Measuring the temporal dynamics of inter-personal neural entrainment in continuous child-adult EEG hyperscanning data
Current approaches to analysing EEG hyperscanning data in the developmental literature typically consider interpersonal entrainment between interacting physiological systems as a time-invariant property. This approach obscures crucial information about how entrainment between interacting systems is established and maintained over time. Here, we describe methods, and present computational algorithms, that will allow researchers to address this gap in the literature. We focus on how two different approaches to measuring entrainment, namely concurrent (e.g., power correlations, phase locking) and sequential (e.g., Granger causality) measures, can be applied to three aspects of the brain signal: amplitude, power, and phase. We guide the reader through worked examples using simulated data on how to leverage these methods to measure changes in interbrain entrainment. For each, we aim to provide a detailed explanation of the interpretation and application of these analyses when studying neural entrainment during early social interactions.
Gaze onsets during naturalistic infant-caregiver interaction associate with ‘sender’ but not ‘receiver’ neural responses, and do not lead to changes in inter-brain synchrony
Temporal coordination during infant-caregiver social interaction is thought to be crucial for supporting early language acquisition and cognitive development. Despite a growing prevalence of theories suggesting that increased inter-brain synchrony associates with many key aspects of social interactions such as mutual gaze, little is known about how this arises during development. Here, we investigated the role of mutual gaze onsets as a potential driver of inter-brain synchrony. We extracted dual EEG activity around naturally occurring gaze onsets during infant-caregiver social interactions in N=55 dyads (mean age 12 months). We differentiated between two types of gaze onset, depending on each partner's role. 'Sender' gaze onsets were defined at a time when either the adult or the infant made a gaze shift towards their partner at a time when their partner was either already looking at them (mutual) or not looking at them (non-mutual). 'Receiver' gaze onsets were defined at a time when their partner made a gaze shift towards them at a time when either the adult or the infant was already looking at their partner (mutual) or not (non-mutual). Contrary to our hypothesis we found that, during a naturalistic interaction, both mutual and non-mutual gaze onsets were associated with changes in the sender, but not the receiver's brain activity and were not associated with increases in inter-brain synchrony above baseline. Further, we found that mutual, compared to non-mutual gaze onsets were not associated with increased inter-brain synchrony. Overall, our results suggest that the effects of mutual gaze are strongest at the intra-brain level, in the 'sender' but not the 'receiver' of the mutual gaze.
Emotional reactions are usually accompanied by vocalizations whose acoustic features are largely impacted by the physiological state of the body. While many theoretical frameworks emphasize the role played by the perception of bodily changes in the emergence of emotional feelings, few attempts have been made to assess the impact of vocal self-perception in this process. Here, we address this question by asking participants to deliberate out loud about how they would feel in various imaginary situations while we covertly manipulate their voices in order to make them sound emotional. Perceiving these artificial expressive cues in their own voice altered participants' inferences about how they would feel. Crucially, this effect of vocal self-perception on felt emotions was abolished when participants detected our manipulation either explicitly or implicitly. Beyond demonstrating that vocal self-perception plays a role in the emergence of emotions, these results provide causal evidence for self-perception theories. All rights reserved. No reuse allowed without permission. was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
A widespread belief is that large groups engaged in joint actions that require a high level of flexibility are unable to coordinate without the introduction of additional resources such as shared plans or hierarchical organizations. Here, we put this belief to a test, by empirically investigating coordination within a large group of 16 musicians performing collective free improvisation—a genre in which improvisers aim at creating music that is as complex and unprecedented as possible without relying on shared plans or on an external conductor. We show that musicians freely improvising within a large ensemble can achieve significant levels of coordination, both at the level of their musical actions (i.e., their individual decisions to play or to stop playing) and at the level of their directional intentions (i.e., their intentions to change or to support the music produced by the group). Taken together, these results invite us to reconsider the range and scope of actions achievable by large groups, and to explore alternative organizational models that emphasize decentralized and unscripted forms of collective behavior.
Human interactions are often improvised rather than scripted, which suggests that efficient coordination can emerge even when collective plans are largely underspecified. One possibility is that such forms of coordination primarily rely on mutual influences between interactive partners, and on perception–action couplings such as entrainment or mimicry. Yet some forms of improvised joint actions appear difficult to explain solely by appealing to these emergent mechanisms. Here, we focus on collective free improvisation, a form of highly unplanned creative practice where both agents' subjective reports and the complexity of their interactions suggest that shared intentions may sometimes emerge to support coordination during the course of the improvisation, even in the absence of verbal communication. In four experiments, we show that shared intentions spontaneously emerge during collective musical improvisations, and that they foster coordination on multiple levels, over and beyond the mere influence of shared information. We also show that musicians deploy communicative strategies to manifest and propagate their intentions within the group, and that this predicts better coordination. Overall, our results suggest that improvised and scripted joint actions are more continuous with one another than it first seems, and that they differ merely in the extent to which they rely on emergent or planned coordination mechanisms.
Emotions are often accompanied by vocalizations whose acoustic features provide information about the physiological state of the speaker. Here, we ask if perceiving these affective signals in one’s own voice has an impact on one’s own emotional state, and if it is necessary to identify these signals as self-originated for the emotional effect to occur. Participants had to deliberate out loud about how they would feel in various familiar emotional scenarios, while we covertly manipulated their voices in order to make them sound happy or sad. Perceiving the artificial affective signals in their own voice altered participants’ judgements about how they would feel in these situations. Crucially, this effect disappeared when participants detected the vocal manipulation, either explicitly or implicitly. The original valence of the scenarios also modulated the vocal feedback effect. These results highlight the role of the exteroception of self-attributed affective signals in the emergence of emotional feelings.
Listeners’ perceptions of the certainty and honesty of a speaker are associated with a common prosodic signature
The success of human cooperation crucially depends on mechanisms enabling individuals to detect unreliability in their conspecifics. Yet, how such epistemic vigilance is achieved from naturalistic sensory inputs remains unclear. Here we show that listeners’ perceptions of the certainty and honesty of other speakers from their speech are based on a common prosodic signature. Using a data-driven method, we separately decode the prosodic features driving listeners’ perceptions of a speaker’s certainty and honesty across pitch, duration and loudness. We find that these two kinds of judgments rely on a common prosodic signature that is perceived independently from individuals’ conceptual knowledge and native language. Finally, we show that listeners extract this prosodic signature automatically, and that this impacts the way they memorize spoken words. These findings shed light on a unique auditory adaptation that enables human listeners to quickly detect and react to unreliability during linguistic interactions.
Interdependencies between vocal behaviour and interpersonal arousal coupling in caregiver-infant dyads
We currently understand little about how autonomic arousal influences early vocal development. 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 show greater functional flexibility, and their vocal production is more influenced by the infant’s arousal than their own. 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 vocal development is more dependent on interpersonal arousal coupling across caregiver-infant dyads than previously thought.
Even in infancy children from low-SES backgrounds differ in frontal cortex functioning and, by the start of pre-school, they frequently show poor performance on executive functions including attention control. These differences may causally mediate later difficulties in academic learning. Here, we present a study to assess the feasibility of using computerized paradigms to train attention control in infants, delivered weekly over five sessions in early intervention centres for low-SES families. Thirty-three 12-month-old infants were recruited, of whom 23 completed the training. Our results showed the feasibility of repeat-visit cognitive training within community settings. Training-related improvements were found, relative to active controls, on tasks assessing visual sustained attention, saccadic reaction time, and rule learning, whereas trend improvements were found on assessments of short-term memory. No significant improvements were found in task switching. These results warrant further investigation into the potential of this method for targeting ‘at-risk’ infants in community settings.
The ability to sustain attention is a major achievement in human development and is generally believed to be the developmental product of increasing self-regulatory and endogenous (i.e., internal, top-down, voluntary) control over one’s attention and cognitive systems [1–5]. Because sustained attention in late infancy is predictive of future development, and because early deficits in sustained attention are markers for later diagnoses of attentional disorders , sustained attention is often viewed as a constitutional and individual property of the infant [6–9]. However, humans are social animals; developmental pathways for seemingly nonsocial competencies evolved within the social group and therefore may be dependent on social experience [10–13]. Here, we show that social context matters for the duration of sustained attention episodes in one-year-old infants during toy play. Using headmounted eye tracking to record moment-by-moment gaze data from both parents and infants, we found that when the social partner (parent) visually attended to the object to which infant attention was
directed, infants, after the parent’s look, extended their duration of visual attention to the object. Looks to the same object by two social partners is a wellstudied phenomenon known as joint attention, which has been shown to be critical to early learning and to the development of social skills [14, 15]. The present findings implicate joint attention in the development of
the child’s own sustained attention and thus challenge the current understanding of the origins of individual differences in sustained attention, providing a new and potentially malleable developmental pathway to the self-regulation of attention.
Acute stress attenuates frontal lobe functioning and increases distractibility while enhancing subcortical processes in both human and nonhuman animals (reviewed by Arnsten  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.
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.
New meanings of thin-skinned: The contrasting attentional profiles of typical 12-month-olds who show high, and low, stress reactivity.
Previous research is inconsistent as to whether a more labile (faster-changing) autonomic system confers performance advantages, or disadvantages, in infants and children. To examine this, we presented a stimulus battery consisting of mixed static and dynamic viewing materials to a cohort of 63 typical 12-month-old infants. While viewing the battery, infants’ spontaneous visual attention (looks to and away from the screen) was measured. Concurrently, arousal was recorded via heart rate (HR), electrodermal activity, head velocity, and peripheral movement levels. In addition, stress reactivity was assessed using a mild behavioral stressor (watching a video of another infant crying). We found that infants who were generally more attentive showed smaller HR increases to the stressor. However, they also showed greater phasic autonomic changes to attractive, attention-getting stimulus events, a faster rate of change of both look duration and of arousal, and more general oscillatory activity in arousal. Finally, 4 sessions of attention training were applied to a subset of the infants (24 trained, 24 active controls), which had the effect of increasing visual sustained attention. No changes in HR responses to stressor were observed as a result of training, but concomitant increases in arousal lability were observed. Our results point to 2 contrasting autonomic profiles: infants with high autonomic reactivity to stressors show short attention durations, whereas infants with lower autonomic reactivity show longer attention durations and greater arousal lability.
How orchids concentrate? The relationship between physiological stress reactivity and cognitive performance during infancy and early childhood
The Autonomic Nervous System (ANS) is involved both in higher-order cognition such as attention and learning, and in responding to unexpected, threatening events. Increased ANS reactivity may confer both superior short-term cognitive performance, and heightened long-term susceptibility to adverse events. Here, we evaluate this hypothesis within the Differential Susceptibility Theory (DST) framework. We hypothesise that individuals with increased reactivity may show heightened biological sensitivity to context, conferring both positive (development-enhancing) effects (superior attention and learning) and negative (risk-promoting) effects (increased sensitivity to unsupportive environments). First, we examine how ANS reactivity relates to early cognitive performance. We hypothesise that increased phasic ANS reactivity, observed at lower tonic (pre-stimulus) ANS activity, is associated with better attention and learning. We conclude that the evidence is largely in support. Second we discuss whether ANS reactivity to ‘positive’, attention-eliciting and to ‘negative’, aversive stimuli is a one-dimensional construct; and evaluate evidence for how the real-world environment influences physiological stress over short and long time-frames. We identify three areas where the evidence is currently inconclusive.
Increases in Arousal are More Long‐Lasting than Decreases in Arousal: On Homeostatic Failures During Emotion Regulation in Infancy
In emotion regulation, negative or undesired emotions are downregulated, but there are also opponent processes to emotion regulation—in which undesired emotions are exacerbated dynamically over time by processes that have an amplifying or upregulating impact. Evidence for such processes has been shown in adults, but little previous work has examined whether infants show similar patterns. To examine this, we measured physiological arousal in 57 typical 12 month olds while presenting a 20-min mixed viewing battery. Fluctuations in autonomic arousal were measured via heart rate, electrodermal activity, and movement. We reasoned that if transitions in autonomic arousal are random (stochastic), then (1) arousal would be normally distributed across the session, and (2) episodes where arousal exceeded a certain threshold above the mean should be as long-lived as those where arousal exceeded the same threshold below the mean. In fact we found that (1) heart rate and movement (but not electrodermal activity) were positively skewed, and (2) that increases in arousal have a lower extinction probability than decreases in arousal. Our findings may suggest that increases in arousal are self-sustaining. These patterns are the opposite of the homeostatic mechanisms predicted by naïve approaches to emotion regulation.
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.
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.
When we see someone experiencing an emotion, and when we experience it ourselves, common neurophysiological activity occurs [1, 2]. But although inter-dyadic synchrony, concurrent and sequential , has been identified, its functional significance remains inadequately understood. Specifically, how do influences of partner A on partner B reciprocally influence partner A? For example, if I am experiencing an affective state and someone matches their physiological state to mine, what influence does this have on me—the person experiencing the emotion? Here, we investigated this using infant-parent dyads. We developed miniaturized microphones to record spontaneous vocalizations and wireless autonomic monitors to record heart rate, heart rate variability, and movement in infants and parents concurrently in naturalistic settings. Overall, we found that infant-parent autonomic activity did not covary across the day—but that “high points” of infant arousal led to autonomic changes in the parent and that instances where the adult showed greater autonomic responsivity were associated with faster infant quieting. Parental responsivity was higher following peaks in infant negative affect than in positive affect. Overall, parents responded to increases in their child’s arousal by increasing their own. However, when the overall arousal level of the dyad was high, parents responded to elevated child arousal by decreasing their own arousal. Our findings suggest that autonomic state matching has a direct effect on the person experiencing the affective state and that parental co-regulation may involve both connecting and disconnecting their own arousal state from that of the child contingent on context.
Investigating the factors that cause stress in young children and how this affects their concentration
.I am a research scientist based at the University of East London, who receives funding from mainly government-funded research sources. The main focus of my research is on investigating the factors that cause stress in young children, and how this affects their concentration. When I was approached by the Assistant Headteacher of a local school, I jumped at the opportunity for us to do some research together. The school is an inner-city school in a highly ethnically diverse and socio-economically challenged area, and the kinds of children who attend are exactly the kinds of children I am interested in understanding better. The research followed ethical guidelines with informed consent.
Elevated physiological arousal is associated with larger but more variable neural responses to small acoustic change in children during a passive auditory attention task
Little is known of how autonomic arousal relates to neural responsiveness during auditory attention. We presented N = 21 5-7-year-old children with an oddball auditory mismatch paradigm, whilst concurrently measuring heart rate fluctuations. Children with higher mean autonomic arousal, as indexed by higher heart rate (HR) and decreased high-frequency (0.15-0.8 Hz) variability in HR, showed smaller amplitude N250 responses to frequently presented (70%), 500 Hz standard tones. Follow-up analyses showed that the modal evoked response was in fact similar, but accompanied by more large and small amplitude responses and greater variability in peak latency in the high HR group, causing lower averaged responses. Similar patterns were also observed when examining heart rate fluctuations within a testing session, in an analysis that controlled for between-participant differences in mean HR. In addition, we observed larger P150/P3a amplitudes in response to small acoustic contrasts (750 Hz tones) in the high HR group. Responses to large acoustic contrasts (bursts of white noise), however, evoked strong early P3a phase in all children and did not differ by high/low HR. Our findings suggest that elevated physiological arousal may be associated with high variability in auditory ERP responses in young children, along with increased responsiveness to small acoustic changes.
Interpersonal processes influence our physiological states and associated affect. Physiological arousal dysregulation, a core feature of anxiety disorders, has been identified in children of parents with elevated anxiety. However, little is understood about how parent–infant interpersonal regulatory processes differ when the dyad includes a more anxious parent.
We investigated moment-to-moment fluctuations in arousal within parent-infant dyads using miniaturised microphones and autonomic monitors. We continually recorded arousal and vocalisations in infants and parents in naturalistic home settings across day-long data segments.
Our results indicated that physiological synchrony across the day was stronger in dyads including more rather than less anxious mothers. Across the whole recording epoch, less anxious mothers showed responsivity that was limited to ‘peak’ moments in their child's arousal. In contrast, more anxious mothers showed greater reactivity to small-scale fluctuations. Less anxious mothers also showed behaviours akin to ‘stress buffering’ – downregulating their arousal when the overall arousal level of the dyad was high. These behaviours were absent in more anxious mothers.
Our findings have implications for understanding the differential processes of physiological co-regulation in partnerships where a partner is anxious, and for the use of this understanding in informing intervention strategies for dyads needing support for elevated levels of anxiety.
Influences of environmental stressors on autonomic function in 12‐month‐old infants: understanding early common pathways to atypical emotion regulation and cognitive performance
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.
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.
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.
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.
Currently, we understand much about how children’s brains attend to and learn from information presented while they are alone, viewing a screen – but less about how interpersonal social influences are substantiated in the brain. Here, we consider research that examines how social behaviors affect not one, but both partners in a dyad. We review studies that measured interpersonal neural entrainment during early social interaction, considering two ways of measuring entrainment: concurrent entrainment (e.g., ‘when A is high, B is high’ – also known as synchrony) and sequential entrainment (‘changes in A forward-predict changes in B’). We discuss possible causes of interpersonal neural entrainment, and consider whether it is merely an epiphenomenon, or whether it plays an independent, mechanistic role in early attention and learning.
Previous research has suggested that similar patterns of neural activity occur between watching someone else perform an action and performing it oneself. Here, we demonstrate a comparable phenomenon: that, while engaged in free-flowing naturalistic parent-child play, parents’ oscillatory activity recorded overfrontal areas co-varies with their infants’ attention patterns, independent of their own attention patterns. We also found weaker evidence for the opposite relationship: that infants’ brain activity tracks adults’ attention. We demonstratethis by recording dual EEG in 12-month-old infants and their parents while they were engaged in joint and solo tabletop play with toys, andanalysing the time-lagged temporal associations between infants’ attention towards play objects and adults’ neural activity, and vice versa. We discuss how these inter-dyadic brain-behaviour correspondences relate to actor-observer relationships previously been documented, and consider their role asdriversof inter-personal neural synchrony.
Automated systems for identifying and removing non-neural ICA components are growing in popularity among adult EEG researchers. Infant EEG data differs in many ways from adult EEG data, but there exists almost no specific system for automated classification of source components from paediatric populations. Here, we adapt one of the most popular systems for adult ICA component classification for use with infant EEG data. Our adapted classifier significantly outperformed the original adult classifier on samples of naturalistic free play EEG data recorded from 10 to 12-month-old infants, achieving agreement rates with the manual classification of over 75% across two validation studies (n=44, n=25). Additionally, we examined both classifiers ability to remove stereotyped ocular artifact from a basic visual processing ERP dataset, compared to manual ICA data cleaning. Here the new classifier performed on level with expert manual cleaning and was again significantly better than the adult classifier at removing artifact whilst retaining a greater amount of genuine neural signal, operationalised through comparing ERP activations in time and space. Our new system (iMARA) offers developmental EEG researchers a flexible tool for automatic identification and removal of artifactual ICA components.
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. While interpersonal synchrony is considered a multimodal phenomenon, it is not clear how different biological and behavioral synchrony markers are related to each other. The current study, thus, addresses whether INS is functionally-distinct from synchrony in other systems - specifically the autonomic nervous system (ANS) and motor behavior. To test this, we used a novel methodological approach, based on concurrent functional near-infrared spectroscopy-electrocardiography, recorded while N = 34 mother-child and stranger-child dyads (child mean age 14 years) engaged in cooperative or competitive tasks. Results showed a marked differentiation between neural, ANS and behavioral synchrony. Importantly, only in the neural domain was higher synchrony for mother-child compared to stranger-child dyads observed. Further, ANS 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. Mother-child INS may arise due to neural processes related to social affiliation, which go beyond shared arousal and similarities in behavior.
Bidirectional Mechanisms rather than Alternatives: The Role of Sustained Attention in Interactive Contexts Can Only Be Understood through Joint Attention
Although associations between joint attention and infant development have been extensively investigated (eg, Carpenter et al., 1998; Donnellan et al., 2020; Mundy & Newell, 2007), the question of how, exactly, interactive behaviours support infant learning remains widely debated (Abney et al., 2020; Tomasello et al., 2007). Hudspeth and Lewis (this issue, DOI 10.1159/000515681) suggest that measures of joint attention in early interaction with an adult partner might merely reflect the ability of the infant to sustain their attention. This theory places infant object engagement at the forefront of attention and learning in joint interaction, in contrast to more traditional views that emphasise infants’ engagement with the attentional behaviours of their adult partner (eg, Carpenter et al., 1998). First, we discuss Hudspeth and Lewis’s comments on methodological issues to do with defining sustained attention. Next, we consider an important point that they do not mention - namely, the inconsistencies in defining joint attention in the literature. We end by exploring endogenous and exogenous influences on sustained and concurrent looking in early interaction, as well as their implications for understanding infant learning.
Current approaches typically measure the connectivity between interacting physiological systems as a time-invariant property. This approach obscures crucial information about how connectivity between interacting systems is established and maintained. Here, we describe methods, and present computational algorithms, that will allow researchers to address this deficit. We focus on how two different approaches to measuring connectivity, namely concurrent (e.g., power correlations, phase locking) and sequential (e.g., Granger causality), can be applied to three aspects of the brain signal, namely amplitude, power, and phase. We guide the reader through worked examples using mainly simulated data on how to leverage these methods to measure changes in interbrain connectivity between adults and children/infants relative to events identified within continuous EEG data during a free-flowing naturalistic interaction. For each, we aim to provide a detailed explanation of the interpretation of the analysis and how they can be usefully used when studying early social interactions.
Most research has studied self-regulation by presenting experimenter-controlled test stimuliand measuring change between a baseline period and the stimulus. But in the real world weare not passive recipients of discrete chunks of external stimulation, to which we in turnrespond; rather, the real world is continuous and we self-regulate by adaptively selectingwhich aspects of the social environment that we attend to from one moment to the next. Here,we contrast two dynamic processes that guide this process – the ‘yin’ and ‘yang’ of self-regulation. First, allostasis, through which we dynamically compensate for change tomaintain homeostasis. This involves upregulating in some situations and downregulating inothers. And second, metastasis, the dynamical principle underling dysregulation. Throughmetastasis, small initial fluctuations can become progressively amplified over time. Wecontrast these processes at the individual level (i.e. by examining moment-to-moment changein one child, considered independently) and also at the inter-personal level (i.e. by examiningchange across a dyad, such as a parent-child dyad). Finally, we discuss practical implicationsof this approach in improving the self-regulation of emotion and cognition, in typicaldevelopment and psychopathology.
In infancy, it’s the extremes of arousal that are ‘sticky’: Naturalistic data challenge purely homeostatic approaches to studying self-regulation
Most theoretical models of arousal/regulatory function emphasise the maintenance of homeostasis; consistent with this, most previous research into arousal has concentrated on examining individuals’ recovery following the administration of experimentally administered stressors. Here, we take a different approach: we recorded day-long spontaneous fluctuations in autonomic arousal (indexed via electrocardiogram, heart rate variability and actigraphy) in a cohort of 82 typically developing 12-month-old infants while they were at home and awake. Based on the aforementioned models, we hypothesised that extreme high or low arousal states might be more short-lived than intermediate arousal states. Our results suggested that, contrary to this, both low- and high-arousal states were more persistent than intermediate arousal states. The same pattern was present when the data were viewed over multiple epoch sizes from 1 s to 5 min; over 10–15-minute time-scales, high-arousal states were more persistent than low- and intermediate states. One possible explanation for these findings is that extreme arousal states have intrinsically greater hysteresis; another is that, through ‘metastatic’ processes, small initial increases and decreases in arousal can become progressively amplified over time. Rather than exclusively using experimental paradigms to study recovery, we argue that future research should also use naturalistic data to study the mechanisms through which states can be maintained or amplified over time.
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.
We currently understand little about how autonomic arousal influences early vocaldevelopment. To examine this, we used wearable microphones and autonomic sensors tocollect multimodal naturalistic datasets from 12-month-olds and their caregivers. Weobserved that, across the day, clusters of vocalisations occur during elevated infant andcaregiver arousal. This relationship is stronger in infants than caregivers:caregivers showgreater functional flexibility, and their vocal production is more influenced by the infant’sarousal than their own. Cries occur following reduced infant arousal stability and lead toincreased child-caregiver arousal coupling, and decreased infant arousal. Speech-likevocalisations also occur at elevated arousal, but lead to longer-lasting increases in arousal,and elicit more parental verbal responses. Our results suggest that vocal development is moredependent on interpersonal arousal coupling across caregiver-infant dyads than previously thought.
Physiological stress, sustained attention, emotion regulation, and cognitive engagement in 12-month-old infants from urban environments
Over the last 2 centuries there has been a rapid increase in the proportion of children who grow up in cities. However, relatively little work has explored in detail the physiological and cognitive pathways through which city life may affect early development. To assess this, we observed a cohort of infants growing up in diverse settings across South East England across a 2-day assessment battery. On Visit 1, day-long home recordings were made to monitor infants’ physiological stress in real-world settings. On Visit 2, lab batteries were administered to measure infants’ cognitive, emotional, and neural reactivity. Infants from more high-density urban environments showed increased physiological stress (decreased parasympathetic nervous system activity) at home. This relationship was independent of socioeconomic status and lifelong stressors. Behaviorally, infants raised in high-density settings showed lower sustained attention in the lab, along with increased behavioral and physiological reactivity during an emotion elicitation task. However, they also showed increased recognition memory for briefly presented stimuli and increased neural engagement with novel stimuli. This pattern is consistent with other research into how elevated physiological stress influences cognition, and with theoretical approaches from adult research that predict that city life is associated with a profile of cognitive strengths as well as weaknesses. Implications for education and developmental psychopathology are discussed.
Infant effortful control mediates relations between nondirective parenting and internalising-related child behaviours in an autism-enriched infant cohort
Internalising problems are common within Autism Spectrum Disorder (ASD); early intervention to support those with emerging signs may be warranted. One promising signal lies in how individual differences in temperament are shaped by parenting. Our longitudinal study of infants with and without an older sibling with ASD investigated how parenting associates with infant behavioural inhibition (8–14 months) and later effortful control (24 months) in relation to 3-year internalising symptoms. Mediation analyses suggest nondirective parenting (8 months) was related to fewer internalising problems through an increase in effortful control. Parenting did not moderate the stable predictive relation of behavioural inhibition on later internalising. We discuss the potential for parenting to strengthen protective factors against internalising in infants from an ASD-enriched cohort.
The origins of effortful control: How early development within arousal/regulatory systems influences attentional and affective control
In this review, I consider the developmental interactions between two domains sometimes characterised as at opposite ends of the human spectrum: early-developing arousal/regulatory domains, that subserve basic mechanisms of survival and homeostasis; and the later-developing ‘higher-order’ cognitive domain of effortful control. First, I examine how short-term fluctuations within arousal/regulatory systems associate with fluctuations in effortful control during early childhood. I present evidence suggesting that both hyper- and hypo-arousal are associated with immediate reductions in attentional and affective control; but that hyper-aroused individuals can show cognitive strengths (faster learning speeds) as well as weaknesses (reduced attentional control). I also present evidence that, in infancy, both hyper- and hypo-aroused states may be dynamically amplified through interactions with the child’s social and physical environment. Second, I examine long-term interactions between arousal/regulatory systems and effortful control. I present evidence that atypical early arousal/regulatory development predicts poorer attentional and affective control during later development. And I consider moderating influences of the environment, such that elevated early arousal/regulatory system reactivity may confer both cognitive advantages in a supportive environment, and disadvantages in an unsupportive one. Finally, I discuss how future research can further our understanding of these close associations between attentional and affective domains during early development.
How the development of executive function influences our moment-by-moment interactions with the real-world environment
Historically, the study of executive function (EF) development has relied on using experimental paradigms to assess EFs as abstract, time-invariant properties of individual brains. Here, we discuss new research that moves away from studying EFs purely as internal mental constructs, towards an approach that aims to understand how EFs are expressed through the inter-relationship between an individual’s brain and the world around them. We offer three illustrative examples of this approach. The first looks at how we learn to make predictions and anticipations based on different types of regularity in our early social and physical environment. The second looks at how we learn to correct, moment-by-moment, for changes in the outside world to maintain stability in the face of change. The third looks at how we allocate our attention on a moment-by-moment basis, in naturalistic settings. We discuss potential new therapeutic avenues for improving EFs arising from this research.
Oscillatory entrainment to our early social or physical environment and the emergence of volitional control
An individual’s early interactions with their environment are thought to be largely passive; through the early years, the capacity for volitional control develops. Here, we consider: how is the emergence of volitional control characterised by changes in the entrainment observed between internal activity (behaviour, physiology and brain activity) and the sights and sounds in our everyday environment (physical and social)? We differentiate between contingent responsiveness (entrainment driven by evoked responses to external events) and oscillatory entrainment (driven by internal oscillators becoming temporally aligned with external oscillators). We conclude that ample evidence suggests that children show behavioural, physiological and neural entrainment to their physical and social environment, irrespective of volitional attention control; however, evidence for oscillatory entrainment beyond contingently responsiveness is currently lacking. We also discuss environmental entrainment as a mechanism that might explain why periodic environment rhythms facilitate sensory processing, and explain the relationships observed between how periodic a child’s environment is and their long-term development of volitional control.
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 towards the end of the first year is fundamental to language acquisition and social cognition (Carpenter et al., 1998). 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 EEG from 12-month-old infants whilst they engaged in table-top play with their caregiver, we examined the ostensive signals and neural activity preceding and following infant-vs. adult-led joint attention. Contrary to traditional theories of socio-communicative development (Tomasello et al., 2007), infant-led joint attention episodes appeared largely reactive: they were not associated with increased theta power, a neural marker of endogenously driven attention, or 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 10-12 months, infants are not yet proactive in creating joint attention. They do, however, anticipate behavioural contingency, a potentially foundational mechanism for the emergence of intentional communication (Smith & Breazeal, 2007).
Needing to shout to be heard? Affective dysregulation, caregiver under-responsivity, and disconnection between vocal signalling and autonomic arousal in infants from chaotic households
Higher levels of household chaos have been related to increased child affect dysregulation during later development. To understand why this relationship emerges, we used miniature wearable microphones and autonomic monitors to obtain day-long recordings in home settings from a cohort of N=74 12-month-old infants and their caregivers from the South-East of the UK. Our findings suggest a disconnect between what infants communicate and their physiological arousal levels, that are likely to reflect what they experience. Specifically, in households which families self-reported as being more chaotic, infants were more likely to produce negative affect vocalisations such as cries at lower levels of arousal. This disconnection between signalling and autonomic arousal was also present in a lab still face procedure, where infants from more chaotic households showed reduced change in facial affect and slower physiological recovery despite equivalent change in arousal during the still face episode. Finally, we found that this disconnect between what infants communicate and their physiological arousal levels may influence the likelihood of a caregiver responding. Implications for understanding the mechanisms underlying the relationship between household chaos, emotion dysregulation and caregiver under-responsivity are discussed.