Why behaviour matters: Studying inter-brain coordination during child-caregiver interaction.

Modern technology allows for simultaneous neuroimaging from interacting caregiver-child dyads. Whereas most analyses that examine the coordination between brain regions within an individual brain do so by measuring changes relative to observed events, studies that examine coordination between two interacting brains generally do this by measuring average intra-brain coordination across entire blocks or experimental conditions. In other words, they do not examine changes in inter-brain coordination relative to individual behavioural events. Here, we discuss the limitations of this approach. First, we present data suggesting that fine-grained temporal interdependencies in behaviour can leave residual artifact in neuroimaging data. We show how artifact can manifest as both power and (through that) phase synchrony effects in EEG and affect wavelet transform coherence in fNIRS analyses. Second, we discuss different possible mechanistic explanations of how inter-brain coordination is established and maintained. We argue that non-event-locked approaches struggle to differentiate between them. Instead, we contend that approaches which examine how interpersonal dynamics change around behavioural events have better potential for addressing possible artifactual confounds and for teasing apart the overlapping mechanisms that drive changes in inter-brain coordination.

Annual Research Review: 'There, the dance is - at the still point of the turning world' - dynamic systems perspectives on coregulation and dysregulation during early development.

During development we transition from coregulation (where regulatory processes are shared between child and caregiver) to self-regulation. Most early coregulatory interactions aim to manage fluctuations in the infant's arousal and alertness; but over time, coregulatory processes become progressively elaborated to encompass other functions such as sociocommunicative development, attention and executive control. The fundamental aim of coregulation is to help maintain an optimal 'critical state' between hypo- and hyperactivity. Here, we present a dynamic framework for understanding child-caregiver coregulatory interactions in the context of psychopathology. Early coregulatory processes involve both passive entrainment, through which a child's state entrains to the caregiver's, and active contingent responsiveness, through which the caregiver changes their behaviour in response to behaviours from the child. Similar principles, of interactive but asymmetric contingency, drive joint attention and the maintenance of epistemic states as well as arousal/alertness, emotion regulation and sociocommunicative development. We describe three ways in which active child-caregiver regulation can develop atypically, in conditions such as Autism, ADHD, anxiety and depression. The most well-known of these is insufficient contingent responsiveness, leading to reduced synchrony, which has been shown across a range of modalities in different disorders, and which is the target of most current interventions. We also present evidence that excessive contingent responsiveness and excessive synchrony can develop in some circumstances. And we show that positive feedback interactions can develop, which are contingent but mutually amplificatory child-caregiver interactions that drive the child further from their critical state. We discuss implications of these findings for future intervention research, and directions for future work.

Comparative strengths and challenges on face-to-face and computer-based attention tasks in autistic and neurotypical toddlers.

The objectives were to compare patterns of visual attention in toddlers diagnosed with autism spectrum disorder (ASD) as compared to their sex- and age-matched neurotypical (NT) peers. Participants included 23 toddlers with ASD and 19 NT toddlers (mean age: 25.52 versus 25.21 months, respectively) assessed using computerized tasks to measure sustained attention, disengaging attention, and cognitive control, as well as an in-person task to assess joint attention. Toddlers in the ASD group showed increased looking durations on the sustained attention task, as well as reduced frequencies of responding to and initiating joint attention compared to NT peers, but showed no differences on tasks of disengaging attention and cognitive control. The results suggest that toddlers with ASD have attentional strengths that may provide a foundation for building attention, communicative, and ultimately, academic skills.

Proactive or reactive? Neural oscillatory insight into the leader-follower dynamics of early infant-caregiver interaction.

We know that infants' ability to coordinate attention with others toward the end of the first year is fundamental to language acquisition and social cognition. Yet, we understand little about the neural and cognitive mechanisms driving infant attention in shared interaction: do infants play a proactive role in creating episodes of joint attention? Recording electroencephalography (EEG) from 12-mo-old infants while they engaged in table-top play with their caregiver, we examined the communicative behaviors and neural activity preceding and following infant- vs. adult-led joint attention. Infant-led episodes of joint attention appeared largely reactive: they were not associated with increased theta power, a neural marker of endogenously driven attention, and infants did not increase their ostensive signals before the initiation. Infants were, however, sensitive to whether their initiations were responded to. When caregivers joined their attentional focus, infants showed increased alpha suppression, a pattern of neural activity associated with predictive processing. Our results suggest that at 10 to 12 mo, infants are not routinely proactive in creating joint attention episodes yet. They do, however, anticipate behavioral contingency, a potentially foundational mechanism for the emergence of intentional communication.

Parent-infant affect synchrony during social and solo play.

While mother-infant affect synchrony has been proposed to facilitate the early development of social understanding, most investigations into affect synchrony have concentrated more on negative than positive affect. We analysed affect sharing during parent-infant object play, comparing positive and negative affect, to examine how it is modulated by shared playful activity. Mother-infant dyads (N = 20, average infant age 10.7 months) played together (social) or separately (solo) using an object. Both participants increased positive affect during social play as compared with solo play. Positive affect synchrony also increased during social play compared with solo play, whereas negative affect synchrony did not differ. Closer examination of the temporal dynamics of affect changes showed that infants' shifts to positive affect tended to occur contingently in response to their mothers', whereas mothers' shifts to negative affect followed their infants'. Further, during social play, positive affect displays were more long-lived while negative more short-lived. While our sample was small and from a homogeneous population (e.g. white, highly educated parents), limiting the implications of the findings, these results demonstrate that maternal active engagement in playful interaction with her infant affords, increases, and extends infant positive affect and parent-infant positive affect synchrony, providing insights into how the social context modulates infants' affective experiences. This article is part of a discussion meeting issue 'Face2face: advancing the science of social interaction'.

Editorial perspective: Leaving the baby in the bathwater in neurodevelopmental research.

Neurodevelopmental conditions are characterised by differences in the way children interact with the people and environments around them. Despite extensive investigation, attempts to uncover the brain mechanisms that underpin neurodevelopmental conditions have yet to yield any translatable insights. We contend that one key reason is that psychologists and cognitive neuroscientists study brain function by taking children away from their environment, into a controlled lab setting. Here, we discuss recent research that has aimed to take a different approach, moving away from experimental control through isolation and stimulus manipulation, and towards approaches that embrace the measurement and targeted interrogation of naturalistic, user-defined and complex, multivariate datasets. We review three worked examples (of stress processing, early activity level in ADHD and social brain development in autism) to illustrate how these new approaches might lead to new conceptual and translatable insights into neurodevelopment.

Vocalization and physiological hyperarousal in infant-caregiver dyads where the caregiver has elevated anxiety.

Co-regulation of physiological arousal within the caregiver-child dyad precedes later self-regulation within the individual. Despite the importance of unimpaired self-regulatory development for later adjustment outcomes, little is understood about how early co-regulatory processes can become dysregulated during early life. Aspects of caregiver behavior, such as patterns of anxious speech, may be one factor influencing infant arousal dysregulation. To address this, we made day-long, naturalistic biobehavioral recordings in home settings in caregiver-infant dyads using wearable autonomic devices and miniature microphones. We examined the association between arousal, vocalization intensity, and caregiver anxiety. We found that moments of high physiological arousal in infants were more likely to be accompanied by high caregiver arousal when caregivers had high self-reported trait anxiety. Anxious caregivers were also more likely to vocalize intensely at states of high arousal and produce intense vocalizations that occurred in clusters. High-intensity vocalizations were associated with more sustained increases in autonomic arousal for both anxious caregivers and their infants. Findings indicate that caregiver vocal behavior differs in anxious parents, cooccurs with dyadic arousal dysregulation, and could contribute to physiological arousal transmission. Implications for caregiver vocalization as an intervention target are discussed.

Inhibitory deficits and symptoms of attention-deficit hyperactivity disorder: How are they related to effortful control?

Separate studies with clinical and community-based samples have identified an association between symptoms of attention-deficit hyperactivity disorder (ADHD) and inhibitory control deficits and ADHD and weak effortful control. We tested whether differences in effortful control explained the associations between ADHD symptoms and inhibitory control deficits, controlling for conduct problems. In a community sample, parents rated ADHD symptoms, conduct problems, effortful control, surgency and negative affect in 77 4-7-year-olds (47 girls), who performed an inhibitory control task. ADHD symptoms, deficient inhibitory control and low effortful control were correlated. Controlling for conduct problems, path analysis showed the ADHD symptoms - inhibitory control link was mediated statistically by effortful control. This focuses attention on cognitive-energetic factors associated with ADHD-related executive deficits.

Vocal communication is tied to interpersonal arousal coupling in caregiver-infant dyads.

It has been argued that a necessary condition for the emergence of speech in humans is the ability to vocalise irrespective of underlying affective states, but when and how this happens during development remains unclear. To examine this, we used wearable microphones and autonomic sensors to collect multimodal naturalistic datasets from 12-month-olds and their caregivers. We observed that, across the day, clusters of vocalisations occur during elevated infant and caregiver arousal. This relationship is stronger in infants than caregivers: caregivers vocalisations show greater decoupling with their own states of arousal, and their vocal production is more influenced by the infant's arousal than their own. Different types of vocalisation elicit different patterns of change across the dyad. Cries occur following reduced infant arousal stability and lead to increased child-caregiver arousal coupling, and decreased infant arousal. Speech-like vocalisations also occur at elevated arousal, but lead to longer-lasting increases in arousal, and elicit more parental verbal responses. Our results suggest that: 12-month-old infants' vocalisations are strongly contingent on their arousal state (for both cries and speech-like vocalisations), whereas adults' vocalisations are more flexibly tied to their own arousal; that cries and speech-like vocalisations alter the intra-dyadic dynamics of arousal in different ways, which may be an important factor driving speech development; and that this selection mechanism which drives vocal development is anchored in our stress physiology.

Attention and social communication skills of very preterm infants after training attention control: Bayesian analyses of a feasibility study.

BACKGROUND: Very preterm (VP) infants (born 28 to <32 weeks of gestation) are at risk of cognitive delays and lower educational attainments. These risks are linked to anomalies in attention and information processing that emerge in the first years of life. Early interventions targeting attention functioning may equip VP infants with key building blocks for later attainments. METHODS: We tested the feasibility of a randomised trial where VP infants took part in a computerised cognitive procedure to train attention control. Ten healthy VP infants aged approximately 12 months (corrected age) and randomly allocated with 1:1 ratio to the training (interactive computerised presentations) or an active control procedure completed the study. Before and after the training programme, participating infants completed a battery of screen-based attention tests, naturalistic attention and communication tasks, and temperament assessments. In a previous study we analysed the data concerning feasibility (e.g. recruitment and retention). In the paper presented here we considered the infants' performance and used Bayesian regression in order to provide credible treatment estimates considering the data collected. RESULTS: Estimates indicate moderate treatment effects in visual memory: compared to controls, trained infants displayed improvements equivalent to 0.59 SD units. Trained infants also improved in their abilities to attend to less salient stimuli presentations by 0.82 SD units, compared to controls. However, results did not indicate relevant gains in attention habituation or disengagement. We also reported moderate improvements in focused attention during naturalistic tasks, and in directing other people's attention to shared objects. DISCUSSION: The results warrant further investigation concerning the effectiveness of training attention control in VP infants, extending this line of research beyond our small and homogeneous sample of healthy VP infants. This study also emphasises the utility of Bayesian approaches in estimating potentially relevant effects in small samples or exploratory studies. The scope for further research on early attention control training is discussed in light of studies indicating VP children's susceptibility to positive environmental inputs. TRIAL REGISTRATION: Registration ID: NCT03896490. Retrospectively registered at Clinical Trials Protocol Registration and Results System (clinicaltrials.gov).

Studying the Developing Brain in Real-World Contexts: Moving From Castles in the Air to Castles on the Ground.

Most current research in cognitive neuroscience uses standardized non-ecological experiments to study the developing brain. But these approaches do a poor job of mimicking the real-world, and thus can only provide a distorted picture of how cognitive operations and brain development unfold outside of the lab. Here we consider future research avenues which may lead to a better appreciation of how developing brains dynamically interact with a complex real-world environment, and how cognition develops over time. We raise several problems faced by current mainstream methods in the field, before briefly reviewing novel promising approaches that alleviate some of these issues. First, we consider research that examines perception by measuring entrainment between brain activity and temporal patterns in naturalistic stimuli. Second, we consider research that examines our ability to parse our continuous experience into discrete events, and how this ability develops over time. Third, we consider the role of children as active agents in selecting what they sample from the environment from one moment to the next. Fourth, we consider new approaches that measure how mutual influences between children and others are instantiated in suprapersonal brain networks. Finally, we discuss how we may reduce adult biases when designing developmental studies. Together, these approaches have great potential to further our understanding of how the developing brain learns to process information, and to control complex real-world behaviors.

DEEP: A dual EEG pipeline for developmental hyperscanning studies.

Cutting-edge hyperscanning methods led to a paradigm shift in social neuroscience. It allowed researchers to measure dynamic mutual alignment of neural processes between two or more individuals in naturalistic contexts. The ever-growing interest in hyperscanning research calls for the development of transparent and validated data analysis methods to further advance the field. We have developed and tested a dual electroencephalography (EEG) analysis pipeline, namely DEEP. Following the preprocessing of the data, DEEP allows users to calculate Phase Locking Values (PLVs) and cross-frequency PLVs as indices of inter-brain phase alignment of dyads as well as time-frequency responses and EEG power for each participant. The pipeline also includes scripts to control for spurious correlations. Our goal is to contribute to open and reproducible science practices by making DEEP publicly available together with an example mother-infant EEG hyperscanning dataset.

Dialogic Book-Sharing as a Privileged Intersubjective Space.

Parental reading to young children is well-established as being positively associated with child cognitive development, particularly their language development. Research indicates that a particular, "intersubjective," form of using books with children, "Dialogic Book-sharing" (DBS), is especially beneficial to infants and pre-school aged children, particularly when using picture books. The work on DBS to date has paid little attention to the theoretical and empirical underpinnings of the approach. Here, we address the question of what processes taking place during DBS confer benefits to child development, and why these processes are beneficial. In a novel integration of evidence, ranging from non-human primate communication through iconic gestures and pointing, archaeological data on Pre-hominid and early human art, to experimental and naturalistic studies of infant attention, cognitive processing, and language, we argue that DBS entails core characteristics that make it a privileged intersubjective space for the promotion of child cognitive and language development. This analysis, together with the findings of DBS intervention studies, provides a powerful intellectual basis for the wide-scale promotion of DBS, especially in disadvantaged populations.

Multimodal hyperscanning reveals that synchrony of body and mind are distinct in mother-child dyads.

Hyperscanning studies have begun to unravel the brain mechanisms underlying social interaction, indicating a functional role for interpersonal neural synchronization (INS), yet the mechanisms that drive INS are poorly understood. The current study, thus, addresses whether INS is functionally-distinct from synchrony in other systems - specifically the autonomic nervous system and motor behavior. To test this, we used concurrent functional near-infrared spectroscopy - electrocardiography recordings, while N = 34 mother-child and stranger-child dyads engaged in cooperative and competitive tasks. Only in the neural domain was a higher synchrony for mother-child compared to stranger-child dyads observed. Further, autonomic nervous system and neural synchrony were positively related during competition but not during cooperation. These results suggest that synchrony in different behavioral and biological systems may reflect distinct processes. Furthermore, they show that increased mother-child INS is unlikely to be explained solely by shared arousal and behavioral similarities, supporting recent theories that postulate that INS is higher in close relationships.

The effect of perinatal interventions on parent anxiety, infant socio-emotional development and parent-infant relationship outcomes: A systematic review.

Background: Infants of parents with perinatal anxiety are at elevated likelihood of experiencing disruption in the parent-infant relationship, as well as difficulties with socio-emotional functioning in later development. Interventions delivered in the perinatal period have the potential to protect the early dyadic relationship and support infants' ongoing development and socio-emotional outcomes. This review primarily aimed to examine the efficacy of perinatal interventions on parent anxiety, infant socio-emotional development/temperament, and parent-infant relationship outcomes. Secondarily, the review sought to understand how interventions focused principally on one member of the dyad affected the outcomes of the other, and which intervention components were common to successful interventions. Method: Five electronic databases as well as manual search procedures were used to identify randomised controlled trials according to a PICO eligibility criteria framework. Risk of bias assessments were undertaken, and a narrative synthesis was conducted. The review was pre-registered on PROSPERO (CRD42021254799). Results: Twelve studies were analysed in total, including five interventions focused on the adult, and seven interventions focused on the infant, or the infant's relationship with their parent. Interventions incorporating cognitive behavioural strategies for affective disorders showed reductions in parent anxiety (N = 3), and interventions focusing on altering distorted maternal internal representations showed positive change in parent-child dyadic interactions, and infant outcomes (N = 2). Evidence that interventions focused on one partner of the dyad led to improved outcomes for the other partner was limited. However, evidence was of mixed methodological quality. Conclusions: It is important to integrate both parents and infants into treatment programmes for perinatal anxiety. Implications for clinical practice and future intervention trials are discussed.

INTERSTAARS: Attention training for infants with elevated likelihood of developing ADHD: A proof-of-concept randomised controlled trial.

Attention-deficit/hyperactivity disorder (ADHD) is first diagnosed during middle childhood, when patterns of difficulty are often established. Pre-emptive approaches that strengthen developing cognitive systems could offer an alternative to post-diagnostic interventions. This proof-of-concept randomised controlled trial (RCT) tested whether computerised gaze-based attention training is feasible and improves attention in infants liable to develop ADHD. Forty-three 9- to 16-month-old infants with a first-degree relative with ADHD were recruited (11/2015-11/2018) at two UK sites and randomised with minimisation by site and sex to receive 9 weekly sessions of either (a) gaze-contingent attention training (intervention; n = 20); or (b) infant-friendly passive viewing of videos (control, n = 23). Sessions were delivered at home with blinded outcome assessments. The primary outcome was a composite of attention measures jointly analysed via a multivariate ANCOVA with a combined effect size (ES) from coefficients at baseline, midpoint and endpoint (Registration: ISRCTN37683928 ). Uptake and compliance was good but intention-to-treat analysis showed no significant differences between 20 intervention and 23 control infants on primary (ES -0.4, 95% CI -0.9 to 0.2; Complier-Average-Causal Effect ES -0.6, 95% CI -1.6 to 0.5) or secondary outcomes (behavioural attention). There were no adverse effects on sleep but a small increase in post-intervention session fussiness. Although feasible, there was no support for short-term effects of gaze-based attention training on attention skills in early ADHD. Longer-term outcomes remain to be assessed. The study highlights challenges and opportunities for pre-emptive intervention approaches to the management of ADHD.

Stress and Learning in Pupils: Neuroscience Evidence and its Relevance for Teachers.

Our understanding of how stress affects primary school children's attention and learning has developed rapidly. We know that children experience differing levels of stressors (factors that cause stress) in their environments, and that this can influence how they respond to new stressors when they occur in educational contexts. Here, we review evidence showing that stress can increase children's attention and learning capacities in some circumstances but hinder them in others. We show how children differ in their attention and learning styles, dependent on stress levels: for example, more highly stressed children may be more distracted by superficial features and may find it harder to engage in planning and voluntary control. We review intervention research on stress management techniques in children, concentrating on psychological techniques (such as mindfulness and stress reappraisal), physiological techniques (such as breathing exercises) and environmental factors (such as reducing noise). At the current time, raising teachers' awareness of pupils' differing stress responses will be an important step in accommodating the differing needs of children in their classrooms.

Measures of attention in Rett syndrome: Internal consistency reliability.

OBJECTIVE: Rett syndrome (RTT), an x-linked neurodevelopmental disorder caused by spontaneous mutations in the MECP2 gene, is characterized by profound impairments in expressive language and purposeful hand use. We have pioneered the use of gaze-based tasks to by-pass these limitations and developed measures suitable for clinical trials with RTT. Here we estimated internal consistency reliability for three aspects of attention that are key to cognitive growth and that we previously identified as impaired in RTT. METHOD: Using a sample of 66 children with RTT (2-19 years), we assessed Sustained Attention (butterfly task: Butterfly traverses the screen only when fixated and distractors are ignored); Disengaging/Shifting Attention ("gap/overlap" task: Shifts of gaze from central to peripheral targets are compared in conditions where the central stimulus remains or disappears at the onset of the peripheral target); Selective Attention (search task: the target is embedded in arrays differing in size and distractor type). RESULTS: Reliability was acceptable to excellent on almost all key measures from tasks assessing Sustained Attention and Disengaging/Shifting Attention, with split-half coefficients and Cronbach alphas ranging from .70 to .93. Reliability increased as more trials were aggregated, with acceptable levels often reached with as few as six to nine trials. Measures from Selective Attention showed only limited reliability. CONCLUSION: Finding that critical aspects of attention can be reliably assessed in RTT with gaze-based tasks constitutes a major advance in the development of cognitive measures appropriate for clinical and translational work. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Very preterm infants engage in an intervention to train their control of attention: results from the feasibility study of the Attention Control Training (ACT) randomised trial.

BACKGROUND: Very premature birth (gestational age between 28 and 31 + 6 weeks) is associated with increased risk of cognitive delay and attention deficit disorder, which have been linked to anomalies in the development of executive functions (EFs) and their precursors. In particular, very preterm (VP) infants display anomalies in controlling attention and gathering task-relevant information. Early interventions that support attention control may be pivotal in providing a secure base for VP children's later attainments. The Attention Control Training (ACT) is a cognitive training intervention that targets infants' abilities to select visual information according to varying task demands but had not been tested in VP infants. We conducted a feasibility study to test the processes we intend to use in a trial delivering the ACT to VP infants. METHODS AND DESIGN: We tested recruitment and retention of VP infants and their families in a randomised trial, as well as acceptability and completion of baseline and outcome measures. To evaluate these aims, we used descriptive quantitative statistics and qualitative methods to analyse feedback from infants' caregivers. We also investigated the quality of eye-tracking data collected and indicators of infants' engagement in the training, using descriptive statistics. RESULTS: Twelve VP infants were recruited, and 10 (83%) completed the study. Participants' parents had high education attainment. The rate of completion of baseline and outcome measures was optimal. VP infants demonstrated engagement in the training, completing on average 84 min of training over three visits, and displaying improved performance during this training. Eye-tracking data quality was moderate, but this did not interfere with infants' engagement in the training. DISCUSSION: The results suggest the ACT can be delivered to VP infants. However, challenges remain in recruitment of numerous and diverse samples. We discuss strategies to overcome these challenges informed by results of this study. TRIAL REGISTRATION: Registered Registration ID: NCT03896490 . Retrospectively registered at Clinical Trials Protocol Registration and Results System ( clinicaltrials.gov ).