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. 2023 Jul 3:12:e84072.
doi: 10.7554/eLife.84072.

Brain and molecular mechanisms underlying the nonlinear association between close friendships, mental health, and cognition in children

Chun Shen #  1   2   3 , Edmund T Rolls #  1   4   5 , Shitong Xiang  1   2 , Christelle Langley  6   7 , Barbara J Sahakian  1   6   7 , Wei Cheng  1   2   8   9   10 , Jianfeng Feng  1   2   3   4   8   11
Affiliations

Brain and molecular mechanisms underlying the nonlinear association between close friendships, mental health, and cognition in children

Chun Shen et al. Elife. .

Abstract

Close friendships are important for mental health and cognition in late childhood. However, whether the more close friends the better, and the underlying neurobiological mechanisms are unknown. Using the Adolescent Brain Cognitive Developmental study, we identified nonlinear associations between the number of close friends, mental health, cognition, and brain structure. Although few close friends were associated with poor mental health, low cognitive functions, and small areas of the social brain (e.g., the orbitofrontal cortex, the anterior cingulate cortex, the anterior insula, and the temporoparietal junction), increasing the number of close friends beyond a level (around 5) was no longer associated with better mental health and larger cortical areas, and was even related to lower cognition. In children having no more than five close friends, the cortical areas related to the number of close friends revealed correlations with the density of μ-opioid receptors and the expression of OPRM1 and OPRK1 genes, and could partly mediate the association between the number of close friends, attention-deficit/hyperactivity disorder (ADHD) symptoms, and crystalized intelligence. Longitudinal analyses showed that both too few and too many close friends at baseline were associated with more ADHD symptoms and lower crystalized intelligence 2 y later. Additionally, we found that friendship network size was nonlinearly associated with well-being and academic performance in an independent social network dataset of middle-school students. These findings challenge the traditional idea of 'the more, the better,' and provide insights into potential brain and molecular mechanisms.

Keywords: cognition; friendships; human; mental health; neuroscience; social brain.

Plain language summary

Close friendships are crucial during the transition from late childhood to adolescence as children become more independent from their parents and influenced by their peers. The brain undergoes a tremendous amount of development during this period, and it is also a time when mental health disorders often begin to emerge. Scientists are still learning about how friendships shape brain development and mental health during this transition. Maintaining friendships takes time and mental resources so there may be limits on how many friends are beneficial. Here, Shen, Rolls et al. show that the having more friends is not always directly related to better mental health and cognitive abilities. In the study, Shen, Rolls et al. analyzed data from nearly 7,500 young people between around 10 to 12 years old: this included, their number of close friends, their mental health and cognitive abilities such as working memory, attention and processing speed, and images of their brains. Data from a second set of about 16,000 young people were then analyzed to confirm the results. Shen, Rolls et al. found having a higher number of close friends was associated with improved mental health and cognitive ability. However, this association stopped once around five friends had been reached, after which having more friends was no longer linked to better mental health and was even correlated with lower cognition. Additionally, individuals with too few or too many friends had more symptoms of Attention-deficit/hyperactivity disorder (ADHD) and were less able to learn from their experiences. This non-linear relationship between number of friends and mental health and cognitive abilities can be partly explained by the structure of the brain. Shen, Rolls et al. found that brain regions associated with friendship were larger in individuals with more close friends, but did not increase any further once the number of friends a person had exceeded five individuals with around five close friends also had more of a receptor that is part of the opioid system, which may make them more responsive to laughter, friendly touch, or other positive social interactions. These findings challenge the idea that having more friends is always better. It also provides insights into how friendships affect brain health during the transition from late childhood to adolescence. Insights from this study may aid the development of interventions to support healthy brain development during youth.

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Conflict of interest statement

CS, ER, SX, CL, BS, WC, JF No competing interests declared

Figures

Figure 1.
Figure 1.. The study workflow.
(a) Study datasets and key measures used in the present study. (b) A two-step approach to evaluate the nonlinear association. The number of close friends is used as the independent variable in quadratic regression models. Once a significant squared term (‘b’) is found, a two-lines test is conducted to estimate the breakpoint. Then participants are classified into two groups according to the breakpoint. (c) Correlation of brain differences related to the number of close friends with neurotransmitter density and gene expression level. (d) Longitudinal and mediation analysis of the number of close friends, ADHD symptoms, crystalized intelligence, and the significant surface areas.
Figure 2.
Figure 2.. Results of behavior-level nonlinear association analyses in the Adolescent Brain Cognitive Developmental (ABCD) study at baseline.
(a) Results of quadratic regression models. The total F values of quadratic and linear terms, and the t values of linear and quadratic terms are reported. An asterisk indicates statistical significance after Bonferroni correction (i.e., p<0.05/30 for F value, and p<0.05/60 for t value). Relationship between the number of close friends and the total problems (b), attention problems (c), withdrawn/depressed (d), social problems (e), fluid intelligence (f), and crystalized intelligence (g). The number of close friends is classified into 13 bins, sample sizes of which are 107, 585, 1104, 1196, 957, 914, 631, 399, 463, 363, 416 and 477. In each bin, the mean (i.e., black dot) and standard error (i.e., error bar) of the dependent variable are shown. The x-axis is in log scale, and the median of the number of close friends in each bin was labeled in the x-axis. The red line is the fitted quadratic model. (h) Results of the two-lines tests. The breakpoint and the estimated coefficients with 95% confidence intervals of linear regressions in each group separated by the breakpoint are reported. cbcl-scr-syn-anxdep, Anxious/Depressed Syndrome Scale; cbcl-scr-syn-withdep, Withdrawn/Depressed Syndrome Scale; cbcl-scr-syn-somatic, Somatic Complaints Syndrome Scale; cbcl-scr-syn-social, Social Problems Syndrome Scale; cbcl-scr-syn-thought, Thought Problems Syndrome Scale; cbcl-scr-syn-attention, Attention Problems Syndrome Scale; cbcl-scr-syn-rulebreak, Rule-Breaking Behavior Syndrome Scale; cbcl-scr-syn-aggressive, Aggressive Behavior Syndrome Scale; cbcl-scr-syn-internal, Internalizing Problems Syndrome Scale; cbcl-scr-syn-external, Externalizing Problems Syndrome Scale; cbcl-scr-syn-totprob, Total Problems Syndrome Scale; cbcl-scr-dsm5-depress, Depressive Problems DSM-5 Scale; cbcl-scr-dsm5-anxdisord, Anxiety Problems DSM-5 Scale; cbcl-scr-dsm5-somaticpr, Somatic Problems DSM-5 Scale; cbcl-scr-dsm5-adhd, ADHD DSM-5 Scale; cbcl-scr-dsm5-opposite, Oppositional Defiant Problems DSM-5 Scale; cbcl-scr-dsm5-conduct, Conduct Problems DSM-5 Scale; cbcl-scr-07-sct, Sluggish Cognitive Tempo Scale2007 Scale; cbcl-scr-07-ocd, Obsessive-Compulsive Problems Scale2007 Scale; cbcl-scr-07-stress, Stress Problems Scale2007 Scale; nihtbx-picvocab, Picture Vocabulary Test; nihtbx-flanker, Flanker Inhibitory Control and Attention Test; nihtbx-list, List Sorting Working Memory Test; nihtbx-cardsort, Dimensional Change Card Sort Test; nihtbx-pattern, Pattern Comparison Processing Speed Test; nihtbx-picture, Picture Sequence Memory Test; nihtbx-reading, Oral Reading Recognition Test; nihtbx-fluidcomp, Fluid Composite Score; nihtbx-cryst, Crystallized Composite Score; nihtbx-totalcomp, Total Composite Score.
Figure 2—figure supplement 1.
Figure 2—figure supplement 1.. Effect sizes of linear and quadratic terms of close friend number in the Adolescent Brain Cognitive Developmental (ABCD) study at baseline.
Mental health and cognitive outcomes with a significant F value are shown here. The effect size of the quadratic term was calculated by the change of adjusted R2 between the quadratic model and the corresponding linear model, and the effect size of the linear term was the change of adjusted R2 between the linear model and the model with only covariates.
Figure 2—figure supplement 2.
Figure 2—figure supplement 2.. Behavior-level results of quadratic regression models by random choice of the siblings in the Adolescent Brain Cognitive Developmental (ABCD) study at baseline.
Results of quadratic regression models by randomly selecting siblings once (a) and twice (b). (c) Correlations of F values obtained by randomly selecting siblings 10 times.
Figure 2—figure supplement 3.
Figure 2—figure supplement 3.. Results of behavior-level nonlinear association analyses in the Adolescent Brain Cognitive Developmental (ABCD) study at baseline in girls and boys, respectively.
(a) Results of quadratic regression models in girls (N = 3625). (b) Results of quadratic regression models in boys (N = 3887). (c) Results of two-lines tests in girls. (d) Results of two-lines tests in boys.
Figure 2—figure supplement 4.
Figure 2—figure supplement 4.. Nonlinear association of the number of same-sex and opposite-sex close friends with mental health and cognition in the Adolescent Brain Cognitive Developmental (ABCD) study at baseline.
Results of mental health and cognitive outcomes quadratically regressed on the number of same-sex close friends (a) and opposite-sex close friends (b). (c) Effect sizes of linear and quadratic terms of same-sex close friend number. (d) Results of two-lines tests of same-sex close friend number.
Figure 2—figure supplement 5.
Figure 2—figure supplement 5.. Results of behavior-level nonlinear association analyses in the Adolescent Brain Cognitive Developmental (ABCD) study at 2-year follow-up.
(a) Results of quadratic regression models using cross-sectional 2-year follow-up data. An asterisk indicates statistical significance after Bonferroni correction (i.e., p<0.05/26 for F value, and p<0.05/52 for t value). (b) Effect sizes of linear and quadratic terms of close friend number. (c) Results of two-lines tests. The breakpoint of close friend quantity and the estimated coefficients with 95% confidence intervals of linear regressions in each group separated by the breakpoint are reported.
Figure 3.
Figure 3.. Nonlinear association between the number of close friends and cortical area in the Adolescent Brain Cognitive Developmental (ABCD) study at baseline.
(a) Cortical areas significantly associated with the number of close friends after FDR correction (i.e., 360 regions) based on the total F values of linear and quadratic terms. (b) Cortical areas with a significant linear or quadratic term. FDR correction was performed within the significant regions obtained in (a). (c) Top 10 regions with the strongest effect sizes of linear and quadratic terms, respectively. Relationship between the number of close friends and the total cortical area (d), left STGa (e), right TGd (f), left p32pr (g), left 13l (h), and left 47m (i). The number of close friends is classified into 13 bins, sample sizes of which are 107, 585, 1104, 1196, 957, 914, 631, 399, 463, 363, 416 and 377. In each bin, the mean (i.e., black dot) and standard error (i.e., error bar) of the dependent variable are shown. The x-axis is in log scale, and the median of the number of close friends in each bin was labeled in the x-axis. The red line is the fitted quadratic model. The names of the brain regions are from the HCP-MMP atlas.
Figure 3—figure supplement 1.
Figure 3—figure supplement 1.. Nonlinear association between the number of close friends and cortical areas by random choice of the siblings.
Cortical areas significantly associated with the number of close friends by randomly selecting siblings once (a) and twice (b). (c) Correlations of F values obtained by randomly selecting siblings 10 times. Pairwise Pearson correlation score ranging from 0.89 to 0.95.
Figure 3—figure supplement 2.
Figure 3—figure supplement 2.. Nonlinear association between the number of close friends and cortical volumes.
(a) Cortical volumes significantly associated with the number of close friends after FDR correction (i.e., 360 regions) based on the total F values of linear and quadratic terms. (b) Cortical volumes with a significant quadratic term. FDR correction was performed within the significant regions obtained in (a). No region with a significant linear term after FDR correction.
Figure 3—figure supplement 3.
Figure 3—figure supplement 3.. Relationship between cortical area and cortical volume.
(a) Association between the F-statistics of close friend number with cortical area and the F-statistics of close friend number with cortical volume. (b) Association between regional mean area and regional mean volume across subjects.
Figure 3—figure supplement 4.
Figure 3—figure supplement 4.. Results of two-lines tests for significant cortical areas.
The breakpoint of close friend quantity and the estimated coefficients with 95% confidence intervals of linear regressions in each group separated by the breakpoint are reported.
Figure 3—figure supplement 5.
Figure 3—figure supplement 5.. Results of linear association analyses between close friend quantity and cortical area in ≤5 and >5 groups, respectively.
(a) Unthresholded t-statistic map of cortical areas associated with the number of close friends in the ≤5 group (N = 4863). (b) Significant cortical areas associated with the number of close friends after FDR correction in the ≤5 group. (c) Effect sizes of the top 20 areas associated with the number of close friends in the ≤5 group. The effect size was calculated by the change in the overall proportion of variance (adjusted R2) between the linear model and the model with only covariates. (d) Unthresholded t-statistic map of cortical areas associated with the number of close friends in the >5 group (N = 2649). No region survived after FDR correction. (e) Association between t-statistic maps of cortical areas associated with the number of close friends in the ≤5 and >5 groups.
Figure 4.
Figure 4.. Spatial correlation between cortical area differences related to the number of close friends in children with ≤5 close friends and density of neurotransmitters and gene expression level.
(a) Bootstrapped Spearman correlations (10,000 times) between t-statistics of close friendship quantity and densities of 14 neurotransmitter receptors or transporters. In each box, the line indicates the median and the whiskers indicate the 5th and 95th percentiles. p-Values were estimated by 5000 times permutation. *: Bonferroni corrected pperm < 0.05. MOR: μ-opioid receptor. (b) The scatter map of t-statistics of close friendship quantity and the density of the μ-opioid receptor. (c) The scatter map of t-statistics of close friendship quantity and the expression level of OPRM1 gene. (d) The scatter map of t-statistics of close friendship quantity and the expression level of OPRK1 gene.
Figure 5.
Figure 5.. Results of longitudinal and mediation analysis in the Adolescent Brain Cognitive Developmental (ABCD) study.
(a) Cross-lagged panel model (CLPM) of the absolute value of close friendship quantity to 5 and ADHD symptoms (N = 6013). Comparative fit index (CFI) = 0.996, Tucker–Lewis index (TFI) = 0.97, standardized root mean squared residual (SRMR) = 0.002, root mean square error of approximation (RMSEA) = 0.015. (b) CLPM of the absolute value of close friendship quantity to 5 and crystalized intelligence (N = 6013). CFI = 0.994, TFI = 0.96, SRMR = 0.003, RMSEA = 0.025. (c) Mediation analysis of close friendship quantity, the total area of significant regions, and ADHD symptoms. (d) The effect of individual significant cortical areas that mediated the association between close friendship quantity and ADHD symptoms after FDR correction. (e) Mediation analysis of close friendship quantity, the total area of significant regions and crystalized intelligence. (f) The effect of individual significant cortical areas that mediated the association between close friendship quantity and crystalized intelligence after FDR correction.
Figure 5—figure supplement 1.
Figure 5—figure supplement 1.. Cross-lagged panel models (CLPMs) of close friend number and Adolescent Brain Cognitive Developmental (ADHD) symptoms, and crystalized intelligence in ≤5 and >5 groups, respectively.
CLPMs of close friend number and ADHD symptoms in the ≤5 group (a) and in the >5 group (b). CLPM of close friend number and crystalized intelligence in the ≤5 group (c) and in the >5 group (d).
Figure 6.
Figure 6.. Distribution of outdegree, indegree, and reciprocal degree in the social network dataset.
(a) Distribution of outdegree which is the number of outward nominations. (b) Distribution of indegree which is the number of inward nominations. (c) Distribution of reciprocal degree which is the number of reciprocal nominations. Relationship of well-being with outdegree (d), indegree (e), and reciprocal degree (f). Relationship of grade point average (GPA) with outdegree (g), indegree (h), and reciprocal degree (i). In each bin, the mean (i.e., black dot) and standard error (i.e., error bar) of the dependent variable are shown. The red line is the fitted quadratic model. For outdegree, sample sizes of bins 1-11 are 92, 87, 208, 519, 803, 1230, 1326, 1286, 1235, 1151 and 8119. For indegree, sample sizes of bins 1-14 are 617, 728, 1116, 1341, 1526, 1563, 1532, 1462, 1273, 1095, 870, 1281, 716 and 936. For reciprocal degree, sample sizes of bins 1-11 are 797, 1561, 2356, 2774, 2765, 2260, 1685, 1039, 524, 220 and 75.
Figure 6—figure supplement 1.
Figure 6—figure supplement 1.. Results of nonlinear association analysis in the social network dataset.
(a) Results of well-being quadratically regressed on outdegree, indegree, and reciprocal degree, respectively. (b) Results of grade point average (GPA) quadratically regressed on outdegree, indegree, and reciprocal degree, respectively. The total F values of quadratic and linear terms, and the t values of linear and quadratic terms are reported. An asterisk indicates statistical significance after Bonferroni correction (i.e., p<0.05/6 for F value, and p<0.05/12 for t value). (c) Effect sizes of linear and quadratic terms of social network indicators for well-being and GPA. (d) Results of two-lines tests. The breakpoint and the estimated coefficients with 95% confidence intervals of linear regressions in each group separated by the breakpoint are reported.
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