Neural Correlates of Affective Benefit From Real-life Social Contact and Implications for Psychiatric Resilience

Gabriela Gan; Ren Ma; Markus Reichert; Marco Giurgiu; Ulrich W Ebner-Priemer; Andreas Meyer-Lindenberg; Heike Tost

doi:10.1001/jamapsychiatry.2021.0560

. 2021 May 5;78(7):790–792. doi: 10.1001/jamapsychiatry.2021.0560

Neural Correlates of Affective Benefit From Real-life Social Contact and Implications for Psychiatric Resilience

Gabriela Gan ^1,^✉, Ren Ma ¹, Markus Reichert ^1,^2,³, Marco Giurgiu ^1,², Ulrich W Ebner-Priemer ^1,², Andreas Meyer-Lindenberg ¹, Heike Tost ¹

¹Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany

²Mental mHealth Lab, Chair of Applied Psychology, Institute of Sports and Sports Science, Karlsruhe Institute of Technology (KIT), Karlsruhe, Germany

³Department of eHealth and Sports Analytics, Ruhr-University Bochum, Bochum, Germany

^✉

Corresponding Author: Gabriela Gan, PhD, Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, J5, 68159 Mannheim, Germany (gabriela.gan@zi-mannheim.de).

Accepted for Publication: March 2, 2021.

Published Online: May 5, 2021. doi:10.1001/jamapsychiatry.2021.0560

Author Contributions: Drs Gan and Tost had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Dr Gan and Mr Ma contributed equally to the study. Drs Meyer-Lindenberg and Tost were co–senior authors.

Concept and design: Reichert, Ebner-Priemer, Meyer-Lindenberg, Tost.

Acquisition, analysis, or interpretation of data: Gan, Ma, Reichert, Giurgiu, Ebner-Priemer, Tost.

Drafting of the manuscript: Gan, Ma, Reichert, Meyer-Lindenberg, Tost.

Critical revision of the manuscript for important intellectual content: Gan, Ma, Giurgiu, Ebner-Priemer, Meyer-Lindenberg, Tost.

Statistical analysis: Gan, Ma, Reichert, Giurgiu, Ebner-Priemer, Tost.

Obtained funding: Meyer-Lindenberg, Tost.

Administrative, technical, or material support: Gan, Giurgiu, Meyer-Lindenberg, Tost.

Supervision: Ebner-Priemer, Meyer-Lindenberg, Tost.

Conflict of Interest Disclosures: Dr Gan reports grants from Heidelberg University (Olympia-Morata Program) and German Academic Exchange Service during the conduct of the study. Mr Ma acknowledges support of the Chinese Scholarship Council. Dr Ebner-Priemer reports personal fees from Boehringer Ingelheim for consulting outside the submitted work. Dr Meyer-Lindenberg reports personal fees from Agence Nationale de la Recherche, American Association for the Advancement of Science, Brain Mind Institute, Brainsway, Catania International Summer School of Neuroscience, Daimler und Benz Stiftung, Elsevier, Fondation FondaMental, Janssen-Cilag GmbH, Lundbeck A/S, Lundbeck International Neuroscience Foundation, MedinCell, Sage Therapeutics, Techspert.io, The LOOP Zürich, Thieme Verlag, von Behring Röntgen Stiftung, BAG Psychiatrie Oberbayern, Biotest AG, Forum Werkstatt Karlsruhe, International Society of Psychiatric Genetics (Brentwood), Klinik für Psychiatrie und Psychotherapie Ingolstadt, Lundbeck SAS France, med update GmbH, Merz-Stiftung, and Siemens Healthineers outside the submitted work. No other disclosures were reported.

Funding/Support: Dr Tost acknowledges grant support by the German Research Foundation (GRK 2350 project B2, Collaborative Research Center TRR 265 project A04, Collaborative Research Center SFB 1158 project B04, grant TO 539/3-1) and German Federal Ministry of Education and Research (grant 01EF1803A project WP3, grant 01GQ1102). Dr Meyer-Lindenberg acknowledges grant support by the German Research Foundation (Collaborative Research Center SFB 1158 project B09, Collaborative Research Center TRR 265 project S02, grant ME 1591/4-1), German Federal Ministry of Education and Research (grants 01EF1803A, 01ZX1314G and 01GQ1003B), European Union’s Seventh Framework Programme (grants 602450, 602805, 115300, and HEALTH-F2-2010-241909), Innovative Medicines Initiative Joint Undertaking (grants 115008 and 777394), Ministry of Science, Research and the Arts of the State of Baden-Wuerttemberg, Germany (grant 42-04HV.MED[16]/16/1), Hector Foundation, Klaus-Tschira-Stiftung, and Prix Roger des Spoelberch. Dr Ebner-Priemer acknowledges grant support by the German Research Foundation (Collaborative Research Center TRR 265 project A04, S02).

Role of the Funder/Sponsor: The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Additional Contributions: We thank Oksana Berhe, MSc; Urs Braun, MD; Kristina Schwarz, MSc; Iris Reinhard, PhD; Tracie Ebalu, BSc; Carolin Mößnang, PhD; Ceren Akdeniz, PhD; Andreas Hoell, PhD; Beate Höchemer, MA; Claudia Stief, MTRA, and our student assistants, all Central Institute of Mental Health, Mannheim, Germany, who provided valuable assistance during data collection and/or analysis. We further thank all individuals who contributed their time and effort to participate in this study. No compensation was received.

^✉

Corresponding author.

PMCID: PMC8100908 PMID: 33950218

Abstract

This cohort study examines the association of daily-life social affective benefit with brain structure and psychiatric risk and resilience measures in 2 independent community-based samples.

Social embedding and social support are critical for mental health protection. Here, we study increases in affective well-being in naturalistic social contexts,¹ a concept that we call social affective benefit (SAB). Unlike traditional inventory-based measures, which quantify differences between study participants, SAB reflects within-person social affective reactivity by quantifying the degree to which momentary affective valence increases with momentary social contact in real-life ambulatory assessments^1,2 (eMethods in the Supplement). Despite its relevance for mental health, the fundamental human experience of SAB is underresearched and its neural basis is unknown. We quantified daily-life SAB in 2 independent community-based samples and assessed its association with brain structure and psychiatric risk and resilience measures. At the brain level, we assessed associations between SAB and gray matter volume (GMV) in the anterior cingulate cortex (ACC) given the roles of dorsal and perigenual ACC in social affective reactivity³ and social environmental risk and resilience.^4,5

Methods

Participants provided written informed consent for a study protocol approved by the institutional review board of Heidelberg University. In this community-based cohort study, healthy young adults reported on daily-life social contact and affective valence (eFigure in the Supplement) across 1 week using smartphone-based electronic diaries and completed social and psychological inventories (eMethods in the Supplement) from September 2014 to November 2018. The replication sample additionally underwent 3-T structural magnetic resonance imaging. We predicted affective valence (ie, outcome measure) with social contact (alone vs in company, predictor) using random-intercept random-slope multilevel models with time of day, time of day squared (level 1), sex, and age (level 2) as covariates using SAS version 9.4 (SAS Institute). In this model, individual SAB was reflected by the random association between social contact and affective valence (ie, the person-specific deviation from the fixed group effect; eMethods in the Supplement). We computed regression or correlation analyses (eMethods in the Supplement) for associations of SAB with voxelwise ACC GMV (estimated with voxel-based morphometry using the Computational Anatomy Toolbox implemented in SPM 12 [Statistical Parametric Mapping, The Wellcome Centre for Humang Neuroimaging]; covariates: sex, age, total intracranial volume) and social psychological risk and resilience factors (derived from inventory measures by principal component analysis using SPSS statistical software, version 22.0 [IBM]). All analyses were corrected for multiple comparisons (significance thresholds: multilevel modeling, 2-sided P < .025; voxelwise multiple regression analysis, 1-sided P < .025 within region of interest; correlation analyses, 2-sided P < .0083). Analysis began May 2019 and ended December 2020.

Results

Overall, 277 participants (discovery sample: n = 100; replication sample: n = 177; eMethods in the Supplement) answered a mean (SD) of 10.2 (2.2) e-diary prompts per day. Real-life social contact was significantly associated with increased affective valence within individuals in both the discovery and replication sample (Table and Figure, A). SPM 12 regression modeling revealed that higher individual daily-life SAB was significantly associated with higher GMV in a cluster mapping to the transition area of dorsal and perigenual ACC (Figure, B; peak voxel [MNI space]: x = 3, y = 33, z = 26; t = 3.92; 1-sided peak voxel familywise error–corrected P = .02 within a bilateral ACC mask). No other brain area outside of the ACC showed significant associations with SAB. Moreover, individual daily-life SAB, but not ACC GMV, was correlated with social competence factor scores (2-sided Spearman r = 0.253; P = .001; Figure, C) capturing the variance of social resilience measures (eMethods in the Supplement). SAB and ACC GMV did not correlate with other principal component analysis factors (ie, psychological risk [Spearman r = −0.180; P = .16], other coping [Spearman r = −0.016; P = .84]).

Table. Random-Intercept Random-Slope Multilevel Modeling of Social Affective Benefit in the Discovery and Replication Samples^a.

Fixed effects^b	Discovery sample (n = 100)^c			Replication sample (n = 177)^d
Fixed effects^b	β coefficient (SE)	t (df)	P value^e	β coefficient (SE)	t (df)	P value^e
Intercept	71.012 (7.877)	9.01 (97)	<.001	67.487 (7.473)	9.03 (174)	<.001
Level 1 predictors
Social contact, in company	2.554 (0.578)	4.42 (89)	<.001	2.596 (0.416)	6.25 (168)	<.001
Time, h	0.525 (0.165)	3.18 (3033)	.002	0.645 (0.118)	5.49 (5012)	<.001
Time², h	−0.019 (0.010)	−1.86 (6965)	.06	−0.020 (0.007)	−2.85 (12393)	.004
Level 2 predictors
Age, y	−0.168 (0.335)	−0.50 (96)	.62	−0.040 (0.319)	−0.12 (172)	.90
Female	2.751 (2.305)	1.19 (97)	.24	2.097 (1.754)	1.20 (172)	.23
Random effects	Variance estimate (SE)	Wald z	P value	Variance estimate (SE)	Wald z	P value
Intercept	92.39 (15.270)	6.05	<.001	120.87 (14.417)	8.38	<.001
Social contact	8.67 (2.434)	3.56	<.001	8.71 (1.646)	5.29	<.001
Time, h	0.206 (0.054)	3.81	<.001	0.22 (0.038)	5.74	<.001

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^{^a}

We conducted multilevel analysis and estimated within-person associations in a random-intercept random-slope model (e-diary assessments nested within participants; the multilevel modeling approach is described in detail in the eMethods in the Supplement.)

^{^b}

Besides the main predictor social contact, level 1 predictors included time of day and time of day squared (transformed to the daily study start time: 7:30 am), and level 2 predictors included sex and age (see the eMethods in the Supplement for full model equation). Nonsignificant random effects were deleted from the model (eg, for time²).

^{^c}

Of 100 individuals, 72 (72%) were female and 28 (28%) were male.

^{^d}

Of 177 individuals, 81 (46%) were female and 96 (54%) were male.

^{^e}

P values for the β coefficient are 2-sided and derived from the t statistics of the multilevel model.

Figure. — A, Individual and group SAB shown for discovery (left) and replication (right) samples. Gray (positive SAB) and orange (negative SAB) lines depict the degree to which each participant’s affective valence (y-axis) changed with being in company vs being alone (x-axis). Blue lines represent the respective fixed group associations. B, Brain map showing the association between individual SAB and ACC gray matter volume in the replication sample (familywise error–corrected P = .02, region of interest–corrected within the ACC), displayed at a threshold of P < .005 uncorrected across the whole brain for illustration purposes. The scatterplot displays the positive association between individual SAB and mean relative ACC gray matter volume across k = 128 voxels surviving peak-voxel region of interest correction within the ACC mask (significance threshold: familywise error–corrected P < .05). C, The scatterplot displays the positive association between SAB and social competence factor scores (Spearman r = 0.253, P = .001). AU indicates arbitrary unit; VAS, visual analog scale.

Discussion

The findings show higher affective well-being during real-life social contact that was associated with social resilience measures such as coping by seeking social support. At the brain level, these data implicate the transition area between dorsal and perigenual ACC in this fundamental daily-life resilience-related behavior. These subregions receive overlapping cortical projections, are strongly interconnected, and have been consistently related to core social functions (eg, social affective reactivity, reciprocal interaction, social environmental risk/resilience).^3,4,5,6 Thus, we speculate that ACC structural integrity may be associated with daily-life SAB.

However, study limitations including our cross-sectional design limit inferences associated with the directionality of associations. Further experiments are needed to disentangle the causal mechanisms underlying the interplay between ACC structural integrity, mood, and social contact. Specifically, mobile health experiments could clarify the relationship between social contact and affective well-being and pave the way for mobile health interventions mitigating daily-life social symptoms in vulnerable populations.

Supplement.

eFigure. e-Diary items (for illustrative purposes shown on a single screen) and location tracking for an exemplary study day

eMethods

eReferences

Click here for additional data file.^{(308.8KB, pdf)}

References

1.Oorschot M, Lataster T, Thewissen V, et al. Emotional experience in negative symptoms of schizophrenia—no evidence for a generalized hedonic deficit. Schizophr Bull. 2013;39(1):217-225. doi: 10.1093/schbul/sbr137 [DOI] [PMC free article] [PubMed] [Google Scholar]
2.Brown LH, Silvia PJ, Myin-Germeys I, Kwapil TR. When the need to belong goes wrong: the expression of social anhedonia and social anxiety in daily life. Psychol Sci. 2007;18(9):778-782. doi: 10.1111/j.1467-9280.2007.01978.x [DOI] [PubMed] [Google Scholar]
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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplement.

eFigure. e-Diary items (for illustrative purposes shown on a single screen) and location tracking for an exemplary study day

eMethods

eReferences

Click here for additional data file.^{(308.8KB, pdf)}

[yld210002r1] 1.Oorschot M, Lataster T, Thewissen V, et al. Emotional experience in negative symptoms of schizophrenia—no evidence for a generalized hedonic deficit. Schizophr Bull. 2013;39(1):217-225. doi: 10.1093/schbul/sbr137 [DOI] [PMC free article] [PubMed] [Google Scholar]

[yld210002r2] 2.Brown LH, Silvia PJ, Myin-Germeys I, Kwapil TR. When the need to belong goes wrong: the expression of social anhedonia and social anxiety in daily life. Psychol Sci. 2007;18(9):778-782. doi: 10.1111/j.1467-9280.2007.01978.x [DOI] [PubMed] [Google Scholar]

[yld210002r3] 3.Eisenberger NI. The pain of social disconnection: examining the shared neural underpinnings of physical and social pain. Nat Rev Neurosci. 2012;13(6):421-434. doi: 10.1038/nrn3231 [DOI] [PubMed] [Google Scholar]

[yld210002r4] 4.Meyer-Lindenberg A, Tost H. Neural mechanisms of social risk for psychiatric disorders. Nat Neurosci. 2012;15(5):663-668. doi: 10.1038/nn.3083 [DOI] [PubMed] [Google Scholar]

[yld210002r5] 5.Akdeniz C, Tost H, Streit F, et al. Neuroimaging evidence for a role of neural social stress processing in ethnic minority-associated environmental risk. JAMA Psychiatry. 2014;71(6):672-680. doi: 10.1001/jamapsychiatry.2014.35 [DOI] [PubMed] [Google Scholar]

[yld210002r6] 6.Margulies DS, Kelly AM, Uddin LQ, Biswal BB, Castellanos FX, Milham MP. Mapping the functional connectivity of anterior cingulate cortex. Neuroimage. 2007;37(2):579-588. doi: 10.1016/j.neuroimage.2007.05.019 [DOI] [PubMed] [Google Scholar]

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Neural Correlates of Affective Benefit From Real-life Social Contact and Implications for Psychiatric Resilience

Gabriela Gan, PhD

Ren Ma, MSc

Markus Reichert, PhD

Marco Giurgiu, PhD

Ulrich W Ebner-Priemer, PhD

Andreas Meyer-Lindenberg, MD

Heike Tost, MD, PhD

Abstract

Methods

Results

Table. Random-Intercept Random-Slope Multilevel Modeling of Social Affective Benefit in the Discovery and Replication Samples^a.

Figure. Association Between Individual Social Affective Benefit (SAB), Anterior Cingulate Cortex (ACC) Gray Matter Volume, and Social Resilience.

Discussion

References

Associated Data

Supplementary Materials

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PERMALINK

Neural Correlates of Affective Benefit From Real-life Social Contact and Implications for Psychiatric Resilience

Gabriela Gan, PhD

Ren Ma, MSc

Markus Reichert, PhD

Marco Giurgiu, PhD

Ulrich W Ebner-Priemer, PhD

Andreas Meyer-Lindenberg, MD

Heike Tost, MD, PhD

Abstract

Methods

Results

Table. Random-Intercept Random-Slope Multilevel Modeling of Social Affective Benefit in the Discovery and Replication Samplesa.

Figure. Association Between Individual Social Affective Benefit (SAB), Anterior Cingulate Cortex (ACC) Gray Matter Volume, and Social Resilience.

Discussion

References

Associated Data

Supplementary Materials

ACTIONS

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RESOURCES

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Table. Random-Intercept Random-Slope Multilevel Modeling of Social Affective Benefit in the Discovery and Replication Samples^a.