Sensitive Infant Care Tunes a Frontotemporal Interbrain Network in Adolescence

doi:10.21203/rs.3.rs-4717524/v1

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Sensitive Infant Care Tunes a Frontotemporal Interbrain Network in Adolescence

https://doi.org/10.21203/rs.3.rs-4717524/v1

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Caregiving plays a critical role in children's cognitive, emotional, and psychological well-being. In the current longitudinal study, we investigated the enduring effects of early maternal behavior on processes of interbrain synchrony in adolescence. Mother-infant naturalistic interactions were filmed when infants were 3 months old and interactions were coded for maternal sensitivity and intrusiveness using the Coding Interactive Behavior. In early adolescence (Mean = 12.30, SD = 1.25), mother-adolescent interbrain synchrony was measured using hyperscanning EEG during a naturalistic interaction of positive valance. Consistent with prior hyperscanning research, we focused on interbrain connections within the right frontotemporal network. Results indicate that maternal sensitivity in early infancy was longitudinally associated with interbrain synchrony in the right frontotemporal network. Post-hoc comparisons highlighted enhancement of mother-adolescent frontal-frontal connectivity, a connection implicated in parent-child social communication. In contrast, maternal intrusiveness in infancy linked with attenuation of interbrain synchrony in the right frontotemporal network. Sensitivity and intrusiveness are key maternal social orientations that are individually stable in the mother-child relationship from infancy to adulthood and foreshadow children's positive and negative social-emotional outcomes, respectively. Our findings are the first to demonstrate that these two maternal orientations play a role in enhancing or attenuating the child's frontotemporal interbrain network that sustains social communication and affiliation. Results suggest that the long-term impact of the mother's sensitive and intrusive style may relate, in part, to its effects on tuning the child's interbrain network to sociality.

Biological sciences/Psychology/Human behaviour

Biological sciences/Neuroscience

Biological sciences/Neuroscience/Social behaviour

Biological sciences/Neuroscience/Social neuroscience

Social Neuroscience

Hyperscanning

EEG

Synchrony

Technological Communication

Mother-Child Relationships

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From the moment infants are born, they depend on their caregivers to fulfil the basic physiological needs and teach the necessary social skills to prepare their brain and behavior for participation in the social world. The caregiver's social behavior plays a critical role in the infant's cognitive, social, and emotional development ^1–5, and in the formation of brain structure and functions ^6–9. This renders early caregiving an important contributor to the maturation of brain and behavior throughout life.

Much research has connected positive developmental outcomes with sensitive caregiving. Sensitivity was first described within the attachment theory framework as the mother's ability to recognize the infant’s signals, accurately interpret them, and respond in an appropriate and timely manner ¹⁰. Sensitive parenting can be observed in mother-infant interactions that include reciprocal exchanges, awareness of the infant’s state, and appropriate stimulation that are contingent upon the infant’s social signals ^11–15. Empirical and meta-analytic studies have confirmed the importance of sensitive caregiving in the first months of life for the development of children’s social-emotional competencies in both normative and high-risk populations ^2,16–20. Longitudinal studies have shown that maternal sensitivity in infancy shapes the development of secure attachment ^21–23, social abilities ^24–28, emotion regulation and social adjustment ^29–33, and cognitive and executive function ^34,35 across childhood ^28,35,36, adolescence ^{22,24,31,34,37,38}, and adulthood ^23,25.

In contrast, researchers have placed maternal intrusiveness as an orientation that is diametrically opposite to the sensitive style and is characterized by maternal overriding and impingement, forceful behavior, overstimulation, and disregard of the child's state, signals, and social initiation ^15,39,40. The mother's intrusive style early in life has been shown to predict insecure attachment ⁴¹, behavior problems and social maladjustment ^39,42,43, difficulties in emotion regulation ⁴⁴, and executive function ^45,46, and language delays ⁴⁷. Both sensitivity and intrusiveness were found in longitudinal studies to be individually stable from infancy to adolescence and young adulthood ^12,37,38,48. As the mother's sensitive-synchronous and intrusive-overriding styles are stable over time, they are considered as resilience and risk factors, respectively, for the child's well-being and development ⁴⁹.

The mechanisms by which maternal sensitivity and intrusiveness render their long-term effects on the developing brain are not fully clear. Studies suggest that the experience of adjusted versus unadjusted parenting behaviors over time impact the maturation of neural systems implicated in social, emotional and cognitive functioning ^6,50–55. Indeed, several longitudinal studies demonstrated the effects of early maternal sensitivity and intrusiveness on brain development and functioning. An EEG study reported that mother-infant interactions characterized by positive affect and less physical stimulation at the age of 5 months predicted higher frontal resting EEG power (alpha and theta band) at the age of 10 and 15 months, suggesting that a more sensitive and less intrusive maternal style quality facilitate brain development ⁵⁶. Structural magnetic resonance imaging (MRI) studies linked maternal sensitivity and support in early childhood with higher gray matter volume ⁶, larger hippocampal volume ⁵⁷ and smaller amygdala volume at school age ⁵⁸. A functional MRI (fMRI) study found that maternal behavior characterized by the awareness of infant’s mental states, appropriate response, and autonomy support at 13 and 15 months predicted functional connectivity between default mode network (DMN) and salience network at 10 years, pointing to the effect of maternal behavior on maturation of networks involved in social cognition, affect cognition and cognitive control ⁹. Another fMRI study found that the mother's sensitive style from infancy to adolescence predicted young adults’ amygdalar and insular sensitivity to others’ emotions ⁴⁸ and greater mother sensitivity and child social engagement in infancy predicted a more consolidated response to attachment reminders in adulthood ⁵⁹. Using magnetoencephalography (MEG), it was found that maternal sensitivity in infancy predicted more accurate neural emphatic response to others’ distress ⁶⁰ and to attachment cues in adolescence ⁶¹.

In addition to the long-term effects of maternal sensitivity on the developing brain, intrusive mothering in infancy has similarly been shown to carry long-term negative effects on the child's brain. Intrusive parenting at 9 months predicted aberrant neural response to others’ pain ⁶² and disrupted default mode network (DMN) connectivity in adolescence ^63,64. Overall, these studies demonstrate the long-term effects of the mother's sensitive and intrusive style on social brain functioning in adolescence.

In contrast to studies that describe the effects of early caregiving on the brain, no study to date have tested the longitudinal impact of the parent's relational style in infancy on interbrain synchrony in later life. Interbrain synchrony considers the temporal concordance of neural dynamics between two or more brains ^65–67. Studies have shown that interbrain synchrony increases when partners are within an attachment relationship, including parents and children ^68,69, romantic partners ⁷⁰, close friends ⁷¹, and patients and therapists ⁷². Mother-child dyads in infancy, childhood, and adolescence, have been shown to display strong interbrain synchrony across multiple tasks, including free play ^68,73–76, joint problem-solving tasks ^77–79, naturalistic face-to-face and video-chat conversations ⁸⁰, and cooperative video-games ^65,69,81.

Interbrain synchrony is sensitive to social behavior and increases when interactions are engaged and reciprocal ^{67,68,70,82–86}. Sharing social gaze, joint engagement, empathic resonance, and interpersonal reciprocity enhance interbrain synchrony, particularly during naturalistic, ecologically-valid interactions ^71,80,87.

According to the biobehavioral synchrony model ^88,89, children acquire the capacity for brain synchrony within the mother-infant context during sensitive, well-timed social interactions (Feldman, 2017, 2020). Consistent with the model, studies have shown that episodes of brain coupling during infancy and early childhood were aligned with the mother's or female stranger's social behavior, including touch, gaze, or vocalizations ^67,85. As to the two maternal orientations, sensitivity and intrusiveness, it was found that maternal sensitivity at 5–9 months was associated with higher mother-infant neural synchrony in a frontotemporal network, while maternal intrusiveness was related to attenuated interbrain coupling in that network, pointing to a differential impact of these two styles on mother-child interbrain synchrony ⁵¹. Another recent fNIRs study found association between secure child attachment and higher mother-child interbrain synchrony within temporal regions ⁷⁹, indirectly pointing at the effect of parenting on mother-child neural synchrony. Still, to our knowledge, no study to date has examined the long-term effect of parenting on the maturation of interbrain synchrony beyond infancy.

In the current study, we examined the longitudinal associations between early maternal caregiving and the development of interbrain synchrony in adolescence. We focused on maternal sensitivity and intrusiveness during naturalistic interactions in infancy and measured mother-adolescent interbrain synchrony 12 years later using hyperscanning EEG. Our key hypothesis was that maternal sensitivity would predict enhanced interbrain synchrony, while intrusiveness attenuated interbrain coupling.

We focused on the frontotemporal network that underpins core socio-cognitive functions ^91,92. Studies of mother-child neural synchrony have shown that this network plays an important role during face-to-face interactions, as well as in remote interactions of zoom or texting ^80,93. In infancy, this network has been associated with the mother's sensitive and intrusive style, respectively ⁵¹. Specifically, we focused on inter-brain synchrony in the right frontotemporal network, and based this hypothesis on the "right hemisphere hypothesis" ⁹⁴. This hypothesis suggests a general dominance of the right hemisphere in processing emotions, and has been supported by numerous studies demonstrating right- hemisphere dominance in multiple emotional functions ^95–102. Given its crucial role in survival-related functions and nonverbal communication, right hemisphere dominance is thought to have a more ancient evolutionary origin as well as to mature early in human development ^103–106. As the mother-child context is the first to facilitate synchrony of brain and behavior, we expected early caregiving to have a more notable impact on the right hemisphere network in connecting the brains of mother and child in adolescence.

Consistent with prior research, we examined interbrain synchrony in the beta frequency band, due to its role in parent-child attachment processes in both mothers ^107,108 and young adolescents ⁶¹. Naturalistic two-brain studies have shown that synchrony of beta rhythms sustains communication between romantic couples and close friends ⁷¹, facilitates empathy and compassion ¹⁰⁹, and is underpinned by social engagement and shared gaze ⁸⁷. Importantly, beta synchrony has been found to sustain interactions between mothers and adolescents during naturalistic interactions ^80,93.

Two hypotheses were formulated. First, we expected that the mother-adolescent face-to-face interaction would trigger significant interbrain synchrony within the frontotemporal network relative to surrogate data baseline. We expected interbrain connections of four types; homologue (same area, same hemisphere), same-region cross-brain links (same area, different hemisphere), cross-region same-hemisphere (same hemisphere, different area), and multi-dimensional (cross-region and cross hemisphere). Second, guided by the bio-behavioral synchrony model ^49,88, we expected longitudinal associations between maternal sensitivity in infancy and greater connectivity in the right frontotemporal interbrain network in adolescence and between early maternal intrusiveness and attenuated interbrain synchrony of the same network in adolescence.

2.1 Participants

Participants included 60 individuals, comprising 30 mother-firstborn pairs seen over a span of 12 years. Mothers and their infants were initially recruited for the study through ads posted in campus for a study on the transition to parenthood (Time 1). All were the infant's biological mothers, served as the child's primary caregiver, and all children were firstborns. At the first time-point mother-infant dyads were seen when infants were 3–4 months old and 40% of the infants were male. All mothers had completed at least high-school education and 83% finished college and all were of middle to upper-middle SES. Mothers were all healthy, infants were all born at term without complications, and 87% were breastfeeding.

In early adolescence (Time 2) the mothers’ average age was 41.31 years old (SD = 3.40), and the adolescents’ average age was 12.30 years old (SD = 1.25). 40% of the adolescents were males. All participants were healthy, and all adolescents attended state-controlled typical schools.

The original study during Time 1 was approved by the Bar-Ilan University ethics committee. The Reichman University institutional ethics committee approved the hyperscanning EEG experiment during Time 2, and all experiments were performed in accordance with the relevant guidelines and regulations. All mothers signed a written informed consent form for themselves and their adolescent children. All procedures were explained to the participants prior to the experiment, and the participants were free to leave the experiment at any time with full compensation. Participants were reimbursed for study participation ($30 per hour).

2.2 Procedure

Infancy

Mother-infant dyads were videotaped during a naturalistic interaction. Instructions were “play with your infant as you normally do” and 10 minutes of free play interaction were filmed for offline coding.

Adolescence

The study utilized hyperscanning dual-EEG during positive-valance interaction. Mother-adolescent dyads set on chairs in the same room, 50 cm apart from each other, in a face-to-face position and were instructed to discuss a positive topic randomly selected by the researchers. Three possible positive topics were counterbalanced; "plan a fun day to spend together" "plan a camping trip", "plan a visit to an amusement park". (See Fig. 1)

2.3 Dual neural and behavioral data acquisition

The EEG activity of both the mother and adolescent was recorded simultaneously and continuously throughout the experiment. The first 2 minutes of the interaction were analyzed, consistent with prior research ^68,80. Data acquisition was performed using a 64-channel BrainAmp amplifier from Brain Products Company (Germany). The EEG system was composed of two Brain product standard subtemporal BrainCap with an integrated chin belt. Each cap included 32 electrodes each, buttoned directly to the cap and arranged according to the international 10/10 system, an extension of the standard 10/20 system (See Supplementary Table S1 for full list of electrodes and electrode positions. Theta/Phi coordinates are reported, standardized to a Theta of 90 for the plane through Fpz, T7, T8, Oz). Analog 0.1–500 Hz band-pass was used for filtering, and data was sampled at 1000Hz. Impedances were maintained below 10 kOhm, and the ground electrode was placed on the AFz electrode. Both helmets were connected to the same amplifier to ensure millisecond-range synchrony between the EEG recording of the mother and adolescent.

2.4 EEG Preprocessing

Preprocessing was conducted using Spyder 5.05 and Python 3.8, utilizing MNE (v0.17.0). First, the EEG data file of each dyad was separated into two data files, one for the mother and one for the child, so that each file could undergo separate preprocessing. Data were then average-referenced, and a 1–50 Hz bandpass filter was applied to all data files, consistent with prior studies ^68,71,80. Next, the data were segmented into 1000 ms epochs with 500 ms overlap between epochs. Autoreject v0.1 ¹¹⁰, an unsupervised algorithm with Bayesian optimization as the threshold method, was utilized to remove trials containing transient jumps in isolated EEG channels and artifacts affecting groups of channels. Following AR, a sample of the first 10 epochs of each participant was visually inspected pre- and post-AR correction to verify the algorithm's output. While AutoReject specializes in excluding trials containing transient jumps in specific channels, systematic physiological artifacts that may affect multiple sensors, such as eye blinks or muscular movements are not optimally removed by AR algorithms. Therefore, ICA was used to remove artifact components from the data. To that end, MNE’s implementations of fastica and CORRMAP ¹¹¹ were used to remove systematic physiological artifacts that affected the data. Independent components (IC) were manually selected for exclusion and served as templates for selecting and excluding similar components in all other participants. Such components included non-physiological components, eye blinks, eye movements, and muscle artifacts to control for muscular movements while speaking (see Supplementary Fig. S1).

Overall, following preprocessing and cleaning procedures, an average of 110.08 (SD = 54.31) epochs per dyad remained in the face-to-face condition. Following preprocessing, dyads that did not share a minimum of 30 common epochs in each condition were excluded from the following connectivity analysis, resulting in the exclusion of one dyad.

2.5 Connectivity Analysis

Interbrain synchrony was calculated using the weighted phase lag index (wPLI), an interbrain connectivity method that has been used in various previous studies of naturalistic social interactions ^68,80,93,112. Interbrain connectivity values were calculated for the beta rhythm (13.5–29.5 Hz).

Consistent with prior research, we divided the EEG cap into pre-defined areas of interest based on the research hypotheses ^71,80,93,113, resulting in a total of 4 ROIs that were examined in this study. Each ROI consisted of 3 electrodes: right frontal (RF - Fp2, F4, F8), left frontal (LF - Fp1, F3, F7), right temporal (RT - T8, TP10, P8), and left temporal (LT - T7, TP9, P7). We were particularly interested in the right frontal and temporal areas. The grouping of channels was used to enhance the reliability of region specification and provide a more meaningful and realistic interpretation of the results ¹¹⁴. Overall, a total of 4 ROIs were measured in each brain, resulting in 16 possible links between the mother's and adolescent's ROIs in the comparison to surrogate data (control) analysis. The respective wPLI value of the partners' ROIs was calculated as the mean connectivity value of each of the 3 electrodes in one target ROI with each of the 3 electrodes in the second target ROI, resulting in a total of 9 connectivity values averaged for each interbrain link between 2 ROIs.

Of the 30 dyads participating in the experiment, one dyad did not share sufficient common epochs following AutoReject and IC rejection, so connectivity could not be measured, resulting in a total of 29 dyads that were included in the analysis.

2.6 Behavioral Coding

Mother-infant interaction was coded offline using the Coding Interactive Behavior manual (CIB, Feldman, 1998). The CIB is a well-validated rating system used for coding social interactions that has yielded over 200 publications across multiple cultures, age range, and pathological conditions (see Feldman, 2012, 2021 for review), including hyper-scanning research ^68,71,80,93. The CIB yields 52 codes, each rated on 5-point scales that aggregate into theoretically-based constructs. Here, we used the two central constructs of maternal behavior. Maternal sensitivity comprised the following scales: parent gaze, vocal appropriateness, reciprocity, enthusiasm (alpha = .91). Maternal intrusiveness included the following scales: overriding, imitation, anxiety, constriction (alpha = .89). Coding was conducted by trained coders who were blind to study hypotheses with inter-rater reliability for 20% of the interactions exceeding 90% on all codes (intra-class r = .93, range = .89–99).

2.7 Statistical Analysis

2.7.1 – Comparing neural synchrony during social interaction vs. surrogate data

First, we conducted a validation analysis of the neural connectivity values of the face-to-face relative to a control condition of surrogate data. Our goal was to evaluate whether face-to-face interaction resulted in increased interbrain connectivity values relative to the surrogate data control, consistent with previous literature on two-brain research ^65,77,80,116. This analysis was conducted on the fronto-temporal network, resulting in 4 areas of interest (RT, LT, RF, LF) in each brain, leading to 16 possible interbrain links between the mother and child brains.

Surrogate data was created by computing the data of one member of a dyad (mother) with the data of the other member (adolescent) from a different dyad and calculating the wPLI connectivity values for the surrogate dyad. This was done for every possible combinations of mother and other-adolescent in each of the other dyads, resulting in 28 different surrogates for each of the 29 mothers. Overall, this resulted in 812 surrogate mother other-adolescent combinations. Then, the 28 surrogate connectivity values that were created for each mother were averaged, leading to a single, “average surrogate” for each mother.

The average surrogate connectivity values were then examined relative to the data of the real dyads. The analysis was conducted using "eelbrain", an open source Python module for accessible statistical analysis of MEG and EEG data (v0.31.7, https://github.com/christianbrodbeck/eelbrain, DOI 10.5281/zenodo.598150). A non- parametric permutation test with mass-univariate was utilized as this test uses the distribution derived from permuting the observed scores of the data and to avoid multiple comparisons ¹¹⁷.

The permutation test was used to compute the F value for each of the ROI pairs in order to compare connectivity patterns between the real connectivity scores and the surrogate data. The same procedure was repeated in 1000 random permutations of the two data, shuffling the condition labels (face-to-face, control). For each permutation, the largest F value was retained to form the nonparametric estimate of the distribution under the null hypothesis that condition labels are exchangeable. The p-value was computed for each ROI pair as the proportion of permutations that yielded a comparison with a larger F value than the comparison under question. Following the permutation tests, only ROIs that reached a p-value of 0.05 or smaller are reported in the results section.

2.7.3 Brain-behavior correlations

Following, brain-behavior Pearson correlations were used to examine whether maternal behavior during infancy affected neural synchrony in adolescence. Here, we chose to focus on two well-known and validated constructs – maternal sensitivity and maternal intrusiveness ¹¹⁸. Consistent with previous research describing the advantage of the right hemisphere in infancy ^104,119, the brain-behavior correlations focused on the right hemisphere network, and were computed between the maternal behavior during the child’s infancy and the IBS connectivity values. Notably, IBS values were calculated as the increase in interbrain connectivity relative to control (wPLI of face-to-face interaction – wPLI of surrogate data = ΔwPLI).

3.1. Comparing neural synchrony during Face-to-face relative to surrogate data

We first compared neural synchrony during face-to-face interaction and the control condition (surrogate data) by using nonparametric permutation test with mass-univariate analysis of variance (ANOVA) based on one-way repeated-measures ANOVA designed to detect effects stemming from the face-to-face interaction compared to control on wPLI scores. The results revealed a significant main effect for the face-to-face condition compared to control (F(1, 61) = 23.83, p < .001). (See Fig. 2A, 2B).

Significant (p < 0.05) inter-brain connections were observed in every one of the possible 16 links of the fronto-temporal network (Fig. 2B, Table 1). The greater neural synchrony in the face-to-face interaction compared to the control condition comprised four sub-groups: (a) Homologous links between mother-child frontal and temporal regions (b) same hemisphere, cross-regional links between the mother and child’s temporal and frontal regions (c) inter-hemispheric same-region linkage of mother and child's frontal and temporal regions, (d) Inter hemisphere inter-region between mother and child’s fronto-temporl network.

Homologous connections between mother-adolescent frontotemporal network – the homolog links included the left-frontal-left-frontal link (F(1, 28) = 15.8, p = .001, η²_p = 0.36), the right-frontal-right-frontal link (F(1, 28) = 12.26, p = .011, η²_p = 0.3), the left-temporal-left-temporal link (F(1, 28) = 10.8, p = .017, η²_p = 0.28), and the right-temporal-right-temporal link (F(1, 28) = 13.99, p = .001, η²_p = 0.33).

Same-hemisphere, cross-regional connections within mother-adolescent frontotemporal network – comprised four links; two in the left hemisphere: between the mother's left frontal region and the adolescent's left temporal region (F(1, 28) = 23.1, p < .001, η²_p = 0.45), and the mother's left temporal region with the adolescent's left frontal region (F(1, 28) = 13.9, p = .001, η²_p = 0.33). Two links were also found In the right hemisphere: between the mother's right frontal region and the adolescent's right temporal region (F(1, 28) = 12.1, p = .011, η²_p = 0.3), and the mother’s right temporal region with the adolescent’s right frontal region (F(1, 28) = 12.6, p = .001, η²_p = 0.31).

Same-region, cross-hemisphere connections within mother –adolescent frontotemporal network included four links: between the mother's left frontal region and the adolescent's right frontal region (F(1, 28) = 10.9, p = .016, η²_p = 0.28), between the mother’s right frontal and the adolescent’s left frontal region (F (1, 28) = 11.1, p = .016, η²_p = 0.28), between the mother’s left temporal region and the adolescent’s right temporal region (F(1, 28) = 14.9, p = .001, η²_p = 0.35), and between the mother’s right temporal region and the adolescent’s left temporal region (F(1, 28) = 16.8, p < .001, η²_p = 0.38).

Cross-region connections within mother-adolescent fronto-temporal network. This included four links: between the mother's left frontal region and the adolescent's right temporal region (F(1, 28) = 12.9, p = .007, η²_p = 0.32), between the mother's right frontal region and the adolescent's left temporal region (F(1, 28) = 15.2, p = .001, η²_p = 0.35), between the mother's left temporal region and the adolescent's right frontal region (F(1, 28) = 10.1, p = .02, η²_p = 0.27), and finally between the mother's right temporal region and the adolescent's left frontal region ((F(1, 28) = 10.7, p = .017, η²_p = 0.28). (See Fig. 2B, Table 1).

Following the findings that mother-child face-to-face interactions facilitated greater interbrain synchrony relative to control across all links, we assessed our next hypothesis on the association between maternal behavior in infancy and interbrain synchrony in adolescence.

Table 1

Table 1

– Mean (SD) for Face-to-face and Texting Interactions
Interbrain link	wPLI Face-to-face (SD)	wPLI surrogate (SD)	F	p value
Mother left frontal - Child left frontal	0.138 (0.05)	0.107 (0.03)	15.75	0.001 ***
Mother left frontal - Child right frontal	0.134 (0.05)	0.106 (0.03)	10.93	0.016 *
Mother left frontal - Child left temporal	0.139 (0.05)	0.109 (0.03)	23.06	< .001 ***
Mother left frontal - Child right temporal	0.136 (0.05)	0.109 (0.03)	12.89	0.007 **
Mother right frontal - Child left frontal	0.132 (0.05)	0.107 (0.03)	11.06	0.016 *
Mother right frontal - Child right frontal	0.132 (0.05)	0.108 (0.03)	12.26	0.011 *
Mother right frontal - Child left temporal	0.140 (0.05)	0.110 (0.03)	15.24	0.001 ***
Mother right frontal - Child right temporal	0.135 (0.05)	0.110 (0.03)	12.05	0.011 *
Mother left temporal - Child left frontal	0.137 (0.05)	0.110 (0.03)	13.86	0.001 ***
Mother left temporal - Child right frontal	0.134 (0.05)	0.108 (0.03)	10.13	0.02 *
Mother left temporal - Child left temporal	0.138 (0.05)	0.111 (0.03)	10.79	0.017 *
Mother left temporal - Child right temporal	0.134 (0.05)	0.109 (0.03)	14.9	0.001 ***
Mother right temporal - Child left frontal	0.131 (0.05)	0.109 (0.03)	10.74	0.017 *
Mother right temporal - Child right frontal	0.138 (0.05)	0.109 (0.03)	12.57	0.01 **
Mother right temporal - Child left temporal	0.140 (0.05)	0.110 (0.03)	16.75	< .001 ***
Mother right temporal - Child right temporal	0.131 (0.04)	0.110 (0.03)	13.99	0.001 ***

Table 1: Increased IBS following face to face interactions relative to control. Reported here are the significant interbrain links emerging following nonparametric permutation test with mass-univariate analysis of variance (ANOVA) to detect differences on wPLI connectivity measures during face to face interactions relative to control. All results were corrected to accommodate multiple comparisons. Inter-brain neural synchrony was found in each link of the fronto-temporal network. *P < 0.05 **P < 0.01, ***P < 0.001.

3.2 Brain-behavior coupling

3.2.1 Increase in interbrain connectivity within the right hemisphere network is related to maternal sensitivity and intrusiveness

Focusing on the right hemisphere, we then assessed the advantage of the right hemisphere interbrain network over control (averaged across all 4 links that are specific to the right hemisphere – RF-RF, RT-RT, RF-RT, RT-RF). A repeated-measures ANOVA revealed greater right network synchrony in the face-to-face interaction relative to control (F(1, 28) = 18.47, p < .001, η²_p = 0.4) (See Fig. 2C). Following, we investigated the association between maternal sensitivity and intrusiveness and the index of increased right hemisphere interbrain connectivity in the face-to-face condition compared to control (wPLI of face-to-face interaction – wPLI control = ΔwPLI).

Maternal sensitivity predicts greater synchrony in the right frontotemporal interbrain network

The results revealed that the maternal sensitivity strongly correlated with the improvement in face-to-face interbrain synchrony relative to control (N = 29, r = 0.41, p = 0.026, see Fig. 3A). Following this finding, we next sought to shed light on the links that sustained this correlation within the right hemisphere network in a set of post-hoc tests. Results indicate that maternal sensitivity correlated with both the right frontal homolog link (N = 29, r = 0.41, p = 0.029) and the mother-right-frontal adolescent-right-temporal link (N = 29, r = 0.47, p = 0.01). The remaining links in the right network did not correlate with maternal sensitivity (see Supplementary Table 2) (see Fig. 3A).

Next, to evaluate the achieved power, we examined the correlation using a regression model, with the maternal sensitivity (measured when the children were 3-motths) to predict the frontotemporal IBS in the right hemisphere network. The results indicate that for effect size of F² = 0.22, with α = 0.05, and a total sample size of N = 29, with one predictor, the power was 0.688.

Maternal intrusiveness predicts lower synchrony in the right frontotemporal interbrain network

The results revealed that the maternal intrusiveness correlated negatively with the improvement in interbrain synchrony in the face-to-face interaction relative to control (N = 29, r = -0.37 p = 0.049) (see Fig. 3A). Following this finding, we next sought to shed light on the links that sustained this correlation within the right network in a set of post-hoc tests, and revealed that maternal intrusiveness negatively correlated the mother-right-frontal adolescent-right-temporal link (N = 29, r = -0.43, p = 0.02). The remaining links in the right network did not correlate with maternal intrusiveness (see Supplementary Table 3) (see Fig. 3A).

Then, to evaluate the achieved power, we examined the correlation using a regression model. The results indicate that for effect size of F² = 0.16, with α = 0.05, and a total sample size of N = 29, with one predictor, the power was 0.55.

Cross-hemisphere frontotemporal connections associated with maternal sensitivity and intrusiveness

Finally, based on the findings described by Endelvalt-Shapira & Feldman (2023), who revealed that the mother-left-frontal infant-right-temporal connection correlated negatively with maternal intrusiveness in real-life interactions, the same link has been evaluated in our study. The results indicated that in our study the mother-left-frontal child-right-temporal link also correlated negatively with maternal intrusiveness (N = 29, r = -0.49 p = 0.007). The same cross-hemisphere connection also correlated positively with maternal sensitivity (N = 29, r = 0.42 p = 0.022), (see Fig. 3B)

Maternal care provides the basis for the child's future development, well-being, social competencies, and brain functioning ^{1,2,120–122}. However, despite research on interbrain synchrony flourishing in the last decade, the current study is the first to describe the association between early caregiving and the maturation of interbrain synchrony, that have been proposed as a key mechanism for joint cognitive processes ^123,124.

Several important findings are highlighted by our data. First, consistent with previous literature on mother-child interbrain synchrony from infancy to adulthood ^{68,69,71,77,79–81,125}, we found a significant synchrony between mother and child's brain in frontotemporal regions, as indexed by an increase in interbrain synchrony between mother and child in the frontotemporal network during free interaction relative to a control condition. The face-to-face naturalistic interaction tightened a frontotemporal interbrain network that increased the connectivity in each of the 16 possible combinations of connections between mother and child's brains; homologous same-region-same-hemisphere connections, same-hemisphere-different-region connections, same-region-different-hemisphere connections, and frontal-to-temporal or temporal-to-frontal different hemisphere connections.

Second, results point to the long-term associations between the main maternal caregiving orientations in infancy described in the literature and interbrain synchrony in adolescence. Maternal sensitivity in infancy was associated with the degree of improvement in neural synchrony in the right hemisphere frontotemporal network; more attuned caregiving to the infant's cues linked with greater neural synchrony 12 years later. This brain-behavior link was specific to the partners' right hemisphere and was facilitated by two important connections. The first is the mother-child right-frontal-right-frontal connection, a link that has been found in multiple studies of parent‒child interbrain synchrony ^65,80,126. The second is the connection between the mother’s right-frontal region and the adolescent’s right-temporal region, a link that is consistent with previous mother-child interbrain studies ^80,93. These findings point to the possibility that sensitivity and intrusiveness may have lingering effects on children's capacity for interbrain synchrony, particularly of the right hemisphere.

The two hemispheres are known to exhibit asymmetrical involvement in various cognitive processes, with such lateralization enabling the right hemisphere to specialize in distinct functions ^95–102,127. The right hemisphere's advantage in processing non-verbal cues is evident early in life: infants aged 2–3 months demonstrate right hemispheric activation in response to women's faces ¹²⁸, and by 6 months they show a greater activation in the right fronto-temporal cortex following exposure their mother's face relative to unknown faces ¹²⁹. Notably, such right-hemisphere advantage extends beyond the visual system, as words spoken with emotional over neutral prosody elicited greater right temporal response in 7-month old infants ¹³⁰. These findings support the hypothesis that the right hemisphere specializes in the interpretation of non-verbal cues. This hypothesis is further supported by evidence that right hemisphere damage impairs the ability to recognize and interpret emotional expressions and signals ¹³¹ and to understand and produce the emotional tone of speech ^132,133. These non-verbal social signals are critical for understanding social interactions and play an important role in emotional and attentional processes (for review see Hartikainen, 2021).

In line with these findings, the right-hemisphere lateralized network is crucial for various social functions, including empathy ¹³⁵, emotional processing ^136,137, theory of mind ¹³⁸, and understanding others ¹³⁹. The right hemisphere has been proposed to be a pivotal center for interpersonal emotional communication, particularly in early infancy when the non-verbal emotional interactions between the mother-infant dyad take place ¹³⁷. This pre-verbal communication relies on facial emotional expressions, gestures, and prosody, which collectively provide the groundwork for attachment formation. Through sensitive caregiving, in which mother monitors and adjusts her behavior to the infant's emotional state, the mother can regulate the infant’s emotions, a process that depends on the aforementioned right-hemispheric functions of both individuals. Over time, these mother-infant social interactions facilitate the maturation of the infant's social and emotional functions, including the brain regions and networks that support these functions, such as the right TPJ ¹⁴⁰.

Our findings may suggest that the joint activation of the right-hemisphere network begins in early infancy and extends into adolescence. Possibly, the maternal right brain influences the development of the infant's right brain, resulting in a consistent pattern of right-lateralized processing years after infancy. This pattern is dependent on the mother's ability to respond to and regulate the child's brain throughout development.

Specifically, our findings underscore the centrality of right frontal areas to mother-child interbrain coupling and their association with maternal sensitivity. The frontal-frontal connection between parents and children have been well-established across multiple studies using both hyperscanning EEG and fNIRS methodologies. Mother-child fNIRS studies reported right frontal-frontal synchrony during recovery as compared to a frustration task (Quiñones-Camacho et al., 2020), during cooperation tasks (Miller et al., 2019), and in both cooperation and competition tasks ¹²⁶. In addition, mother-child dyads exhibited greater right frontal-frontal synchrony as compared to stranger-child dyads in both competition and cooperation tasks ¹⁴¹. The frontal areas implicate higher-order social functions, including social cognition, mental state knowledge, and social decision-making ^142,143, abilities that are known to develop in the context of maternal care ¹⁴⁴. Overall, our findings add to the existing literature and suggest that the mother’s frontal areas play an important role in monitoring, adjusting, and regulating the two-brain dynamics with her child and adjust in real-time to the child's signals and needs. This tunes the developing brain to social life, partly through interbrain synchrony mechanisms ^49,145.

Our findings indicate interbrain synchrony of beta rhythms. This aligns with extensive research pointing to the crucial role of beta rhythm in parent-child interactions and attachment processes ^{61,80,93,107,108}. Beta rhythms are also involved in higher social functions related to the frontotemporal network and to right-hemisphere functions, including empathy ¹⁴⁶, mentalization ¹⁴⁷, the prediction of others' behavior ¹⁴⁸, and active information processing ¹⁴⁹. Consistent with the theory that mothers adjust their behavior in real-time to match their child's cues and regulate the child through sensitive caregiving, the beta frequency is further linked with continuous adaptation and updating of predictions ¹⁵⁰. Overall, we propose that the neural synchrony in the beta frequency observed here may be related to the ongoing adaptation and mutual adjustment of the mother-child dyad, processes that are essential for interbrain coordination ¹⁵¹.

Across the development from infancy to adolescence the brain undergoes significant changes, particularly in regions involved in social functions, such as the prefrontal cortex (PFC) and the posterior superior temporal sulcus (pSTS) ¹⁵². In our study, we identified a network of interconnections between the mother’s and child’s right and left frontal and temporal regions in various combinations. Their joint activations across a variety of connection suggests that this frontotemporal network supports joint socio-cognitive functions ^91,92. Despite the rapid maturation and changes these regions experience during adolescence, we found that the neural coherence of the dyad correlated with maternal behaviors measured years earlier. Our findings are consistent with previous hyperscanning studies that have reported frontal-temporal neural synchrony during social interactions (Pérez et al., 2017; Schwartz et al., 2022; Tang et al., 2015; Zhang et al., 2017), and further extend the existing literature by showing that increased connectivity in the right frontotemporal network during face-to-face interactions could be predicted by maternal behavior measured many years earlier.

Several limitations of the study should be noted. First, we base our findings on a relatively small sample. Although the uniqueness of our study lies in the longitudinal follow-up of over 12 years, future longitudinal studies are needed to validate the findings in larger samples. Studies should also examine the longitudinal impact of fathering and of early difficulties to bonding, in conditions such as postpartum depression, premature birth, or environmental adversity. Our study points to the potential enduring effects of early maternal behavior on the development of interbrain synchrony processes. Much further research is needed to explore these longitudinal links and shed light on the mechanisms by which maternal behavior tunes the child's brain to the social world.

Author Contribution

LS -conceptualization, study design, wrote the main manuscript, performed statistical analysis, and run the experiment at timepoint 2.OH - conceptualization, study design, wrote the main manuscript, performed statistical analysis, and run the experiment at timepoint 2. J. L - Conceptualization, experimental designI. G - Conceptualization, study design, running experiment at timepoint 1R. F - Conceptualization, writing, study design, statistical analysis, supervision

Data Availability

The data generated during the current study are not publicly available due to participants' privacy but are available from the corresponding author on reasonable request.

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No competing interests reported.

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Sensitive Infant Care Tunes a Frontotemporal Interbrain Network in Adolescence

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Abstract

Figures

Introduction

Materials and Methods

2.1 Participants

2.2 Procedure

2.3 Dual neural and behavioral data acquisition

2.4 EEG Preprocessing

2.5 Connectivity Analysis

2.6 Behavioral Coding

2.7 Statistical Analysis

2.7.1 – Comparing neural synchrony during social interaction vs. surrogate data

2.7.3 Brain-behavior correlations

Results

3.1. Comparing neural synchrony during Face-to-face relative to surrogate data

3.2 Brain-behavior coupling

Maternal sensitivity predicts greater synchrony in the right frontotemporal interbrain network

Maternal intrusiveness predicts lower synchrony in the right frontotemporal interbrain network

Cross-hemisphere frontotemporal connections associated with maternal sensitivity and intrusiveness

Discussion

Declarations

Author Contribution

Data Availability

References

Additional Declarations

Supplementary Files

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