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Hyperscanning Studies on Interbrain Synchrony and Child Development:
A Narrative Review
Xiaoyan Bi,
a,b
Hongbo Cui
a
and Yankun Ma
a
*
a
School of Education, Guangzhou University, Guangzhou, China
b
Institution of Science, Chinese Academy of Science, Beijing, China
Abstract—
Social interactions between parents and children are closely linked with children’s development, and
interbrain synchrony has been shown to be a neural marker of social interaction. However, to truly capture the
essence of social interactions through interbrain synchrony, it is necessary to simultaneously discuss the paren-
tal and child brains and adequately record neurological signals during parent–child interactions in interactive
tasks. In the current review, we have reviewed three main contents. First, we discuss the correlation between par-
ent–child interbrain synchrony and the development of cognitive (e.g., emotion regulation, attention, and learn-
ing) and behavioral abilities (e.g., cooperation, problem-solving) in children. Second, we examine the different
neural mechanisms of interbrain synchrony in mother–child and father-child interactions, aiming to highlight
the separate roles of mother and father in child development. Last, we have integrated four methods to enhance
interbrain synchrony, including communication patterns, nonverbal behavior, music, and multichannel stimula-
tion. A significant correlation exists between parent–child interbrain synchrony and the development of children’s
cognitive and behavioral abilities. This summary may be useful for expanding researchers’ and practitioners’
understanding of the ways in which parenting and the parent–child relationship shape children’ cognitive and
behavioral abilities.Ó2023 IBRO. Published by Elsevier Ltd. All rights reserved.
Key words: interbrain synchrony, mother, father, child development, hyperscanning.
STUDYING NATURALISTIC DYADIC
INTERACTIONS
Social interactions with others are essential for virtually all
aspects of human development (Hamilton, 2021). These
interactions are fast-paced and multi-layered, requiring
the brain to process complex information from multiple
visual and auditory sources in a timely manner (Wass
et al., 2019). From early life, social interactions between
parents and children play an important role in children’s
structural and functional brain development (Nguyen,
Banki, et al., 2020; Ratliff et al., 2022), mental health
(Su et al., 2022), affective states, self-regulation (Bell,
2020), emotion regulation abilities (Turk et al., 2022),
attention and learning (Kuhl et al., 2003; Begus et al.,
2014), internalizing and externalizing problems
(Eisenberg et al., 2010; Abulizi et al., 2017) and so on.
Decades of research exploring the relationship
between child development and parenting have already
revealed that positive socio-emotional outcomes are
predicted by supportive parental interactions with
children (Knauer et al., 2019; Turk et al., 2022), whereas
negative family interactions are detrimental to children’s
psychological wellbeing, causing and maintaining various
psychopathological symptoms and altering emotional
brain development (Diaz et al., 2019; Su et al., 2022).
The psychosocial and bio-behavioral synchrony models
suggest there is a significant correlation between child-
parent social interactions and children’s development
(Ratliff et al., 2022). The bio-behavioral synchrony model
integrates both biological and behavioral aspects of
parent–child interactions. It posits that the alignment or
synchrony in biological and behavioral responses
between parents and children can foster effective commu-
nication, emotional co-regulation, and social bonding.
This synchrony can be manifested in various forms, such
as synchronized heart rates, hormonal levels, and brain
activities, as well as coordinated behaviors and emotional
expressions.Table 1.
It is crucial to understand how very young children
begin to make sense of their parents in order to interact
with them effectively. In their relationships with others,
children are embodied agents rather than passive
observers, actively participating in dynamic exchanges
https://doi.org/10.1016/j.neuroscience.2023.08.035
0306-4522/Ó2023 IBRO. Published by Elsevier Ltd. All rights reserved.
*Corresponding author.
E-mail address: 631360184@qq.com (Y. Ma).
Key words: EEG, electroencephalography; fNIRS, functional near-
infrared spectroscopy; dlPFC, the bilateral dorsolateral prefrontal
cortex; TPJ, temporo-parietal junction; NAcc, the Nucleus
Accumbens; PFC, the prefrontal cortex; ERP, Event-Related
Potentials.
NEUROSCIENCE
REVIEW
X. Bi et al. / Neuroscience 530 (2023) 38–45
38
(De Jaegher et al., 2016). And naturalistic interaction offer
promising avenues for investigating brain function across
the rich, realistic spectrum of parent–child interactions
experiences, which are integral to the naturalistic para-
digm (Finn et al., 2020; Ogilvie et al., 2020; Simony and
Chang, 2020). Optimal parental interactions can be
defined as synchronous relationships in which the parent
is aware of the child’s current condition and social signals
and responds appropriately (Feldman, 2007). The theoret-
ical synchrony model postulates that healthy interactions
between parents and children play a crucial role in regulat-
ing the child’s developing social skills and their neurobio-
logical states (Carollo et al., 2021). This model offers a
comprehensive perspective on the complex interplay
between social, emotional, and biological dimensions of
development. Healthy interactions between parents and
children, according to this model, are characterized by a
synchronous, reciprocal, and responsive relationship. This
synchrony, often referred to as ’attunement’, involves the
alignment of emotional states, behaviors, and physiologi-
cal responses between the parent and child. Such interac-
tions provide a rich social environment that nurtures the
child’s developing social skills, such as empathy, cooper-
ative behavior, and conflict resolution skills.
INTERBRAIN SYNCHRONY WITH PARENT–
CHILD
However, to truly capture the essence of social
interactions through interbrain synchrony, it is necessary
to simultaneously discuss the parental and child brains
and adequately record neurological signals during
Table 1. Increasing interbrain synchrony to promote parent–child behavior.
Conversational patterns
The conversational synchrony indicated that conversation patterns, such as turn-
taking, may support cross-brain associations and emphasize the significance of
understanding dynamic emotion-related processes and their relationship to
psychological well-being during parent–child social interactions.
Nonverbal behavior
Affectionate touch: an essential pathway to establishing
Speaker eye contact and gaze: enhances information coupling
Gestural imitation: nonverbal interpersonal contact is established
Joint attention: promoted mutual entrainment
Music
Music has been an integral facilitator of social bonds among variety of different
species, including humans. Musical intervention children can enhance brain-to-brain
coupling with their parents.
Multimodal stimulation
Adults often use multiple modalities to interact with children, and these multimodal
forms of stimulation (such as joint attention, play, speech, and daily routines) are
more likely to improve the interbrain synchrony present in the interaction than a
single mode of stimulation.
X. Bi et al. / Neuroscience 530 (2023) 38–45 39
parent–child interactions in interactive tasks. Interbrain
synchrony has been shown to be a neural marker of
social interaction. It is more commonly used to describe
methods in which activity in specific brain regions (the
same area in both individuals’ brains) is correlated over
time to identify regions that activate in sync in parent–
child relationships (Ratliff et al., 2021; Roque et al.,
2022). Research indicates that, compared to performing
identical tasks separately or interacting with a third party,
parents and children synchronize their brain processes
more in interactive contexts that involve mutual participa-
tion when they are together (Nguyen, Schleihauf, et al.,
2020; Ratliff et al., 2022). In addition, the research con-
ducted by Carollo et al., (2021) investigated the neural
correlates of parent–child interbrain synchrony, employ-
ing a neuroscience lens to illuminate the psychological
dynamics of these interactions. Nevertheless, further
researches are required to understand the several fine
ways in which synchrony at all level of analysis emerges
and is dynamically modulated.
So far, hyperscanning studies have demonstrated that
interbrain synchronizations is associated with successful
communication (Nguyen, Banki, et al., 2020), enhanced
cooperation (Ratliff, 2019), improved emotion regulation
(Atzaba-Poria et al., 2017), and increased mutual under-
standing between parents and children, rather than
merely being a physiological response to physical speech
signals. Extending beyond these aspects, interbrain syn-
chrony could play a role in the long-term development of
attachment (Atzaba-Poria et al., 2017; Feldman, 2017;
Wong et al., 2018; Markova et al., 2019; Djalovski et al.,
2021). Hyperscanning, capturing neural activity from mul-
tiple individuals simultaneously, employs ’naturalistic’
designs to glean insights from real-life interactions (Cui
et al., 2012; Samadani et al., 2021). As such, it is essen-
tial to simultaneously record the neural signals of all par-
ticipants in the interaction task using hyperscanning, as
this approach can truly capture the essence of parent–
child social interactions through inter-brain synchroniza-
tion. We believe that this may promote interpersonal coor-
dination during parent–child interactions.
PARENT-CHILD INTERACTION AND CHILD
DEVELOPMENT
Interbrain synchrony may embody an underlying neural
mechanism that facilitates the emotional connection
between parent and child, which in turn is associated
with the child’s developing cognitive abilities (e.g.,
emotion regulation, attention, and learning) and
behavioral competencies (e.g., cooperation, problem-
solving). Longitudinal research has demonstrated that
the degree of parent–child synchrony is predictive of
child development (Feldman and Greenbaum, 1997).
Emotional regulation ability. Studies have shown
that greater child emotion regulation abilities are
associated with higher levels of interbrain synchrony
(Reindl et al., 2018). This relationship between synchrony
and child emotion regulation may be mediated by attach-
ment security (Feldman, 2007). Reindl et al. (2018) found
that both parental and child habitual emotion regulation
were positively related to interbrain synchrony when par-
ent–child cooperation was compared to stranger-child
cooperation. Similarly, Lee et al. (2017) discovered that
greater interbrain synchrony between parent and child
led to improved emotional regulation in the child. Previous
parent–child electroencephalography (EEG) studies have
shown that a mother’s positive emotional expression is
associated with greater frontal alpha asymmetry
(Atzaba-Poria et al., 2017; Perone et al., 2020) and stron-
ger brain-to-brain alpha connectivity between mother and
child (Santamaria et al., 2020). Conversely, decreased
dual-functional near-infrared spectroscopy (fNIRS) based
interbrain synchrony between a mother and child has
been linked to the child displaying increased irritability
after experiencing frustration (Camacho et al., 2020).
Attention and learning. Attention and learning in
infants are closely related to parent-infant interbrain
synchrony (Wass et al., 2018; Zhao et al., 2021).
Research has shown that a stronger connection between
a child’s attention and their parents’ brain activity
increases the likelihood that the child will be more atten-
tive. Wass et al. (2018) observed that 12-month-old
infants paid more attention to toys when playing with their
mothers compared to when playing alone. Moreover,
when the mother’s EEG was monitored during the interac-
tion, it was found that her neural response was height-
ened when the child sustained attention for longer
periods. This suggests that parent-infant interbrain syn-
chrony plays a crucial role in enhancing attention and
learning in infants.
Interbrain synchrony serves as a mechanism for
learning from social partners in children (Bevilacqua
et al., 2019; Leong et al., 2019). In child-teacher interac-
tions, interbrain synchrony is associated with learning
success. Furthermore, interbrain synchrony during joint
play between mother and child has been linked to
enhanced learning in the child, starting from infancy.
Leong et al. (2019) demonstrated that 10-month-old
infants are more likely to learn during social interactions
with their mothers when interbrain synchrony is present
at central and parietal scalp locations. This evidence high-
lights the importance of interbrain synchrony between
children and their social partners in promoting learning
and development.
Cooperation. Synchrony during cooperation has
been positively associated with dyadic task
performance, as higher levels of interpersonal
synchrony are linked to better cooperative performance
(Cui et al., 2012; Cheng et al., 2015; Baker et al., 2016).
Interbrain synchrony increases during cooperation com-
pared to baseline, and is higher for mother–child dyads
than stranger-child dyads (Reindl et al., 2022). Similarly,
mother–child cooperation during a cooperative task may
enhance overall interbrain synchrony when compared to
a non-cooperative task (Miller et al., 2019). In a study of
father-child dyads, Nguyen et al. (2021) found increased
interbrain synchrony between the bilateral dorsolateral
prefrontal cortex (dlPFC) and the left temporo-parietal
junction (TPJ) when dyads completed a cooperative task
as opposed to an individual task. Ultimately, interbrain
synchrony has been shown to predict parent–child coop-
40 X. Bi et al. / Neuroscience 530 (2023) 38–45
erative performance, which can assist future studies in
examining different levels of cooperative behavior.
Problem-solving. Increased interbrain synchrony
has been shown to predict a dyad’s ability to solve
presented problems, with higher interbrain
synchronization being associated with successful joint
problem-solving (Nguyen, Banki, et al., 2020; Zhao
et al., 2023). The father-child and mother–child studies
found increased interbrain synchrony in prefrontal and
temporo-parietal regions during problem-solving com-
pared to individual (Nguyen, Banki, et al., 2020; Nguyen
et al., 2021). In other words, the more synchronized the
brain activity between parents and children, the more tan-
gram templates they solved in a tangram puzzle task.
So far, increased interbrain synchrony has been
linked to children’s positive emotions, enhanced
attention and learning abilities, better cooperative
performance, and problem-solving skills. This suggests
that interbrain synchrony could be a sensitive marker for
successful mutual attunement between parents and
their children.
DIFFERENCES IN SYNCHRONY BY FATHER
AND MOTHER ROLE
The traditional view that mothers are typically the first to
seek safety and comfort and act as the primary
caregivers in daily life is supported by contemporary
data (Umemura et al., 2013). However, traditional parent-
ing roles are changing. The latest U.S. Census data
shows that 7% of fathers do not work outside the home,
with 24% of these fathers reporting that they care for their
children (Livingston, 2018). Research has indicated that
fathers and mothers play distinct roles in parent–child
interactions. Fathers generally spend less time interacting
with their children and tend to engage in more physically
active and outdoor activities. In contrast, mothers usually
spend more time interacting with their children, participat-
ing in caregiving and domestic interactions (Oliveri et al.,
2018). As a result, fathers and mothers may play different
roles in their interactions with their children, reflecting the
ongoing changes in parenting interaction.
Meanwhile, the attachment specific hypothesis
suggests that children have unique experiences of
interaction with different caregivers, and the multiple
attachments formed have neither primary nor secondary
effects on children’s social and psychological development
(Bretherton, 2010). In other words, the effects of mother
and father attachment on children’s development are not
superimposed or combined, but have independent effects
(Cabrera et al., 2014; Oliveri et al., 2018).
Interbrain synchrony may also differ between father-
child and mother–child interactions (Davis et al., 2018;
Bell, 2020). Thus, examining the differences between
father-child and mother–child interactions may provide
new insights into the distinctions between father-mother
relationships. Additionally, understanding the variations
in brain activity patterns between mother–child and
father-child dyads could reveal their unique contributions
to child development.
Brain structure and activation pathways. When
parents are exposed to infant cues, such as crying,
specific brain regions become more active, and this
activity is associated with maternal psychopathology
and parenting behaviors(Feldman, 2015). Research has
shown that depressed mothers exhibit lower activation
in reward network regions in response to their infants
(Goodman et al., 2021). Furthermore, mothers who
engage in more sensitive parenting behaviors demon-
strate increased activation in reward network regions
when responding to their children (Goodman et al.,
2021). Lambert et al. (2011) found that active paternal
care increased the integration of brain networks in fathers
involved in nurturance, learning, and motivation. Previous
research comparing brain activation responses of moth-
ers and fathers revealed that mothers had greater amyg-
dala activation (Atzil et al., 2012; Carter, 2014), while
fathers had greater cortical activation (Abraham et al.,
2014), supporting the distinct pathway hypothesis. In
terms of functional connectivity, mothers who exhibited
more interactive synchrony with their children displayed
greater connectivity between the Nucleus Accumbens
(NAcc, reward circuit) and mentalizing, mirror, and empa-
thy networks, suggesting that reward motivation underlies
the conscious aspects of parenting (Atzil et al., 2012).
Additionally, a longitudinal study of mothers’ and fathers’
brains from the first to the fourth postnatal month found
that mothers’ gray-matter volume increased (amygdala,
hypothalamus, thalamus, and substantia nigra) (Kim
et al., 2010). However, the increase in gray matter volume
(amygdala, striatum, hypothalamus, subgenual cortex,
lateral prefrontal cortex, and superior temporal gyrus) in
fathers was different. This difference may contribute to
the variations in interbrain synchrony between father-
child and mother–child interactions (Kim et al., 2014).
Gender effects. Some research has reported gender
effects in parent–child interaction situations, suggesting
that father-child and mother–child dyads might display
different interbrain synchrony patterns (Cheng et al.,
2015; Azhari et al., 2021). For instance, positive father
role perceptions have been associated with increased
unique interbrain synchronization during cooperative
tasks and co-viewing video in the prefrontal cortex
(PFC) (Azhari et al., 2021; Nguyen et al., 2021). More
specifically, fathers’ involvement in child care has been
linked to their sensitivity in caregiving and subsequent
positive outcomes in child development (Flouri et al.,
2016; Cowan et al., 2019). In adolescent interactions with
mothers, Lee et al. (2015) discovered increased activation
in regions associated with emotional and social pain (the
lentiform nucleus and the posterior insula) and decreased
activation in regions associated with emotional regulation
and cognitive control (Dorsolateral Prefrontal Cortex and
Anterior Cingulate Cortex). Endevelt-Shapira and
Feldman (2023) research underscores the role of the
mother’s frontal brain regions and the infant’s temporal
regions in achieving interbrain synchrony during direct
communication. Their findings suggest that maternal sen-
sitivity enhances this synchrony, while maternal intrusive-
ness may reduce it. Moreover, the extended Parent–Child
X. Bi et al. / Neuroscience 530 (2023) 38–45 41
Emotion Regulation Dynamics Model proposes that there
are gender differences between children and parents,
including distinctions in father-daughter, mother-
daughter, father-son, and mother-son relationships, which
may influence cross-brain associations during parent–
child interactions (Ratliff et al., 2022).
Age differences. To investigate differences interbrain
synchronization between father-child and mother–child
interactions, we must consider age differences in the
findings on interpersonal synchrony and its role as a
mechanism for dynamic mutual adjustments of brain
activity. In the first year of life, mother–child interactions
(such as touching, gazing, singing, and vocalizing) are
more frequent than father-child interactions (Feldman,
2007). This is because infants experience synchrony
between their own physiology and behavior and the
mother’s body, physical presence, and sensory cues. Fur-
thermore, age-related changes have diverse effects on
the temporal and rhythmic characteristics of brain
responses (Dumas et al., 2011). For instance, from age
20 to age 80, the N400, an Event-Related Potentials
(ERP) component associated with semantic access,
demonstrates a progressive increase in latency of approx-
imately 1.5–2 ms per year (Kutas and Iragui, 1998;
Federmeier, 2022). This highlights that the influence of
aging on the timing of neural responses is complex and
varies with modality.
Personality traits. There is a correlation between
interbrain synchrony and personality traits such as
affective empathy and sensitivity (Cohen et al., 2017;
Parada and Rossi, 2017; Bevilacqua et al., 2019;
Czeszumski et al., 2020). Nguyen et al. (2021) showed
that variations in paternal neural synchronization could
be related to differences in the trait-like parenting attitude
of fathers. Furthermore, it was found that the sensitivity of
fathers in child care was associated with positive out-
comes in child development (Harrist and Waugh, 2002;
Leclere et al., 2014). However, females are generally con-
sidered more pro-social and moral (Heinla et al., 2020).
Openness and the need to belong were additional traits
where females scored higher (Vecchione et al., 2012).
OPTIMAL LEVEL OF PARENT–CHILD
INTERBRAIN SYNCHRONIZATION
Previous research has demonstrated that high levels of
interbrain synchrony are strongly associated with more
positive cognition and behavior. Based on existing
evidence, outcomes of neurobehavioral synchrony are
enhanced social connectedness, effective
communication as well as interpersonal regulation
(Feldman, 2007; Stephens et al., 2010; Leong et al.,
2017). However, whether there is an optimal level of par-
ent–child synchronization is a crucial question for the
research. An ‘‘optimum midrange model” of behavioral
contingency in parent–child interactions is supported by
a variety of empirical studies (Beebe et al., 2008; Beebe
and Steele, 2013). How can we increase interbrain syn-
chrony to promote parent–child behavior? Communica-
tion patterns, nonverbal behavior, music, and
multichannel stimulation have all been demonstrated to
increase synchronization between parents and children
(Table).
Conversational patterns. Family Systems Theory
has long held that family members function as a
relational unit and that a pattern of organized, flexible,
and positive exchanges between individuals in the
relational unit leads to optimal relational and emotional
health (Rothbaum et al., 2002; Haefner, 2014). For exam-
ple, Nozawa et al. (2016) found that social communication
enhanced interbrain synchrony in frontal areas is con-
nected with successful information sharing and coopera-
tive behavior using spoken language. Nguyen et al.
(2021, 2023) used fNIRS hyperscanning to explore the
temporal dynamics of interbrain synchrony during par-
ent–child conversations and found that frequent turns-
taking in conversation predicted a higher level of inter-
brain synchronization and later vocabulary size. These
studies of conversational synchrony indicated that con-
versation patterns, such as turn-taking, may support
cross-brain associations and emphasize the significance
of understanding dynamic emotion-related processes
and their relationship to psychological well-being during
parent–child social interactions.
Nonverbal behavior. Parent-child interbrain
synchrony is facilitated not only by verbal
communication but also by nonverbal activities such as
affective touch, eye contact and gaze, gestural mimicry,
and joint attention. First, affectionate touch serves as an
essential pathway for establishing and maintaining
parent–child interbrain synchrony at neural levels. In
terms of physical touch, the closer the distance between
parent and child, the stronger the connection they feel,
resulting in increased interbrain synchrony between
them (Carozza and Leong, 2021; Trinh et al., 2021). For
instance, mother–child dyads displayed increased inter-
brain synchrony in the prefrontal cortex when the child
was seated on the mother’s lap while watching videos.
One possible explanation for this effect is that proximity
may have promoted mutual entrainment through micro-
adjustments of bodily touch, as well as the perception of
heart rhythms and respiration (Wass et al., 2020). Sec-
ond, speaker eye contact and gaze enhance information
coupling between the brains of child and the parents.
Leong et al. (2017) discovered through empirical studies
that direct gaze enhances bidirectional parent-infant brain
connections. Third, gestural imitation and joint attention
both involve a partner with whom nonverbal interpersonal
contact is established. They serve as excellent ecological
models for the study of human social interaction.
Music. Music serves as a medium for social
interaction across various species. Evidence
demonstrates that music has played a crucial role in
fostering social connections among numerous species,
including humans. For instance, a recent parent–child
EEG study indicates that musical interventions can
enhance brain-to-brain connections between children
and their parents (Samadani et al., 2021). Furthermore,
Fachner et al. (2019) used the EEG hyperscanning
method to discover that classical music induced signifi-
cant interbrain synchronization between a music therapist
and client during sessions of Guided Imagery and Music
42 X. Bi et al. / Neuroscience 530 (2023) 38–45
(Fachner et al., 2019). Therefore, musical activities are
intimately connected to parent–child interbrain synchrony.
Multimodal stimulation. In addition to examining
each modality individually, combining modalities might
result in a more potent form of rhythm induction in
parent–child interactions (Levinson and Holler, 2014).
Adults frequently employ multiple modalities when engag-
ing with children, and these multimodal forms of stimula-
tion (such as joint attention, play, speech, and daily
routines) are more likely to enhance the interbrain syn-
chrony within the interaction compared to a single mode
of stimulation.
CONCLUSION AND FUTURE DIRECTIONS
Hyperscanning provides a new perspective into parent–
child interactions and the quality of early relationships
by capturing the dynamics and reciprocity of social
exchanges and involving parents and children as active
and engaged partners, as opposed to the passive
perception required by traditional neuroimaging
approaches. In this review, we first highlight the use of
hyperscanning techniques to simultaneously measure
dyadic brain activity in dynamic parent–child interactions
in order to reveal differences in interbrain synchrony as
well as mother–child and father-child interactions,
especially in infancy, to provide a deeper understanding
of the link between body and brain (Markova et al.,
2019). Moreover, by summarizing the important factors
influencing the interbrain synchrony between parents
and children, we propose ways to promote interbrain syn-
chrony. These findings, when taken as a whole, suggest
that interpersonal neural synchrony may serve as a useful
neural marker for mutual engagement in social interac-
tions between parents and children that rely on both par-
ties being responsive and attentive to one another. This
summary may be useful for expanding researchers’ and
practitioners’ understanding of the ways in which parent-
ing and the parent–child relationship shape children’
brains. Similarly, neurofeedback and parent training
methods could be developed so that adults and children
could see the effects of their interactions on each other’s
brain activity in real time.
Hyperscanning has greater potential for future studies
of the interpersonal neural dynamics of natural parent–
child interactions, and we can conduct more studies.
Firstly, we do not know what is normal or how
synchrony between parent and child develops, and to
explain these issues, a longitudinal design as a potential
approach in future studies to investigate how the
relationship between parent–child relationships and
interbrain synchrony accompanies children’s brain
development and maturation during parent–child
interactions is required. Secondly, previous research
has focused on more mother–child interactions, with
relatively few studies on father-child interactions, and no
detailed studies of mother-son, mother-daughter, or
father-son and father-daughter by gender. Further
research may focus on detailed gender distinctions.
Furthermore, mother-father-child triads could also be
considered, or even multi-person dynamics interactions
between caregivers and several siblings could be
studied. Finally, it is unclear whether and how exactly
behavioral and physiological synchronization between
parents and children is related to neural
synchronization, therefore, future research could use
multimodal simultaneous assessment of synchrony in
parent–child interactions.
CONFLICT OF INTEREST
The authors declare that the research was conducted in
the absence of any real or perceived conflicts of interest.
ACKNOWLEDGMENTS
This study was supported by the China School of
Education in Guangzhou University.
This research was supported by the National Natural
Science Foundation of China (31100734); 2023 Positive
Psychology Project of Guangdong Happiness Positive
Psychology Research Institution (XF230009).
REFERENCES
Abraham E, Hendler T, Shapira-Lichter I, Kanat-Maymon Y, Zagoory-
Sharon O, Feldman R (2014) Father’s brain is sensitive to
childcare experiences. Psychological and Cognitive Sciences 111
(27):9792–9797. https://doi.org/10.1073/pnas.1402569111.
Abulizi X, Pryor L, Michel G, Melchior M, van der Waerden J (2017)
Temperament in infancy and behavioral and emotional problems
at age 5.5: The EDEN mother-child cohort. PLoS One 12(2).
https://doi.org/10.1371/journal.pone.0171971.
Atzaba-Poria N, Deater-Deckard K, Bell MA (2017) Mother-child
interaction: links between mother and child frontal
electroencephalograph asymmetry and negative behavior. Child
Dev 88(2):544–554. https://doi.org/10.1111/cdev.12583.
Atzil S, Hendler T, Zagoory-Sharon O, Winetraub Y, Feldman R
(2012) Synchrony and specificity in the maternal and the paternal
brain: relations to oxytocin and vasopressin. J Am Acad Child
Adolesc Psychiatry 51(8):798–811. https://doi.org/10.1016/
j.jaac.2012.06.008.
Azhari A, Bizzego A, Esposito G (2021) Father-child dyads exhibit
unique inter-subject synchronization during co-viewing of
animation video stimuli. Soc Neurosci 16(5):522–533. https://
doi.org/10.1080/17470919.2021.1970016.
Baker JM, Liu N, Cui X, Vrticka P, Saggar M, Hosseini SM, Reiss AL
(2016) Sex differences in neural and behavioral signatures of
cooperation revealed by fNIRS hyperscanning. Sci Rep 6:26492.
https://doi.org/10.1038/srep26492.
Beebe B, Jaffe J, Buck K, Chen H, Cohen P, Feldstein S, Andrews H
(2008) Six-week postpartum maternal depressive symptoms and
4-month mother-infant self- and interactive contingency. Infant
Ment Health J 29(5):442–471. https://doi.org/10.1002/imhj.20191.
Beebe B, Steele M (2013) How does microanalysis of mother-infant
communication inform maternal sensitivity and infant attachment?
Attach Hum Dev 15(5–6):583–602. https://doi.org/10.1080/
14616734.2013.841050.
Begus K, Gliga T, Southgate V (2014) Infants learn what they want to
learn: responding to infant pointing leads to superior learning.
PLoS One 9(10). https://doi.org/10.1371/journal.pone.0108817.
Bell MA (2020) Mother-child behavioral and physiological synchrony.
In: Benson JB, editor. Adv Child Dev Behav. JAI. p. 163–188.
Available from: https://doi.org/10.1016/bs.acdb.2020.01.006.
Bevilacqua D, Davidesco I, Wan L, Chaloner K, Rowland J, Ding M,
Dikker S (2019) Brain-to-brain synchrony and learning outcomes
vary by student-teacher dynamics: evidence from a real-world
classroom electroencephalography study. J Cogn Neurosci 31
(3):401–411. https://doi.org/10.1162/jocn_a_01274.
X. Bi et al. / Neuroscience 530 (2023) 38–45 43
Bretherton I (2010) Parental incarceration: the challenges for
attachment researchers. Attachment Human Develop 12
(4):417–428. https://doi.org/10.1080/14616730903417136.
Cabrera NJ, Fitzgerald HE, Bradley RH, Roggman L (2014) The
ecology of father-child relationships: an expanded model. J Fam
Theory Rev 6(4):336–354. https://doi.org/10.1111/jftr.12054.
Camacho MC, Quin˜ ones-Camacho LE, Perlman SB (2020) Does the
child brain rest?: An examination and interpretation of resting
cognition in developmental cognitive neuroscience. Neuroimage
212. https://doi.org/10.1016/j.neuroimage.2020.116688 116688.
Carollo A, Lim M, Aryadoust V, Esposito G (2021) Interpersonal
synchrony in the context of caregiver-child interactions: a
document co-citation. Analysis [Systematic Review]. 12. https://
doi.org/10.3389/fpsyg.2021.701824.
Carozza S, Leong V (2021) The role of affectionate caregiver touch in
early neurodevelopment and parent–infant interactional
synchrony. Front Neurosci 1392.
Carter CS (2014) Oxytocin pathways and the evolution of human
behavior. Annu Rev Psychol 66(65):17–39. https://doi.org/
10.1146/010213-115110.
Cheng X, Li X, Hu Y (2015) Synchronous brain activity during
cooperative exchange depends on gender of partner: a fNIRS-
based hyperscanning study. Hum Brain Mapp 36(6):2039–2048.
https://doi.org/10.1002/hbm.22754.
Cohen SS, Henin S, Parra LC (2017) Engaging narratives evoke
similar neural activity and lead to similar time perception. Sci Rep
7(1):4578.
Cowan PA, Cowan CP, Pruett MK, Pruett K (2019) Fathers’ and
mothers’ attachment styles, couple conflict, parenting quality, and
children’s behavior problems: an intervention test of mediation.
Attach Hum Dev 21(5):532–550. https://doi.org/10.1080/
14616734.2019.1582600.
Cui X, Bryant DM, Reiss AL (2012) NIRS-based hyperscanning
reveals increased interpersonal coherence in superior frontal
cortex during cooperation. Neuroimage 59(3):2430–2437. https://
doi.org/10.1016/2011.09.003.
Czeszumski A, Eustergerling S, Lang A, Menrath D, Gerstenberger
M, Schuberth S, Koenig P (2020) Hyperscanning: a valid method
to study neural inter-brain underpinnings of social interaction.
Front Hum Neurosci 14. https://doi.org/10.3389/2020.00039 39.
Davis M, West K, Bilms J, Morelen D, Suveg C (2018) A systematic
review of parent-child synchrony: it is more than skin deep. Dev
Psychobiol 60(6):674–691. https://doi.org/10.1002/dev.21743.
De Jaegher H, Di Paolo E, Adolphs R (2016) What does the
interactive brain hypothesis mean for social neuroscience? A
dialogue. Philos Trans R Soc B-Biol Sci 371(1693):20150379.
https://doi.org/10.1098/rstb.2015.0379.
Diaz A, Swingler MM, Tan L, Smith CL, Calkins SD, Bell MA (2019)
Infant frontal EEG asymmetry moderates the association between
maternal behavior and toddler negative affectivity. Infant Behav
Dev 55:88–99. https://doi.org/10.1016/j.infbeh.2019.03.002.
Djalovski A, Dumas G, Kinreich S, Feldman R (2021) Human
attachments shape interbrain synchrony toward efficient
performance of social goals. Neuroimage 226. Available from:
10.1016/j.neuroimage.2020.117600 117600.
Dumas G, Lachat F, Martinerie J, Nadel J, George N (2011) From
social behaviour to brain synchronization: review and
perspectives in hyperscanning. IRBM 32(1):48–53. Available
from: 10.1016/j.irbm.2011.01.002.
Eisenberg N, Spinrad TL, Eggum ND (2010) Emotion-related self-
regulation and its relation to children’s maladjustment. In Annual
review of clinical psychology, vol. 6 (NolenHoeksema S, Cannon
TD, Widiger T, eds.), pp. 495–525. https://doi.org/10.1146/
annurev.clinpsy.121208.131208.
Endevelt-Shapira Y, Feldman R (2023) Mother-infant brain-to-brain
synchrony patterns reflect caregiving profiles. Biology (Basel) 12
(2). https://doi.org/10.3390/biology12020284.
Fachner JC, Maidhof C, Grocke D, Nygaard Pedersen I, Trondalen
G, Tucek G, Bonde LO (2019) ‘‘Telling me not to worry...”
hyperscanning and neural dynamics of emotion processing during
guided imagery and music. Front Psychol 10:1561. https://doi.org/
10.3389/fpsyg.2019.01561.
Federmeier KD (2022) Connecting and considering:
electrophysiology provides insights into comprehension.
Psychophysiology 59(1). https://doi.org/10.1111/psyp.13940.
Feldman R (2007) Parent-infant synchrony and the construction of
shared timing; physiological precursors, developmental
outcomes, and risk conditions. J Child Psychol Psychiatry 48(3–
4):329–354. https://doi.org/10.1111/j.1469-7610.2006.01701.x.
Feldman R (2015) The adaptive human parental brain: implications
for children’s social development. Trends Neurosci 38
(6):387–399. https://doi.org/10.1016/j.tins.2015.04.004.
Feldman R (2017) The neurobiology of human attachments. Trends
Cogn Sci 21(2):80–99.
Finn ES, Glerean E, Khojandi AY, Nielson D, Molfese PJ,
Handwerker DA, Bandettini PAJN (2020) Idiosynchrony: from
shared responses to individual differences during naturalistic
neuroimaging. NeuroImage 215 116828.
Flouri E, Midouhas E, Narayanan MK (2016) The relationship
between father involvement and child problem behaviour in
intact families: a 7-year cross-lagged study. J Abnorm Child
Psychol 44(5):1011–1021. https://doi.org/10.1007/s10802-015-
0077-9.
Goodman SH, Liu R, Lusby CM, Park JS, Bell MA, Newport DJ,
Stowe ZN (2021) Consistency of EEG asymmetry patterns in
infants of depressed mothers. Dev Psychobiol 63(4):768–781.
https://doi.org/10.1002/dev.22046.
Haefner J (2014) An application of Bowen family systems theory.
Issues Ment Health Nurs 35(11):835–841. https://doi.org/10.3109/
01612840.2014.921257.
Hamilton AFD (2021) Hyperscanning: beyond the Hype. Neuron 109
(3):404–407. https://doi.org/10.1016/j.neuron.2020.11.008.
Harrist AW, Waugh RM (2002) Dyadic synchrony: its structure and
function in children’s development. Develop Rev 4:555–592.
Heinla I, Heijkoop R, Houwing DJ, Olivier JDA, Snoeren EMS (2020)
Third-party prosocial behavior in adult female rats is impaired
after perinatal fluoxetine exposure. Physiol Behav 222. https://doi.
org/10.1016/j.physbeh.2020.112899 112899.
Kim P, Leckman JF, Mayes LC, Feldman R, Wang X, Swain JE
(2010) The plasticity of human maternal brain: longitudinal
changes in brain anatomy during the early postpartum period.
Behav Neurosci 124(5):695–700. https://doi.org/10.1037/
a0020884.
Kim P, Rigo P, Mayes LC, Feldman R, Leckman JF, Swain JE (2014)
Neural plasticity in fathers of human infants. Soc Neurosci 9
(5):522–535. https://doi.org/10.1080/17470919.2014.933713.
Knauer HA, Ozer EJ, Dow WH, Fernald LCH (2019) Parenting quality
at two developmental periods in early childhood and their
association with child development. Early Child Res Q
47:396–404. https://doi.org/10.1016/j.ecresq.2018.08.009.
Kuhl PK, Tsao FM, Liu HM (2003) Foreign-language experience in
infancy: effects of short-term exposure and social interaction on
phonetic learning. PNAS 100(15):9096–9101. https://doi.org/
10.1073/pnas.1532872100.
Kutas M, Iragui V (1998) The N400 in a semantic categorization task
across 6 decades. Electroencephalogr Clin Neurophysiol 108
(5):456–471. https://doi.org/10.1016/s0168-5597(98)00023-9.
Leclere C, Viaux S, Avril M, Achard C, Chetouani M, Missonnier S,
Cohen D (2014) Why synchrony matters during mother-child
interactions: a systematic review. Plos One 9(12). https://doi.org/
10.1371/journal.pone.0113571.
Lee KH, Siegle GJ, Dahl RE, Hooley JM, Silk JS (2015) Neural
responses to maternal criticism in healthy youth. Soc Cogn Affect
Neurosci 10(7):902–912. https://doi.org/10.1093/scan/nsu133.
Lee T-H, Miernicki ME, Telzer EH (2017) Families that fire together
smile together: Resting state connectome similarity and daily
emotional synchrony in parent-child dyads. Neuroimage
152:31–37. Available from: 10.1016/j.neuroimage.2017.02.078.
Leong V, Byrne E, Clackson K, Georgieva S, Lam S, Wass S (2017)
Speaker gaze increases information coupling between infant and
44 X. Bi et al. / Neuroscience 530 (2023) 38–45
adult brains. PNAS 114(50):13290–13295. https://doi.org/
10.1073/pnas.1702493114.
Leong V, Noreika V, Clackson K, Georgieva, S, Brightman L,
Nutbrown R, Wass S (2019) Mother-infant interpersonal neural
connectivity predicts infants’ social learning.
Levinson SC, Holler J (2014) The origin of human multi-modal
communication. Philos Trans R Soc Lond B Biol Sci 369
(1651):20130302. https://doi.org/10.1098/rstb.2013.0302.
Markova G, Trinh N, Hoehl S (2019) Neurobehavioral interpersonal
synchrony in early development: the role of interactional rhythms.
Front Psychol 10:2078. https://doi.org/10.3389/
fpsyg.2019.02078.
Miller JG, Vrtic
ˇka P, Cui X, Shrestha S, Hosseini SMH, Baker JM,
Reiss AL (2019) Inter-brain synchrony in mother-child dyads
during cooperation: An fNIRS hyperscanning study.
Neuropsychologia 124:117–124. https://doi.org/10.1016/j.
neuropsychologia.2018.12.021.
Nguyen T, Banki A, Markova G, Hoehl S (2020) Studying parent-child
interaction with hyperscanning. In: New perspectives on early
social-cognitive development, vol. 254 (Hunnius S, Meyer M,
eds.), pp. 1–24. https://doi.org/10.1016/bs.pbr.2020.05.003
Nguyen T, Schleihauf H, Kayhan E, Matthes D, Vrticka P, Hoehl S
(2021) Neural synchrony in mother-child conversation: exploring
the role of conversation patterns. Soc Cogn Affect Neurosci 16(1–
2):93–102. https://doi.org/10.1093/scan/nsaa079.
Nguyen T, Schleihauf H, Kayhan E, Matthes D, Vrtic
ˇka P, Hoehl S
(2020) The effects of interaction quality on neural synchrony
during mother-child problem solving. Cortex 124:235–249.
Available from: 10.1016/j.cortex.2019.11.020.
Nguyen T, Zimmer L, Hoehl S (2023) Your turn, my turn. Neural
synchrony in mother-infant proto-conversation. Philos Trans R
Soc Lond B Biol Sci 378(1875):20210488. https://doi.org/10.1098/
rstb.2021.0488.
Nozawa T, Sasaki Y, Sakaki K, Yokoyama R, Kawashima R (2016)
Interpersonal frontopolar neural synchronization in group
communication: an exploration toward fNIRS hyperscanning of
natural interactions. Neuroimage 133:484–497. https://doi.org/
10.1016/j.neuroimage.2016.03.059.
Ogilvie D, Adams J, Bauman A, Gregg EW, Panter J, Siegel KR,
White M (2020) Using natural experimental studies to guide public
health action: turning the evidence-based medicine paradigm on
its head. J Epidemiol Community Health 74(2):203–208.
Oliveri AN, Ortiz E, Levin ED (2018) Developmental exposure to an
organophosphate flame retardant alters later behavioral
responses to dopamine antagonism in zebrafish larvae.
Neurotoxicol Teratol 67:25–30. https://doi.org/10.1016/j.
ntt.2018.03.002.
Parada FJ, Rossi A (2017) Commentary: brain-to-brain synchrony
tracks real-world dynamic group interactions in the classroom and
cognitive neuroscience: synchronizing brains in the classroom.
Front Hum Neurosci 11. https://doi.org/10.3389/
fnhum.2017.00554 554.
Perone S, Gartstein MA, Anderson AJ (2020) Dynamics of frontal
alpha asymmetry in mother-infant dyads: Insights from the Still
Face Paradigm. Infant Behav Dev 61. https://doi.org/10.1016/j.
infbeh.2020.101500 101500.
Ratliff EL (2019) The role of cross-brain connectivity in emotion
regulation within the parent-adolescent dyad Oklahoma. State
University.
Ratliff EL, Kerr KL, Cosgrove KT, Simmons WK, Morris AS (2022)
The role of neurobiological bases of dyadic emotion regulation in
the development of psychopathology: cross-brain associations
between parents and children. Clin Child Fam Psychol Rev 25
(1):5–18. https://doi.org/10.1007/s10567-022-00380-w.
Ratliff EL, Kerr KL, Misaki M, Cosgrove KT, Moore AJ, DeVille DC,
Morris AS (2021) Into the unknown: examining neural
representations of parent-adolescent interactions. Child Dev 92
(6):E1361–E1376. https://doi.org/10.1111/cdev.13635.
Reindl V, Gerloff C, Scharke W, Konrad K (2018) Brain-to-brain
synchrony in parent-child dyads and the relationship with emotion
regulation revealed by fNIRS-based hyperscanning. Neuroimage
178:493–502. https://doi.org/10.1016/j.neuroimage.2018.05.060.
Reindl V, Wass S, Leong V, Scharke W, Wistuba S, Wirth CL, Gerloff
C (2022) Multimodal hyperscanning reveals that synchrony of
body and mind are distinct in mother-child dyads. Neuroimage
251. https://doi.org/10.1016/j.neuroimage.2022.118982 118982.
Roque TR, Rajagopalan N, Jain S, Mehdizadeh SK, Leslie G (2022)
Multimodal, musical hyperscanning to promote empathy in HCI.
Rothbaum F, Rosen K, Ujiie T, Uchida N (2002) Family systems
theory, attachment theory, and culture. Fam Process 41
(3):328–350. https://doi.org/10.1111/j.1545-5300.2002.41305.x.
Samadani A, Kim S, Moon J, Kang K, Chau T (2021)
Neurophysiological synchrony between children with severe
physical disabilities and their parents during music therapy
[original research]. 15.https://doi.org/10.3389/fnins.2021.531915
Simony E, Chang C (2020) Analysis of stimulus-induced brain
dynamics during naturalistic paradigms. Neuroimage 216.
Available from: 10.1016/j.neuroimage.2019.116461 116461.
Stephens GJ, Silbert LJ, Hasson U (2010) Speaker-listener neural
coupling underlies successful communication. PNAS 107
(32):14425–14430. https://doi.org/10.1073/pnas.1008662107.
Su H, Young CB, Han ZR, Xu J, Xiong B, Wang J, Qin S (2022)
Medial prefrontal-hippocampal concordance in child-parent dyads
underlies children’s psychological wellbeing. bioRxiv.
Trinh N, Abney DH, Salamander D, Bertenthal BI, Hoehl S (2021)
Proximity and touch are associated with neural but not
physiological synchrony in naturalistic mother-infant interactions.
Neuroimage 244. https://doi.org/10.1016/j.
neuroimage.2021.118599 118599.
Turk E, Vroomen J, Fonken Y, Levy J, van den Heuvel M (2022) In
sync with your child: The potential of parent–child
electroencephalography in developmental research. Dev
Psychobiol 64(3).
Umemura T, Jacobvitz D, Messina S, Hazen N (2013) Do toddlers
prefer the primary caregiver or the parent with whom they feel
more secure? The role of toddler emotion. Infant Behav Dev 36
(1):102–114. https://doi.org/10.1016/j.infbeh.2012.10.003.
Vecchione M, Alessandri G, Barbaranelli C, Caprara G (2012)
Gender differences in the Big Five personality development: a
longitudinal investigation from late adolescence to emerging
adulthood. Personal Individual Differen 53(6):740–746.
Wass S, Haresign IM, Whitehorn M, Clackson K, Georgieva S,
Noreika V, Leong V (2020) Parental frontal brain activity tracks
infants’ attention during shared play.
Wass S, Whitehorn M, Phillips E, Haresign IM, Leong V (2019)
Interpersonal neural synchrony and responsivity during early
learning interactions.
Wass SV, Noreika V, Georgieva S, Clackson K, Brightman L,
Nutbrown R, Leong V (2018) Parental neural responsivity to
infants’ visual attention: How mature brains influence immature
brains during social interaction. PLoS Biol 16(12). https://doi.org/
10.1371/journal.pbio.2006328 e2006328.
Wong NML, Yeung PPS, Lee TMC (2018) A developmental social
neuroscience model for understanding loneliness in adolescence.
Soc Neurosci 13(1):94–103. https://doi.org/10.1080/
17470919.2016.1256832.
Zhao H, Cheng T, Zhai Y, Long Y, Wang Z, Lu C (2021) How mother-
child interactions are associated with a child’s compliance. Cereb
Cortex 31(9):4398–4410. https://doi.org/10.1093/cercor/bhab094.
Zhao H, Zhang T, Cheng T, Chen C, Zhai Y, Liang X, Lu C (2023)
Neurocomputational mechanisms of young children’s
observational learning of delayed gratification. Cereb Cortex 33
(10):6063–6076. https://doi.org/10.1093/cercor/bhac484.
(Received 27 April 2023, Accepted 27 August 2023)
(Available online 30 August 2023)
X. Bi et al. / Neuroscience 530 (2023) 38–45 45
