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.

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.

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.

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.

Parental neural responsivity to infants' visual attention: How mature brains influence immature brains during social interaction.

Almost all attention and learning-in particular, most early learning-take place in social settings. But little is known of how our brains support dynamic social interactions. We recorded dual electroencephalography (EEG) from 12-month-old infants and parents during solo play and joint play. During solo play, fluctuations in infants' theta power significantly forward-predicted their subsequent attentional behaviours. However, this forward-predictiveness was lower during joint play than solo play, suggesting that infants' endogenous neural control over attention is greater during solo play. Overall, however, infants were more attentive to the objects during joint play. To understand why, we examined how adult brain activity related to infant attention. We found that parents' theta power closely tracked and responded to changes in their infants' attention. Further, instances in which parents showed greater neural responsivity were associated with longer sustained attention by infants. Our results offer new insights into how one partner influences another during social interaction.

Emotional valence modulates the topology of the parent-infant inter-brain network.

Emotional communication between parents and children is crucial during early life, yet little is known about its neural underpinnings. Here, we adopt a dual connectivity approach to assess how positive and negative emotions modulate the interpersonal neural network between infants and their mothers during naturalistic interaction. Fifteen mothers were asked to model positive and negative emotions toward pairs of objects during social interaction with their infants (mean age 10.3 months) whilst the neural activity of both mothers and infants was concurrently measured using dual electroencephalography (EEG). Intra-brain and inter-brain network connectivity in the 6-9 Hz range (i.e. infant Alpha band) during maternal expression of positive and negative emotions was computed using directed (partial directed coherence, PDC) and non-directed (phase-locking value, PLV) connectivity metrics. Graph theoretical measures were used to quantify differences in network topology as a function of emotional valence. We found that inter-brain network indices (Density, Strength and Divisibility) consistently revealed strong effects of emotional valence on the parent-child neural network. Parents and children showed stronger integration of their neural processes during maternal demonstrations of positive than negative emotions. Further, directed inter-brain metrics (PDC) indicated that mother to infant directional influences were stronger during the expression of positive than negative emotional states. These results suggest that the parent-infant inter-brain network is modulated by the emotional quality and tone of dyadic social interactions, and that inter-brain graph metrics may be successfully applied to examine these changes in parent-infant inter-brain network topology.

Research Review: Do parent ratings of infant negative emotionality and self-regulation predict psychopathology in childhood and adolescence? A systematic review and meta-analysis of prospective longitudinal studies.

BACKGROUND: Identifying low-cost and easy to implement measures of infant markers of later psychopathology may improve targeting of early intervention for prevention. Because of their early manifestation, relative stability and overlap with constructs central to affect-based dimensions of child and adolescent psychopathology, negative emotionality and self-regulation have been the focus of this research. We conducted a meta-analysis of longitudinal studies examining the prospective association between infant temperament measured with parent ratings and child/adolescent psychopathology. METHODS: A systematic literature search for prospective longitudinal studies, which included measures of questionnaire-assessed infant temperament (negative emotionality, self-regulation, behavioural inhibition, surgency/extraversion, activity level) and symptoms of child or adolescent mental health (externalising, internalising) and neurodevelopmental problems (attention deficit/hyperactivity disorder [ADHD], autism spectrum disorder [ASD]), was conducted. Standardised estimates of association were calculated and pooled in meta-analyses. RESULTS: Twenty-five studies (n = 28,425) met inclusion criteria. Small associations were seen between psychopathology aggregated across all domains and infant negative emotionality (r = .15; p < .001) and self-regulation (r = -.19; p = .007). Effects were also significant but weaker for behavioural inhibition (r = .10; p = .027) and activity level (r = .08; p = .016). Surgency/extraversion was not significantly associated with psychopathology in general (r = -.04; p = .094); however, it was negatively associated with ASD (r = -.10, p = .015). Significant correlations were observed with some outcomes isomorphic with predictors, internalising problems and behavioural inhibition (r = .10; p = .013), ADHD symptoms and activity level (r = .19; p = .009). CONCLUSION: Questionnaire-based assessments of infant negative emotionality may have transdiagnostic potential to contribute to a risk index of later childhood psychopathology. Behavioural inhibition, surgency/extraversion and activity ratings may provide more specific predictive power. More data from prospective studies are required before the potential of self-regulation and surgency/extraversion can be properly gauged.

Speaker gaze increases information coupling between infant and adult brains.

When infants and adults communicate, they exchange social signals of availability and communicative intention such as eye gaze. Previous research indicates that when communication is successful, close temporal dependencies arise between adult speakers' and listeners' neural activity. However, it is not known whether similar neural contingencies exist within adult-infant dyads. Here, we used dual-electroencephalography to assess whether direct gaze increases neural coupling between adults and infants during screen-based and live interactions. In experiment 1 (n = 17), infants viewed videos of an adult who was singing nursery rhymes with (i) direct gaze (looking forward), (ii) indirect gaze (head and eyes averted by 20°), or (iii) direct-oblique gaze (head averted but eyes orientated forward). In experiment 2 (n = 19), infants viewed the same adult in a live context, singing with direct or indirect gaze. Gaze-related changes in adult-infant neural network connectivity were measured using partial directed coherence. Across both experiments, the adult had a significant (Granger) causal influence on infants' neural activity, which was stronger during direct and direct-oblique gaze relative to indirect gaze. During live interactions, infants also influenced the adult more during direct than indirect gaze. Further, infants vocalized more frequently during live direct gaze, and individual infants who vocalized longer also elicited stronger synchronization from the adult. These results demonstrate that direct gaze strengthens bidirectional adult-infant neural connectivity during communication. Thus, ostensive social signals could act to bring brains into mutual temporal alignment, creating a joint-networked state that is structured to facilitate information transfer during early communication and learning.

Future preferences and prospection of future of outcomes: Independent yet specific associations with attention-deficit/hyperactivity disorder.

INTRODUCTION: Symptoms of attention-deficit hyperactivity disorder (ADHD) and conduct problems have been associated with heightened temporal discounting of reward value resulting in a preference for immediate over delayed outcomes. We examined the cross-sectional relationship between future preference (including intertemporal choice) and prospection (the ability to bring to mind and imagine the experience of future personally-relevant events and outcomes) in adolescents with a range of ADHD symptoms and aggressive behaviour. METHODS: A combination of behavioural tasks and self-reports measured intertemporal decision making, individual differences in preference for future outcomes and experience of prospection in a convenience sample of English adolescents aged 11-17 (n = 64, 43.8% males). Parents rated symptoms of ADHD and aggression. RESULTS: & Conclusions: Factor analysis identified two factors: "Future Preference" and "Prospection". Significant negative bivariate correlations were found between ADHD and the scores of both factors and between aggression and Future Preference. A path model confirmed the independent significant association of ADHD with both factors but not with aggression. There was no evidence that Prospection was associated with Future Preference or that it reduced the associations between ADHD symptoms and Future Preference. These results provide further evidence that ADHD is associated with a tendency to prefer immediate over future outcomes. The same association with aggression seemed to be driven by the overlap with ADHD symptoms. We provide some of the first evidence that individuals with high ADHD symptoms have difficulty in prospecting about future episodes. However, this is unrelated to their preference for future outcomes.

Influences of environmental stressors on autonomic function in 12-month-old infants: understanding early common pathways to atypical emotion regulation and cognitive performance.

BACKGROUND: Previous research has suggested that children exposed to more early-life stress show worse mental health outcomes and impaired cognitive performance in later life, but the mechanisms subserving these relationships remain poorly understood. METHOD: Using miniaturised microphones and physiological arousal monitors (electrocardiography, heart rate variability and actigraphy), we examined for the first time infants' autonomic reactions to environmental stressors (noise) in the home environment, in a sample of 82 12-month-old infants from mixed demographic backgrounds. The same infants also attended a laboratory testing battery where attention- and emotion-eliciting stimuli were presented. We examined how children's environmental noise exposure levels at home related to their autonomic reactivity and to their behavioural performance in the laboratory. RESULTS: Individual differences in total noise exposure were independent of other socioeconomic and parenting variables. Children exposed to higher and more rapidly fluctuating environmental noise showed more unstable autonomic arousal patterns overall in home settings. In the laboratory testing battery, this group showed more labile and short-lived autonomic changes in response to novel attention-eliciting stimuli, along with reduced visual sustained attention. They also showed increased arousal lability in response to an emotional stressor. CONCLUSIONS: Our results offer new insights into the mechanisms by which environmental noise exposure may confer increased risk of adverse mental health and impaired cognitive performance during later life.

Infants' visual sustained attention is higher during joint play than solo play: is this due to increased endogenous attention control or exogenous stimulus capture?

Previous research has suggested that when a social partner, such as a parent, pays attention to an object, this increases the attention that infants pay to that object during spontaneous, naturalistic play. There are two contrasting reasons why this might be: first, social context may influence increases in infants' endogenous (voluntary) attention control; second, social settings may offer increased opportunities for exogenous attentional capture. To differentiate these possibilities, we compared 12-month-old infants' naturalistic attention patterns in two settings: Solo Play and Joint Play with a social partner (the parent). Consistent with previous research, we found that infants' look durations toward play objects were longer during Joint Play, and that moments of inattentiveness were fewer, and shorter. Follow-up analyses, conducted to differentiate the two above-proposed hypotheses, were more consistent with the latter hypothesis. We found that infants' rate of change of attentiveness was faster during Joint Play than Solo Play, suggesting that internal attention factors, such as attentional inertia, may influence looking behaviour less during Joint Play. We also found that adults' attention forwards-predicted infants' subsequent attention more than vice versa, suggesting that adults' behaviour may drive infants' behaviour. Finally, we found that mutual gaze did not directly facilitate infant attentiveness. Overall, our results suggest that infants spend more time attending to objects during Joint Play than Solo Play, but that these differences are more likely attributable to increased exogenous attentional scaffolding from the parent during social play, rather than to increased endogenous attention control from the infant.

Training Basic Visual Attention Leads to Changes in Responsiveness to Social-Communicative Cues in 9-Month-Olds.

This study investigated transfer effects of gaze-interactive attention training to more complex social and cognitive skills in infancy. Seventy 9-month-olds were assigned to a training group (n = 35) or an active control group (n = 35). Before, after, and at 6-week follow-up both groups completed an assessment battery assessing transfer to nontrained aspects of attention control, including table top tasks assessing social attention in seminaturalistic contexts. Transfer effects were found on nontrained screen-based tasks but importantly also on a structured observation task assessing the infants' likelihood to respond to an adult's social-communication cues. The results causally link basic attention skills and more complex social-communicative skills and provide a principle for studying causal mechanisms of early development.

Infant Attention Is Dynamically Modulated With Changing Arousal Levels.

Traditional accounts of developing attention and cognition emphasize static individual differences in information encoding; however, work from Aston-Jones et al. suggests that looking behavior may be dynamically influenced by autonomic arousal. To test this model, a 20-min testing battery constituting mixed photos and cartoon clips was shown to 53 typical 12-month-olds. Look duration was recorded to index attention, and continuous changes in arousal were tracked by measuring heart rate, electrodermal activity, and movement levels. Across three analyses, we found that continuous changes in arousal tracked simultaneous changes in attention measures, as predicted by the Aston-Jones model. It was also found that changes in arousal tended to precede (occur before) subsequent changes in attention. Implications of these findings are discussed.

Stress reactivity speeds basic encoding processes in infants.

Acute stress attenuates frontal lobe functioning and increases distractibility while enhancing subcortical processes in both human and nonhuman animals (reviewed by Arnsten [2009] Nature Reviews Neuroscience, 10(6):410-422). To date however these relations have not been examined for their potential effects in developing populations. Here, we examined the relationship between stress reactivity (infants' heart rate response to watching videos of another child crying) and infant performance on measures of looking duration and visual recognition memory. Our findings indicate that infants with increased stress reactivity showed shorter look durations and more novelty preference. Thus, stress appears to lead to a faster, more stimulus-ready attentional profile in infants. Additional work is required to assess potential negative consequences of stimulus-responsivity, such as decreased focus or distractibility. © 2016 Wiley Periodicals, Inc. Dev Psychobiol 58: 546-555, 2016.

Visual motherese? Signal-to-noise ratios in toddler-directed television.

Younger brains are noisier information processing systems; this means that information for younger individuals has to allow clearer differentiation between those aspects that are required for the processing task in hand (the 'signal') and those that are not (the 'noise'). We compared toddler-directed and adult-directed TV programmes (TotTV/ATV). We examined how low-level visual features (that previous research has suggested influence gaze allocation) relate to semantic information, namely the location of the character speaking in each frame. We show that this relationship differs between TotTV and ATV. First, we conducted Receiver Operator Characteristics analyses and found that feature congestion predicted speaking character location in TotTV but not ATV. Second, we used multiple analytical strategies to show that luminance differentials (flicker) predict face location more strongly in TotTV than ATV. Our results suggest that TotTV designers have intuited techniques for controlling toddler attention using low-level visual cues. The implications of these findings for structuring childhood learning experiences away from a screen are discussed.

Widely applicable MATLAB routines for automated analysis of saccadic reaction times.

Saccadic reaction time (SRT) is a widely used dependent variable in eye-tracking studies of human cognition and its disorders. SRTs are also frequently measured in studies with special populations, such as infants and young children, who are limited in their ability to follow verbal instructions and remain in a stable position over time. In this article, we describe a library of MATLAB routines (Mathworks, Natick, MA) that are designed to (1) enable completely automated implementation of SRT analysis for multiple data sets and (2) cope with the unique challenges of analyzing SRTs from eye-tracking data collected from poorly cooperating participants. The library includes preprocessing and SRT analysis routines. The preprocessing routines (i.e., moving median filter and interpolation) are designed to remove technical artifacts and missing samples from raw eye-tracking data. The SRTs are detected by a simple algorithm that identifies the last point of gaze in the area of interest, but, critically, the extracted SRTs are further subjected to a number of postanalysis verification checks to exclude values contaminated by artifacts. Example analyses of data from 5- to 11-month-old infants demonstrated that SRTs extracted with the proposed routines were in high agreement with SRTs obtained manually from video records, robust against potential sources of artifact, and exhibited moderate to high test-retest stability. We propose that the present library has wide utility in standardizing and automating SRT-based cognitive testing in various populations. The MATLAB routines are open source and can be downloaded from http://www.uta.fi/med/icl/methods.html .

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.

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'.

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.