Mother-child dyadic interactions shape the developing social brain and Theory of Mind in young children
- The Clinical Hospital of Chengdu Brain Science Institute, School of Life Science and Technology, University of Electronic Science and Technology of China, China
- MOE Key Lab for Neuro information, High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, University of Electronic Science and Technology of China, China
- School of Healthcare Technology, Chengdu Neusoft University, China
- Department of Psychological and Cognitive Sciences, Tsinghua University, China
- Departments of Psychiatry & Behavioral Sciences, Neurology & Neurological Sciences, Wu Tsai Neuroscience Institute, Stanford University School of Medicine, United States
Figures
Figure 1
Overview of analysis pipeline.
(A) Reverse correlation analysis was conducted on the average response network timecourses to identify ToM and Social Pain events driving activity in Theory of Mind (ToM) and Social Pain Matrix (SPM) related brain regions. (B) First, inter-region correlations were computed across all ToM and SPM brain regions of interest for each participant. Neural maturity of a child was then assessed by averaging the similarity between the child’s correlation matrices and those of each adult. (C) Inter-subject synchronization (ISS) was determined by calculating the correlation of neural response time series between child-mother and child-stranger dyads. (D) A structural equation model was employed to explore the relationships among neurobehavioral factors of parenting and personal growth, ToM performance, and social cognition outcomes.
© 2009, Disney-Pixar. All rights reserved. Screenshots in panel A are taken from 'Partly Cloudy' (2009). These are not covered by the CC-BY 4.0 license.
Figure 2
Reverse correlation analysis.
The average timecourses of child (green) and adult (red) groups for the (A) Theory of Mind (ToM) and (B) Social Pain Matrix (SPM) networks during movie viewing are presented. Each time point along the x-axis corresponds to a single repetition time (TR) (2 s). Shaded blocks represent time points identified as ToM and Social Pain events in a reverse correlation analysis conducted on adults, while dark borders indicate time points identified as ToM and Social Pain events in children. Event labels (e.g. T01, P01) denote the ranking of average response magnitude in adults. (C) Example frames and descriptions for the five events with the highest response magnitude in adults are provided.
© 2009, Disney-Pixar. All rights reserved. Screenshots in panel C are taken from 'Partly Cloudy' (2009). These are not covered by the CC-BY 4.0 license.
Figure 3
Inter-region correlation analysis and neural maturity.
(A) Average z-scored correlation matrices were computed across all Theory of Mind (ToM) and Social Pain Matrix (SPM) regions of interest for each age group (Pre-junior: n=12; Junior: n=11; Senior: n=11; Adults: n=34). The nomenclature of brain regions is shown in Table 2. (B) Correlation between the average inter-regional correlation within ToM/SPM networks and age. (C) Correlation between neural maturity and age. (D) Correlation between neural maturity and conflict score of Child-Parent Relationship Scale (CPRS). (E) Correlation between neural maturity and age during ToM/SP and other events, as defined by reverse correlation analysis. Statistical comparisons of group differences (n = 34) were performed using two-sample t-tests. ***p<0.001. (F) Group differences in neural maturity during ToM/SP and other events for each age group (Pre-junior: n = 12; Junior: n = 11; Senior: n = 11). Statistical comparisons were conducted using two-sample t-tests. *p<0.05.
Figure 4
Inter-subject neural synchronization.
(A) Group differences (n = 34) in inter-subject synchronization (ISS) during movie viewing. Statistical comparisons were performed using two-sample t-tests. (B) Partial correlation between conflict scores of Child-Parent Relationship Scale (CPRS) and ISS within child-mother and child-stranger dyads. (C) Correlation between age and ISS within child-mother and child-stranger dyads. (D–E) Partial correlation between conflict scores on the CPRS and ISS within child-mother and child-stranger dyads during ToM/SP events and other events. Group differences (n = 34) in ISS during ToM/SP and other events are displayed on the right. Statistical comparisons were conducted using two-sample t-tests. *p<0.05.
Figure 5
Structural equation model of latent personal traits, latent parental caregiving, ToM behavior, and social development outcomes.
Parenting has a direct and indirect influence on ToM behavior which in turn influences social cognition. Latent factor underlying Personal Trait includes a child’s neural maturity, while the latent factor underlying Parenting includes child-mother inter-subject neural synchronization (ISS). Regression coefficients are displayed for each path. Solid lines indicate significant paths (*p<0.05; **p<0.01), and dashed arrows indicate nonsignificant paths.
Appendix 2—figure 1
Relationship between personal traits, neural measures and parent-child relationship quality for Theory of Mind (ToM) and Social Pain Matrix (SPM) networks analyzed separately.
(A) Correlation between neural maturity within ToM and SPM networks and age. (B) Correlation between parent-child relationship quality and inter-subject synchronization (ISS) within ToM and SPM networks in child-mother dyads. (C–D) Partial correlation between Child-Parent Relationship Scale (CPRS) conflict scores and ISS within ToM/SPM networks in child-mother dyads during ToM/Social Pain and other events, shown in red and black circles, respectively.
Appendix 2—figure 2
Structural equation modeling using (A) Theory of Mind (ToM) and (B) Social Pain Matrix (SPM) networks separately.
Solid lines indicate significant paths, and dashed arrows indicate nonsignificant paths. No significant direct effects on social cognition outcomes were observed when analyzing the networks individually, highlighting the importance of considering both networks together for predicting social cognitive outcomes.
Author response image 1
Scatterplot showing the association between parent-child inter-subject synchronization (ISS) and neural maturity, averaged across the Theory of Mind (ToM) and Social Pain Matrix (SPM) networks.
Each point represents one dyad. No significant correlation was observed between ISS and neural maturity (r = 0.2503, p = 0.1533), suggesting that interpersonal neural synchronization and individual neural maturation may reflect dissociable aspects of social brain development.
Tables
Table 1
Relationship between individual behavioral characteristics and Theory of Mind (ToM) behavior.
| Coefficient β | SE | P_Regress | R_Pearson | P_Pearson | |
|---|---|---|---|---|---|
| Receptive Vocabulary (PPVT) | 0.203 | 0.030 | 0.206 | 0.434 | 0.010 |
| Social Responsiveness (SRS Total) | –0.295 | 0.040 | 0.074 | –0.598 | <0.001 |
| Parent-Child Conflict (CPRS) | –0.191 | 0.103 | 0.189 | –0.377 | 0.028 |
| Parent-Child Closeness (CPRS) | 0.164 | 0.061 | 0.264 | 0.265 | 0.130 |
| Parental Rejection (EMBU) | 0.296 | 0.151 | 0.075 | 0.388 | 0.023 |
| Parental Emotional Warmth (EMBU) | 0.258 | 0.100 | 0.184 | 0.056 | 0.753 |
| Parental Control Attempts (EMBU) | 0.170 | 0.104 | 0.210 | 0.148 | 0.405 |
| Child Age | 0.348 | 0.577 | 0.073 | 0.434 | 0.010 |
-
Note: β is the standard regression coefficient from multiple regression analysis. P_Regress is the P value from multiple regression analysis. R_Pearson is the Pearson correlation coefficient from correlation between the individual behavioral characteristics and ToM behavior. P_Pearson is the P value from correlation between the individual behavioral characteristics and ToM behavior. SRS = Social Responsiveness Scale; CPRS = Child–Parent Relationship Scale; EMBU = Egna Minnen av Barndoms Uppfostran; PPVT = Peabody Picture Vocabulary Test. Bold font indicates the significance level at P<0.05.
Table 2
Definition of ToM and SPM regions of interest.
Regions identified, center coordinate [x y z] for each region of interest in the Theory of Mind (ToM) and Social Pain Matrix (SPM) networks. RTPJ and LTPJ, right and left temporoparietal junction; PC, precuneus; DMPFC, MMPFC and VMPFC, dorsal, middle, and ventral components of medial prefrontal cortex; RS2 and LS2, right and left secondary sensory; Rinsula and Linsula, right and left insula; RMFG and LMFG, right and left middle frontal gyrus; AMCC, anterior middle cingulate cortex.
| Network | ROI | Center coordinate |
|---|---|---|
| ToM | RTPJ | (48 -60 30) |
| LTPJ | [-48–62 30] | |
| PC | [0–54 34] | |
| DMPFC | [–6 54 36] | |
| MMPFC | [–4 58 16] | |
| VMPFC | [–4 56–16] | |
| Pain | RS2 | (60 -28 38) |
| LS2 | [-62–32 34] | |
| Rinsula | (42 6 -6) | |
| Linsula | [-42–2 –4] | |
| RMFG | (50 42 12) | |
| LMFG | [–46 36 14] | |
| AMCC | [0 2 42] |
Table 3
Demographic information and behavioral data by age group.
Note: PPVT, Peabody Picture Vocabulary Test, Fourth Edition; CPRS = Child-Parent Relationship Scale; EMBU = Egna Minnen av Barndoms Uppfostran (parenting style); SRS = Social Responsiveness Scale.
| Group | N | Age(Range) | Gender(Female/Male) | Handedness(Right/Left/Mix) | TOM behavior score | PPVT-4(Standard score) | Parents-children relationship (CPRS) | Parents’ rearing behavior (EMBU) | Social Responsiveness (SRS) Total | |||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Conflict | Closeness | Rejection | Emotional warmth | Control attempts | ||||||||
| Pre-junior | 12 | 4.1±0.4 (3.3~4.8) | 6/6 | 11/0/1 | 7.4±4.7 | 139.2±18.8 | 43.3±5.8 | 22.5±9.0 | 16.4±4.46 | 59.4±7.0 | 43.1±5.0 | 36.7±15.0 |
| Junior | 11 | 5.5±0.3 (5.0~5.8) | 5/6 | 10/0/1 | 10.6±2.3 | 152.3±10.8 | 44.4±5.0 | 26.5±8.0 | 18.8±3.0 | 56.2±8.8 | 41.0±4.8 | 32.0±13.7 |
| Senior | 11 | 6.7±0.7 (6.0~8.0) | 6/5 | 10/0/1 | 11.8±1.9 | 151.5±19.0 | 40.2±3.8 | 27.5±9.33 | 19.2±3.4 | 56.5±5.1 | 42.0±4.6 | 23.0±13.8 |
| Adult (Mother) | 34 | 36.7±4.0 (30.7~48.8) | 34/0 | 33/0/1 | NA | NA | NA | NA | NA | NA | NA | NA |
Appendix 2—table 1
Theory of Mind (ToM) and Social Pain event details.
Time (Events in neural responses were then shifted 6 s in time to account for the hemodynamic lag), duration (seconds), and description for each ToM and Social Pain event. Event labels (T01, P01) reflect rank order of average response magnitude in adults.
| ToM events | |||
|---|---|---|---|
| Events | Time point (in stimulus) | Duration | Description |
| T07 | 1:00-1:04 | 4s | Clouds create baby animals accompanied by laughter. |
| T02 | 1:12-1:18 | 6s | Baby cries, Cloud gives him a helmet, and he’s happy. |
| T04 | 1:30-1:36 | 6s | Gus is a lonely cloud. |
| T01 | 2:38-2:50 | 12 s | Peck (crane) gazed longingly at the happy cloud that was making puppies and wore a look of envy. |
| T06 | 2:54-2:58 | 4s | Peck notices that Gus caught him looking longingly and feels bashful. |
| T05 | 3:18-3:22 | 4s | Gus saw Peck scream in agony as he was stabbed by the porcupine’s thorns and exclaimed. |
| T03 | 3:34-4:56 | 22 s | Peck dons football gear to explain to Gus that he did not abandon him, but rather was acquiring protective equipment so that he could continue to deliver Gus’s babies. |
| Social Pain events | |||
| Events | Time point (in stimulus) | Duration | Description |
| P07 | 0:48-0:54 | 6s | Cloud makes baby cat (lightning). |
| P06 | 1:08-1:12 | 4s | Puppy’s chewing on a bone. |
| P08 | 1:24-1:32 | 8s | Gus makes baby alligator (lightning). |
| P05 | 2:04-2:08 | 4s | Peck got bitten on the head by a baby alligator. |
| P03 | 3:02-3:14 | 12 s | Peck’s wing was repeatedly stabbed by porcupine baby’s pinprick |
| P01 | 3:24-3:28 | 4s | Gus pulls porcupine spines out of Peck’s head |
| P04 | 4:12-4:18 | 6s | Gus expresses anger through thunder |
| P02 | 4:52-5:00 | 8s | Peck is electrocuted by baby eel (lightning). |
Appendix 2—table 2
Structural equation modeling (SEM) results.
| X→ | Y | Estimate | St. Err | Z-value | p |
|---|---|---|---|---|---|
| Latent Variables | |||||
| Neural maturity | Personal growth | 1.00 | |||
| Verbal intelligence | Personal growth | 0.452 | 0.290 | –1.556 | 0.12 |
| Age | Personal growth | 1.243 | 0.560 | 2.238 | 0.025 |
| Sex | Personal growth | –1.234 | 0.552 | –2.236 | 0.025 |
| ISS | Parenting | 1.00 | |||
| Relationship conflict | Parenting | –0.797 | 0.261 | –3.047 | 0.002 |
| Relationship closeness | Parenting | 0.500 | 2.254 | 1.971 | 0.049 |
| Rearing warmth | Parenting | –0.174 | 0.249 | –0.698 | 0.485 |
| Rearing rejection | Parenting | 0.989 | 0.268 | 3.692 | <0.001 |
| Rearing control | Parenting | –0.619 | 0.257 | –2.412 | 0.016 |
| Regressions | |||||
| Parenting | Personal growth | –0.708 | 0.271 | –2.618 | 0.009 |
| Parenting | ToM behavior | 0.550 | 0.288 | 1.909 | 0.050 |
| Personal growth | ToM behavior | –0.647 | 0.338 | –1.916 | 0.049 |
| ToM behavior | Social cognition deficit | –0.458 | 0.209 | –2.193 | 0.028 |
| Parenting | Social cognition deficit | 0.427 | 0.319 | –1.336 | 0.182 |
| Personal growth | Social cognition deficit | –0.491 | 0.323 | –1.521 | 0.128 |
| Defined parameters: | |||||
| Direct effect | –0.491 | 0.323 | –1.521 | 0.128 | |
| Indirect effect | –0.210 | 0.106 | –1.976 | 0.048 | |
| Total | –0.651 | 0.325 | –2.005 | 0.045 | |
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Mother-child dyadic interactions shape the developing social brain and Theory of Mind in young children
eLife 13:RP103017.
https://doi.org/10.7554/eLife.103017.3
