 0.82** 0.77** 0.81** Vigor/Positive Affect 0.94** 0.95** 0.88** Negative Mood 0.50** 0.62* 0.38 Conflict y/n 0.72** 0.74** 0.72** Conflict Distress 0.58** 0.54* 0.78** ** p<.001, *p< n/a; no variance

14 Supplemental Table 4. Average daily-diary ratings of schizophrenia-spectrum symptoms were correlated with standard measures of schizotypy and trait affect to investigate construct validity. Daily-diary variables are underlined in bold italics. Relevant correlations are shown in bold. ** p<.001, *p<.05, ^ p<.10 (trend). All Participants High Social Anhedonia Low Social Anhedonia Paranoia Correlated with Standard Measures of Schizotypy SPQ: Cognitive-Perceptual SPQ: Interpersonal 0.63** SPQ: Disorganized 0.59** SPQ: Suspiciousness Subscale 0.48** Referential Thinking 0.46* Magical Ideation 0.53** Perceptual Aberration 0.46* Hallucinations/Odd Experiences Correlated with Standard Measures of Schizotypy SPQ: Cognitive-Perceptual 0.58 ** 0.51* 0.10 SPQ: Interpersonal SPQ: Disorganized 0.46 ** Referential Thinking 0.42 * Magical Ideation 0.63 ** 0.64* Perceptual Aberration 0.46 * 0.45^ Productivity Correlated with Standard Measures of Schizotypy & Trait Affect SPQ: Cognitive-Perceptual * SPQ: Interpersonal -.46 * * SPQ: Disorganized -.52 ** Referential Thinking Magical Ideation -.38 * Perceptual Aberration BFI: Extraversion.56 ** ** BFI: Neuroticism -.55 ** Vigor/Positive Affect Correlated with Standard Measures of Schizotypy & Trait Affect SPQ: Cognitive-Perceptual * SPQ: Interpersonal -.54 ** SPQ: Disorganized -.48 ** Referential Thinking Magical Ideation Perceptual Aberration Big Five Inventory: Extraversion.61 ** ** Big Five Inventory: Neuroticism -.50 ** Negative Affect Correlated with Standard Measures of Trait Affect Big Five Inventory: Extraversion Big Five Inventory: Neuroticism 0.31^

15 Supplemental Table 5. Results of follow-up, simple slopes analyses for schizophrenia-spectrum symptoms predicted by the interaction of SA, VLPFC activity to positive>neutral expressions, and conflict distress. Significant findings are shown with p values in bold type. 15 Effect of VLPFC activity for Effect of VLPFC activity for Effect of VLPFC activity for Effect of VLPFC activity for high SA people on days of high high SA people on days of low low SA people on days of high low SA people on days of low conflict distress conflict distress conflict distress conflict distress b (S.E.) t p b (S.E.) t p b (S.E.) t p b (S.E.) t p Paranoia (0.41) (0.31) (0.39) (0.30) Effect of conflict distress for Effect of conflict distress for Effect of conflict distress for Effect of conflict distress for high SA people with low high SA people with high low SA people with low low SA people with high VLPFC activity VLPFC activity VLPFC activity VLPFC activity Paranoia 0.12 (0.02) (0.05) (0.05) (0.02) Effect of SA for people with Effect of SA for people with Effect of SA for people with Effect of SA for people with low VLPFC activity on days of high VLPFC activity on days of low VLPFC activity on days of high VLPFC activity on days of high conflict distress high conflict distress low conflict distress low conflict distress Paranoia 0.03 (0.01) (0.01) (0.01) (0.01)

Title of file for HTML: Supplementary Information Description: Supplementary Figures, Supplementary Tables and Supplementary References

Title of file for HTML: Supplementary Information Description: Supplementary Figures, Supplementary Tables and Supplementary References Supplementary Information Supplementary Figure 1. The mean parameter