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.
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.
Electroencephalography (EEG) is perhaps the most widely used brain-imaging
technique for paediatric populations. However, EEG signals are prone to distortion by
motion-related artifacts, which can severely confound interpretation. Compared to adult EEG,
motion during infant EEG acquisition is both more frequent and less stereotypical. Yet the
diverse effects of motion on the infant EEG signal have not been documented. This work
represents the first systematic assessment of the effects of naturalistic motion on infant and
adult EEG signals. In Study 1, five mother-infant pairs were video-recorded during
naturalistic joint- and solo-play with toys. The frequency of occurrence of 27 different facial
and body motions was time-coded for both adults and infants. Our results suggested that
movement was continuously present within dyads, and that different types of movement were
observed when comparing social and non-social play, as well as adults and infants. In Study
2, one adult and one infant actor each re-created the most commonly occurring facial, limb
and postural motions from Study 1, allowing us to assess the topological and spectral features
of motion-related EEG artifacts, as compared to resting state EEG measurements. For the
adult, all movement types (facial, limb and postural) generated significant increases in
spectral power relative to resting state. Topographically and spectrally, the strongest
contamination occurred at peripheral recording sites, and affected delta and high-beta
frequency bands most severely. Exceptionally, at certain central and centro-parietal channels,
virtually no motion-induced power changes were observed in theta, alpha and low-beta
frequencies. By contrast, infant motions mainly produced a decrease in alpha power over
fronto-central and centro-parietal regions, and was most pronounced for talking and upper
limb movements. However, with the exception of peripheral channels, the infant theta band
(3-6 Hz) showed little contamination by face and limb motions. It is intended that this work
will inform future development of methods for EEG motion-artifact detection and removal,
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and contribute toward the development of common artifact-related resources and bestpractice guidelines for EEG researchers in social and developmental neuroscience.
Facial expressions are central components of face-to-face interactions and non-verbal communication. Most studies have measured changes in facial configuration by manually hand-coding videos of participants’ faces. This is relatively easy to setup and has facilitated theoretical developments in many fields e.g. spontaneous mimicry (REF). However, hand-coding does not track graded changes in action magnitude: they typically report onsets and offsets alone (REF). Without the action gradient, facial dynamics are reduced to binary events that do not differ in topography or temporal quality.
The ideal alternative, Electromyography (EMG), requires wired sensors be placed on skin. This spawns the possibility of participant discomfort, introduces the requirement for resources and limits ecological validity. Automated facial coding may provide an optimal trade-off: non-intrusive instruments that assess magnitude. Cross-correlations will be used to assess the degree to which the opensource auto-coder package (Mémoire IRCGN [https://github.com/LafLaurine/imac2-memoire-ircgn]) can approximate EMG data (Corrugator supercilii) in naturalistic, face-to-face interactions between mother-infant dyads (N - 10 dyads; infant age range 4-6 months). The videos will also be hand-coded enabling for the findings to link to the published literature.
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.
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.
Differential Susceptibility Theory explains long-term associations between neurobiological sensitivity and cognitive outcomes, but no comparable theoretical framework exists to understand how neurobiological sensitivity and cognitive performance inter-relate on shorter time-frames. Here, we evaluate a framework proposed by Aston-Jones and colleagues, building on the Yerkes-Dodson model, to understand these associations. The framework describes how slow-moving (tonic) changes in autonomic arousal relate to fast (phasic) changes, as observed for example relative to experimenter-determined events, and how phasic changes relate to attention. Larger phasic changes, which associate with better selective attention, are most likely at mid-level tonic arousal. Smaller phasic changes, and worse selective attention, are observed at hypo- and hyper-arousal. We review the fit of this model to typical and atypical development, during infancy and childhood.
Background: Attention deficit hyperactivity disorder (ADHD) is a prevalent neurodevelopmental disorder that can negatively impact on an individual’s quality of life. It is pathophysiologically complex and heterogeneous with different neuropsychological processes being impaired in different individuals. Executive function deficits, including those affecting attention, working memory and inhibitory control, are common. Cognitive training has been promoted as a treatment option, based on the notion that by strengthening the neurocognitive networks underlying these executive processes, ADHD symptoms will also be reduced. However, if implemented in childhood or later, when the full disorder has become well-established, cognitive training has only limited value. INTERSTAARS is a trial designed to test a novel approach to intervention, in which cognitive training is implemented early in development, before the emergence of the disorder. The aim of INTERSTAARS is to train early executive skills, thereby increasing resilience and reducing later ADHD symptoms and associated impairment. Methods/design: Fifty 10–14-month-old infants at familial risk of ADHD will participate in INTERSTAARS. Infants will be randomised to an intervention or a control group. The intervention aims to train early attention skills by using novel eye-tracking technology and gaze-contingent training paradigms. Infants view animated games on a screen and different events take place contingent on where on the screen the infant is looking. Infants allocated to the intervention will receive nine weekly home-based attention training sessions. Control group infants will also receive nine weekly home visits, but instead of viewing the training games during these visits they will view non-gaze-contingent age-appropriate videos. At baseline and post treatment, infant attention control will be assessed using a range of eye-tracking, observational, parent-report and neurophysiological measures. The primary outcome will be a composite of eye-tracking tasks used to assess infant attention skills. Follow-up data will be collected on emerging ADHD symptoms when the infants are 2 and 3 years old. Discussion: This is the first randomised controlled trial to assess the potential efficacy of cognitive training as a prevention measure for infants at familial risk of ADHD. If successful, INTERSTAARS could offer a promising new approach for developing early interventions for ADHD
Early exposure to noisy, chaotic home environments is associated with increased physiological stress and adverse long-term cognitive and clinical outcomes. However, this research has generally used questionnaires to measure average household noise, despite that stress is, by definition, a dynamic, compensatory mechanism – thus obscuring the detailed picture of how we are dynamically influenced by, and compensate for, stressors in our environment. Here, we used miniaturised microphones and autonomic monitors to measure noise and infants’ spontaneous movement at home. We observed an inverse-U-shaped relationship, such that less movement was observed at extreme low and high ambient noise
levels. This relationship was observed across multiple settings and time scales; however, when we removed the autocorrelation (i.e. slow-varying fluctuation) from the sound data, it disappeared and only a linear relationship (higher movement associated with higher sound)
was observed. This indicates that the effect of reduced movement at extreme high sound is driven by sustained episodes of high sound. This effect may be caused by temporary fatigue, or by children actively down-regulating their movement levels to compensate for highly
arousing situations - analogous to a newborn closing their eyes when over-stimulated. Implications of these findings for understanding how noisy/chaotic environments affect development are discussed
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).
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.
Predominant accounts explaining links between early looking behavior and later cognitive outcomes emphasize static individual differences in information encoding; however, work from Aston-Jones and colleagues suggests that looking behavior may be dynamically influenced by ongoing, phasic changes in autonomic arousal. To test the Aston-Jones model, a 20-minute 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, electro-dermal 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. We also found that changes in arousal tended to precede (occur before) subsequent changes in attention.
In a second study, we investigated causal interactions between attention and arousal by applying, over a 2-week training period, targeted cognitive training to a cohort of 12-month-old infants, aimed at strengthening the voluntary control of visual attention. Before and after training, and relative to an active control group, infants’ attentional control capacity and autonomic arousal were measured. Training was found to lead to marked changes in infants’ behaviour, across a number of different tasks, but infants’ autonomic arousal was unchanged following training. Changes in autonomic arousal remained as predictive of looking behaviour after training, as before. This suggests that arousal and voluntary attention control have separable influences on looking behaviour in infants.
In a third study we examined whether infants with more labile (sensitive) autonomic arousal patterns showed better, or worse, performance on learning tasks. Previous research has suggested that acute stress attenuates frontal lobe functioning and increases distractibility while enhancing subcortical processes in both human and nonhuman animals (Arnsten, 1998, Arnsten et al., 1998, Skosnik, 1999). To date however these relations have not been examined for their potential effects in developing populations. 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
Facial expressions are central components of face-to-face interactions and non-verbal communication. Most studies have measured changes in facial configuration by manually hand-coding videos of participants’ faces. This is relatively easy to setup and has facilitated theoretical developments in many fields e.g. spontaneous mimicry (REF). However, hand-coding does not track graded changes in action magnitude: they typically report onsets and offsets alone (REF). Without the action gradient, facial dynamics are reduced to binary events that do not differ in topography or temporal quality.
The ideal alternative, Electromyography (EMG), requires wired sensors be placed on skin. This spawns the possibility of participant discomfort, introduces the requirement for resources and limits ecological validity. Automated facial coding may provide an optimal trade-off: non-intrusive instruments that assess magnitude. Cross-correlations will be used to assess the degree to which the opensource auto-coder package (Mémoire IRCGN [https://github.com/LafLaurine/imac2-memoire-ircgn]) can approximate EMG data (Corrugator supercilii) in naturalistic, face-to-face interactions between mother-infant dyads (N - 10 dyads; infant age range 4-6 months). The videos will also be hand-coded enabling for the findings to link to the published literature.
During early life, play is a ubiquitous activity, and an individual’s propensity for play is positively related to cognitive development and emotional well-being. Play behaviour is diverse and multi-faceted. A challenge for current research is to converge on a common definition and measurement system for play ‒ whether examined at a behavioural, cognitive or neurological level. Combining these different approaches in a multi-level analysis could yield significant advances in understanding the neurocognitive mechanisms of play, and provide the basis for developing biologically-grounded play models. However, there is currently no integrated framework for conducting a multi-level analysis of play that spans brain, cognition and behaviour. The proposed neuropsychological coding framework uses grounded and observable behaviours along three neuropsychological dimensions (sensorimotor, cognitive and socio-emotional), to compute inferences about playful behaviour and related social interactional states. Here, we illustrate the sensitivity and utility of the proposed coding framework using two contrasting dyadic corpora (N=5) of mother-infant object-oriented interactions during experimental conditions that were either conducive (Condition 1) or non-conducive (Condition 2) to the emergence of playful behaviour. We find that the framework accurately identifies the modal form of social interaction as being either playful (Condition 1) or non-playful (Condition 2), and further provides useful insights about differences in the quality of social interaction and temporal synchronicity within the dyad. In conclusion, here, we present a novel neuropsychological framework for analysing the continuous time-evolution of adult-infant play patterns, underpinned by biologically informed state coding along sensorimotor, cognitive and socio-emotional dimensions. We expect that the proposed framework will have wide utility amongst researchers wishing to employ an integrated, multi-level approach to the study of play, and lead towards a greater understanding of the neuroscientific basis of play and may yield insights into a new biologically-grounded taxonomy of play interactions.
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.
Spontaneous mimicry (SM) is a ubiquitous feature of human communication (Heyes, 2021; Meltzoff & Williamson, 2017). Research shows that SM is both reflexive and flexible (Wang & Hamilton, 2012). It is sensitive to cues that signify implicit social rules and social hierarchy, suggesting that it is at least partly socially shaped. However, we have yet to map the ontogeny of SM, or its developmental factors (Slaughter, 2021). A marked difference in SM behaviour has been observed in atypical populations (e.g., ASD; Arnold & Winkielman, 2020) increasing the onus for further study. In infants, facial mimicry has been studied extensively and is the central focus of a long running debate surrounding the presence of SM in early infancy (Slaughter, 2021). However, most of these studies have used lab-based tasks or non-naturalistic block-design paradigms (Slaughter, 2021; Meltzoff & Williamson, 2017). The few studies that have observed naturalistic interactions used hand-coded video data, scoring onset and offsets of actions: mimicry was operationalised as an action onset in the observer that occurs within a specific timespan of a prior action onset in the interacting partner (Markodimitraki & Kalpidou, 2019). Here, SM behaviour is gauged in terms of frequency and total number of mimicked actions. They do not measure the magnitude of the action i.e. they cannot record graded changes in action. Employing electromyography (EMG) allows us to decipher moment-to-moment dynamics and sub-second changes.
In the present study, we investigated facial SM behaviour in free-play interactions between 5-months-old infants and their caregivers. EMG electrodes are placed on the facial regions that overly the corrugator supercilii (frowning/eyebrow-movement) in both caregiver and infant. Lab based investigation of SM in infants have found evidence of infant SM of eyebrow movement at this age range (De Klerk et al., 2018). The caregiver and infant were tested while during tabletop free play sessions. The obtained EMG signal is rectified, band-pass filtered and z-scored. Artefacts are rejected by identifying and removing outliers that fall outside of one standard deviation above or below the mean. Cross-correlations are carried out to obtain a comprehensive overview of the temporal correspondence between the partners’ EMG waveforms. Granger causality analyses are also conducted on the EMG-waveforms of the interacting partners to identify if changes in the facial action of one predicts changes in that of the other.
Based on our reading of the literature we had predicted that the cross correlations will be significant when the caregiver’s waveform is lagged (mother mimics the infant) but not when the infant’s waveform is lagged. Our target sample size is 20 dyads, and we are currently at the centriole. In our preliminary analyses (N - 9 dyads), in contrast to our expectations, the cross correlations were significant when the caregiver’s waveform preceded the infant’s (infant’s waveform is lagged). This was seen at lags between .2 and .6 seconds. Granger causality analyses will be performed to test if each of the waveforms can significantly predict the other. Control analysis will be performed with shuffled datasets to rule out spurious results.
During development we transition from co-regulation (where regulatory processes are shared
between child and caregiver) to self-regulation. Most early co-regulatory interactions aim to
manage fluctuations in the infant’s arousal and alertness; but over time, co-regulatory
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 hyper-activity.
Early co-regulatory 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. Contingent responsiveness
operates via negative feedback, through which the behavioural changes from the caregiver
compensate for increases and decreases in the child, to help maintain an intermediate critical
state. Similar principles, of interactive but asymmetric contingency, drive joint attention and
the maintenance of epistemic states as well as arousal/alertness, emotion regulation, and
socio-communicative development. Here, we review work that directly observed child-adult
co-regulatory interactions in the context of psychopathology. Early co-regulatory processes
are thought to play a role in the development of attachment and can develop atypically in a
range of ways, across conditions including premature birth, Autism, Attention Deficit
Hyperactivity Disorder, 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/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
3
from their critical state. We discuss implications of these findings for future intervention
research, and directions for future work.
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'.
Almost all early cognitive development takes place in social contexts. At the moment, however, we know little about the neural and cognitive mechanisms that drive infant attention during social interactions. Recording EEG during naturalistic caregiver-infant interactions (N=66), we compare two different accounts. Attentional scaffolding perspectives emphasise the role of the caregiver in structuring the child’s behaviour, whilst active learning models focus on motivational factors, endogenous to the infant, that guide their attention. Our results show that, already by 12-months, intrinsic cognitive processes control infants’ attention: fluctuations in endogenous oscillatory neural activity associated with changes in infant attentiveness, and predicted the length of infant attention episodes towards objects. In comparison, infant attention was not forwards-predicted by caregiver gaze, or modulations in the spectral and temporal properties of their caregiver’s speech. Instead, caregivers rapidly modulated their behaviours in response to changes in infant attention and cognitive engagement, and greater reactive changes associated with longer infant attention. Our findings suggest that shared attention develops through interactive but asymmetric, infant-led processes that operate across the caregiver-child dyad.
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.
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.
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.
Previous research has suggested that children raised in unpredictable and unresponsive environments show worse executive control of attention. Here, we leverage recent findings from developmental neuroscience to discuss how environmental predictability might facilitate executive control development. We focus on two types of predictability: contingent responsiveness (i.e. ‘every time I do X, then Y happens’), and temporal predictability (i.e. ‘at X time intervals, Y happens’). We discuss the mechanisms through which predictability in one aspect of the environment can drive behavioural sensitivity to that aspect to be selectively increased, relative to other less predictable aspects. This selective enhancement is similar to the effect of executive attention, but driven by external properties of the environment. Thus, predictable aspects of the environment are, in the short term, easier to pay attention to than unpredictable ones. We discuss how these short-term effects can lead to long-term improvements in executive attention control.
Background: It has been hypothesized that resting state cardiac vagal activity (CVA) - an indicator of parasympathetic nervous system activity - is a specific psychophysiological marker of executive control function.
Here, we propose an alternative hypothesis - that CVA is associated with early stage attention orientation,
promoting the flexible uptake of new information, on which the later operation of such executive control
functions depends. We therefore predicted that CVA would predict the interaction between orienting and executive control. This was tested using the revised version of the Attention Network Test (ANT-R) that was
developed to distinguish between orienting and executive attention during a stimulus conflict task.
Methods: Healthy adults (N = 48) performed the ANT-R and their resting CVA was measured over a 5 min period
using ECG recordings.
Results: Multiple regression analyses indicated that, when other factors were controlled for, CVA was more
strongly associated with the interaction between the orienting and executive control terms than with either
factor individually.
Conclusion: Higher levels of CVA are specifically implicated in the modulation of executive control by intrinsic
orientation operating at early stages of conflict detection. These initial findings of higher CVA on orienting
attention in conflict detection need to be replicated in larger samples.
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.
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,
co-occurs with dyadic arousal dysregulation, and could contribute to physiological arousal transmission. Implications for caregiver vocalization
as an intervention target are discussed.
During their early years, infants use the temporal statistics of the speech signal to boot-strap language learning, but the neural mechanisms that facilitate this temporal analysis are poorly understood. In adults, neural oscillatory entrainment to the speech amplitude envelope has been proposed to be a mechanism for multi-time resolution analysis of adultdirected speech, with a focus on Theta (syllable) and low Gamma (phoneme) rates. However, it is not known whether developing infants perform multi-time oscillatory analysis of infantdirected speech with the same temporal focus. Here, we examined infants’ processing of the temporal structure of sung nursery rhymes, and compared their neural entrainment across multiple timescales with that of well-matched adults (their mothers). Typical infants and their mothers (N=58, median age 8.3 months) viewed videos of sung nursery rhymes while their neural activity at C3 and C4 was concurrently monitored using dual-electroencephalography (dual-EEG). The accuracy of infants' and adults' neural oscillatory entrainment to speech was compared by calculating their phase-locking values (PLVs) across the EEG-speech frequency spectrum. Infants showed better phase-locking than adults at Theta (~4.5 Hz) and Alpha (~9.3 Hz) rates, corresponding to rhyme and phoneme patterns in our stimuli. Infant entrainment levels matched adults' for syllables and prosodic stress patterns (Delta,~1-2 Hz). By contrast, infants were less accurate than adults at tracking slow (~0.5 Hz) phrasal patterns. Therefore, compared to adults, language-learning infants' temporal parsing of the speech signal shows highest relative acuity at Theta-Alpha rates. This temporal focus could support the accurate encoding of syllable and rhyme patterns during infants' sensitive period for phonetic and phonotactic learning. Therefore, oscillatory entrainment could be one neural mechanism that supports early bootstrapping of language learning from infant-directed speech (such as nursery rhymes).
Objective. The purpose of the present study was to deepen our understanding of attention (a core cognitive ability) in Rett syndrome (RTT), an x-linked neurodevelopmental disorder caused by mutations in the MECP2 gene. We focused on two key aspects of visual orienting--shifting and disengaging attention--both of which are critical for exploring the visual world. We used gaze-based measures and eye-tracking technology to minimize demands on the limited verbal and motor abilities associated with RTT. Method. Shifting and disengaging attention were examined in 31 children (2-12 years) with Rett Syndrome (RTT) and 31 age-matched typically-developing (TD) controls. Using the gap-overlap paradigm, the frequency/speed of shifting attention from a central to peripheral target were compared on Baseline trials, where the central stimulus disappears as the peripheral target appears, and Overlap trials, where the central stimulus remains, thus requiring disengagement. Results. Our findings revealed that children with RTT had more ‘sticky fixations’(p<.001). That is, they had fewer saccades to the peripheral target than TD children, and this was true on both baseline (77% vs 95%), and overlap trials (63% vs 90%); the younger ones also had slower saccadic reaction times (SRTs)(p=.04). Within the RTT group, SRTs correlated with symptom severity. Surprisingly, disengagement cost (the relative difference between gap and overlap SRTs) did not differ across groups. Conclusion. Our results suggest that children with Rett have difficulty shifting attention and, to a lesser extent, disengaging attention, whereas with other disorders, problems with disengagement are paramount.
Background: Children born preterm may display cognitive, learning, and behaviour difficulties as they grow up. In
particular, very premature birth (gestation age between 28 and less than 32 weeks) may put infants at increased risk
of intellectual deficits and attention deficit disorder. Evidence suggests that the basis of these problems may lie in
difficulties in the development of executive functions. One of the earliest executive functions to emerge around 1
year of age is the ability to control attention. An eye-tracking-based cognitive training programme to support this
emerging ability, the Attention Control Training (ACT), has been developed and tested with typically developing
infants. The aim of this study is to investigate the feasibility of using the ACT with healthy very preterm (VP) infants
when they are 12 months of age (corrected age). The ACT has the potential to address the need for supporting
emerging cognitive abilities of VP infants with an early intervention, which may capitalise on infants’ neural plasticity.
Methods/design: The feasibility study is designed to investigate whether it is possible to recruit and retain VP infants
and their families in a randomised trial that compares attention and social attention of trained infants against those
that are exposed to a control procedure. Feasibility issues include the referral/recruitment pathway, attendance, and
engagement with testing and training sessions, completion of tasks, retention in the study, acceptability of outcome
measures, quality of data collected (particularly, eye-tracking data). The results of the study will inform the development
of a larger randomised trial.
Discussion: Several lines of evidence emphasise the need to support emerging cognitive and learning abilities of
preterm infants using early interventions. However, early interventions with preterm infants, and particularly very
preterm ones, face difficulties in recruiting and retaining participants. These problems are also augmented by the
health vulnerability of this population. This feasibility study will provide the basis for informing the implementation of
an early cognitive intervention for very preterm infants.
Preliminary evidence suggests that changes in DNA methylation, a widely studied epigenetic
mechanism, contribute to the etiology of Autism Spectrum Disorder (ASD). However, data is
primarily derived from post-mortem brain samples or peripheral tissue from adults. Deep-phenotyped longitudinal infant cohorts are essential to understand how epigenetic modifications
relate to early developmental trajectories and emergence of ASD symptoms. We present a proof of-principle study designed to evaluate the potential of prospective epigenetic studies of infant
siblings of children with ASD.
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.
Previous research has suggested that early development may be an optimal period to implement cognitive training interventions, particularly those relating to attention control, a basic ability that is essential for the development of other cognitive skills. In the present study, we administered gaze-contingent training (95 minutes across 2 weeks) targeted at voluntary attention control to a cohort of typical 12-month-old children (N = 24) and sham training to a control group (N = 24). We assessed training effects on (a) tasks involving non-trained aspects of attention control: visual sustained attention, habituation speed, visual recognition memory, sequence learning and reversal learning; (b) general attentiveness (on-task behaviours during testing) and (c) salivary cortisol levels. Assessments were administered immediately following the cessation of training and at a 6-week follow-up. On the immediate post-test infants showed significantly more sustained visual attention, faster habituation and improved sequence learning. Significant effects were also found for increased general attentiveness and decreased salivary cortisol. Some of these effects were still evident at the 6-week follow-up (significantly improved sequence learning and marginally improved […] sustained attention). These findings extend the emerging literature showing that attention training is possible in infancy.
Play during early life is a ubiquitous activity, and an individual’s propensity for play is positively related to cognitive development and emotional well-being. Play behavior (which may be solitary or shared with a social partner) is diverse and multi-faceted. A challenge for current research is to converge on a common definition and measurement system for play – whether examined at a behavioral, cognitive or neurological level. Combining these different approaches in a multimodal analysis could yield significant advances in understanding the neurocognitive mechanisms of play, and provide the basis for developing biologically grounded play models. However, there is currently no integrated framework for conducting a multimodal analysis of play that spans brain, cognition and behavior. The proposed coding framework uses grounded and observable behaviors along three dimensions (sensorimotor, cognitive and socio-emotional), to compute inferences about playful behavior in a social context, and related social interactional states. Here, we illustrate the sensitivity and utility of the proposed coding framework using two contrasting dyadic corpora (N = 5) of mother-infant object-oriented interactions during experimental conditions that were either non-conducive (Condition 1) or conducive (Condition 2) to the emergence of playful behavior. We find that the framework accurately identifies the modal form of social interaction as being either non-playful (Condition 1) or playful (Condition 2), and further provides useful insights about differences in the quality of social interaction and temporal synchronicity within the dyad. It is intended that this fine-grained coding of play behavior will be easily assimilated with, and inform, future analysis of neural data that is also collected during adult–infant play. In conclusion, here, we present a novel framework for analyzing the continuous time-evolution of adult–infant play patterns, underpinned by biologically informed state coding along sensorimotor, cognitive and socio-emotional dimensions. We expect that the proposed framework will have wide utility amongst researchers wishing to employ an integrated, multimodal approach to the study of play, and lead toward a greater understanding of the neuroscientific basis of play. It may also yield insights into a new biologically grounded taxonomy of play interactions.
Aim: This study aims to investigate selective attention in Rett syndrome, a severely disabling neurodevelopmental disorder caused by mutations in the X-linked MECP2 gene.
Method: The sample included 28 females with Rett syndrome (RTT) and 32 age-matched typically
developing controls. We used a classic search task, in conjunction with eye-tracking technology. Each
trial included the target and several distractors. The distractors varied in number and differed from
targets in either a "single feature" (color or shape), creating a pop-out effect, or in a "conjunction of
features" (color and shape), requiring serial search. Children searched for the target in arrays containing
five or nine objects; trials ended when the target was fixated (or 4000 ms elapsed).
Results: Children with Rett syndrome had more difficulty finding the target than typically developing
children in both conditions (success rates less than 50% versus 80%) and their success rates were little
influenced by display size or age. Even when successful, children with RTT took significantly longer to
respond (392 to 574 ms longer), although saccadic latency differences were observed only in the singlefeature condition. Both groups showed the expected slowing of saccadic reaction times for larger arrays
in the conjunction-feature condition. Search failures in RTT were not related to symptom severity.
Conclusions: Our findings provide the first evidence that selective attention, the ability to focus on or
select a particular element or object in the environment, is compromised by Rett syndrome. They
reinforce the notion that gaze-based tasks hold promise for quantifying the cognitive phenotype of RTT
Social learning allows infants to learn vicariously by observing adult behaviour, but how the infant brain accomplishes this feat remains unknown. Here, electroencephalography (EEG) signals were simultaneously measured from forty-seven mothers and infants (10.7 months) during a live social learning task. First, infants observed mothers demonstrate positive or negative emotions toward novel toys. Next, infants’ own toy interaction (learning) was measured. Infants’ social learning likelihood was robustly predicted by mother-infant interpersonal neural connectivity in the Alpha (6-9 Hz) band. Stronger dyadic neural connectedness predicted increased learning, and was associated with extended ostensive eye contact and maternal utterances. Intra-infant neural connectivity predicted learning valence (positive/negative) but was unrelated to learning likelihood. Therefore, interpersonal connectivity is a neural mechanism by which infants learn from their social partners.
Eye-tracking is the principle of tracking participants’ eye movements as they look around a scene. Fundamentally, it can be done in two ways: first, in screen-based tasks, in which viewing materials are presented on a computer monitor, and second, in naturalistic contexts.
Objective. The object of the present study is to advance our understanding of the cognitive
profile of Rett Syndrome (RTT), an x-linked neurodevelopmental disorder caused by mutations
in the MECP2 gene. We focus on sustained attention, which plays a critical role in driving
cognitive growth, and use an innovative, gaze-based task that minimizes demands on the limited
verbal and motor abilities associated with RTT.
Method. The task required the ability to sustain attention on a visual target (a butterfly) whilst
inhibiting a prepotent response to look to moving distractors (trees and clouds) presented in the
peripheral visual field. The sample included children with RTT (N = 32) and their typically
developing (TD) counterparts (N = 32), aged 2-12 years.
Results. Our findings revealed that children with RTT had more difficulty sustaining attention
(with the TD group averaging 60% looking at the butterfly vs only 25% for the RTT group).
Furthermore, they showed that RTT was associated with difficulties in three fundamental factors
influencing sustained attention: engagement, distractibility, and re-engagement. The RTT group
was slower to engage, more distractible, and slower to re-engage.
Conclusion. Our findings suggest there may be a fundamental disruption to sustained attention
in RTT, identifies factors related to this impairment, and points to cognitive areas that could be
assessed in evaluating the usefulness of interventions.
Research from the animal literature suggests that dynamic, ongoing changes in arousal lead to dynamic changes in an individual's state of anticipatory readiness, influencing how individuals distribute their attention to the environment. However, multiple peripheral indices exist for studying arousal in humans, each showing change on different temporal scales, challenging whether arousal is best characterized as a unitary or a heterogeneous construct. Here, in 53 typical 12‐month‐olds, we recorded heart rate (HR), head movement patterns, electrodermal activity (EDA), and attention (indexed via look duration) during the presentation of 20 min of mixed animations and TV clips. We also examined triggers for high arousal episodes. Using cross‐correlations and auto‐correlations, we found that HR and head movement show strong covariance on a sub‐minute scale, with changes in head movement consistently preceding changes in HR. EDA showed significant covariance with both, but on much larger time‐scales. HR and head movement showed consistent relationships with look duration, but the relationship is temporally specific: relations are observed between head movement, HR and look duration at 30 s time‐lag, but not at larger time intervals. No comparable relationships were found for EDA. Changes in head movement and HR occurred before changes in look duration, but not for EDA. Our results suggest that consistent patterns of covariation between heart rate, head movement and EDA can be identified, albeit on different time‐scales, and that associations with look duration are present for head movement and heart rate, but not for EDA. Our results suggests that there is a single construct of arousal that can identified across multiple measures, and that phasic changes in arousal precede phasic changes in look duration. © 2016 Wiley Periodicals, Inc. Dev Psychobiol 58: 623–639, 2016.
Background: Attention deficit hyperactivity disorder (ADHD) is a prevalent neurodevelopmental disorder that can
negatively impact on an individual’s quality of life. It is pathophysiologically complex and heterogeneous with
different neuropsychological processes being impaired in different individuals. Executive function deficits, including
those affecting attention, working memory and inhibitory control, are common. Cognitive training has been promoted
as a treatment option, based on the notion that by strengthening the neurocognitive networks underlying these
executive processes, ADHD symptoms will also be reduced. However, if implemented in childhood or later, when the
full disorder has become well-established, cognitive training has only limited value. INTERSTAARS is a trial designed to
test a novel approach to intervention, in which cognitive training is implemented early in development, before the
emergence of the disorder. The aim of INTERSTAARS is to train early executive skills, thereby increasing resilience and
reducing later ADHD symptoms and associated impairment.
Methods/design: Fifty 10–14-month-old infants at familial risk of ADHD will participate in INTERSTAARS. Infants
will be randomised to an intervention or a control group. The intervention aims to train early attention skills
by using novel eye-tracking technology and gaze-contingent training paradigms. Infants view animated games
on a screen and different events take place contingent on where on the screen the infant is looking. Infants
allocated to the intervention will receive nine weekly home-based attention training sessions. Control group
infants will also receive nine weekly home visits, but instead of viewing the training games during these visits
they will view non-gaze-contingent age-appropriate videos. At baseline and post treatment, infant attention
control will be assessed using a range of eye-tracking, observational, parent-report and neurophysiological
measures. The primary outcome will be a composite of eye-tracking tasks used to assess infant attention skills.
Follow-up data will be collected on emerging ADHD symptoms when the infants are 2 and 3 years old.
Discussion: This is the first randomised controlled trial to assess the potential efficacy of cognitive training as
a prevention measure for infants at familial risk of ADHD. If successful, INTERSTAARS could offer a promising
new approach for developing early interventions for ADHD.
The current 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 non-trained aspects of attention control, including table-top tasks assessing social attention in semi-naturalistic contexts. Transfer effects were found on non-trained 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.
A number of authors have suggested that attention control may be a suitable target for cognitive training in children with autism spectrum disorder. This study provided the first evidence of the feasibility of such training using a battery of tasks intended to target visual attentional control in children with autism spectrum disorder within school-based settings. Twenty-seven children were recruited and randomly assigned to either training or an active control group. Of these, 19 completed the initial assessment, and 17 (9 trained and 8 control) completed all subsequent training sessions. Training of 120 min was administered per participant, spread over six sessions (on average). Compliance with the training tasks was generally high, and evidence of within-task training improvements was found. A number of untrained tasks to assess transfer of training effects were administered pre- and post-training. Changes in the trained group were assessed relative to an active control group. Following training, significant and selective changes in visual sustained attention were observed. Trend training effects were also noted on disengaging visual attention, but no convincing evidence of transfer was found to non-trained assessments of saccadic reaction time and anticipatory looking. Directions for future development and refinement of these new training techniques are discussed.
This article examines the educational efficacy of a learning environment in which children diagnosed with Autism Spectrum Conditions (ASC) engage in social interactions with an artificially intelligent (AI) virtual agent and where a human practitioner acts in support of the interactions. A multi-site intervention study in schools across the UK was conducted with 29 children with ASC and learning difficulties, aged 4--14 years old. For reasons related to data completeness and amount of exposure to the AI environment, data for 15 children was included in the analysis. The analysis revealed a significant increase in the proportion of social responses made by ASC children to human practitioners. The number of initiations made to human practitioners and to the virtual agent by the ASC children also increased numerically over the course of the sessions. However, due to large individual differences within the ASC group, this did not reach significance. Although no evidence of transfer to the real-world post-test was shown, anecdotal evidence of classroom transfer was reported. The work presented in this article offers an important contribution to the growing body of research in the context of AI technology design and use for autism intervention in real school contexts. Specifically, the work highlights key methodological challenges and opportunities in this area by leveraging interdisciplinary insights in a way that (i) bridges between educational interventions and intelligent technology design practices, (ii) considers the design of technology as well as the design of its use (context and procedures) on par with one another, and (iii) includes design contributions from different stakeholders, including children with and without ASC diagnosis, educational practitioners, and researchers.
The use of electroencephalography (EEG) to study infant brain development is a growing trend. In
addition to classical longitudinal designs that study the development of neural, cognitive and behavioural functions, new areas of EEG application are emerging, such as novel social neuroscience
paradigms using dual infant-adult EEG recordings. However, most of the experimental designs, analysis
methods, as well as EEG hardware were originally developed for single-person adult research. When
applied to study infant development, adult-based solutions often pose unique problems that may go
unrecognised. Here, we identify 14 challenges that infant EEG researchers may encounter when designing new experiments, collecting data, and conducting data analysis. Challenges related to the
experimental design are: (1) small sample size and data attrition, and (2) varying arousal in younger
infants. Challenges related to data acquisition are: (3) determining the optimal location for reference
and ground electrodes, (4) control of impedance when testing with the high-density sponge electrode
nets, (5) poor fit of standard EEG caps to the varying infant head shapes, and (6) ensuring a high
degree of temporal synchronisation between amplifiers and recording devices during dual-EEG acquisition. Challenges related to the analysis of longitudinal and social neuroscience datasets are: (7)
developmental changes in head anatomy, (8) prevalence and diversity of infant myogenic artefacts, (9)
a lack of stereotypical topography of eye movements needed for the ICA-based data cleaning, (10) and
relatively high inter-individual variability of EEG responses in younger cohorts. Additional challenges
for the analysis of dual EEG data are: (11) developmental shifts in canonical EEG rhythms and difficulties in differentiating true inter-personal synchrony from spurious synchrony due to (12) common
intrinsic properties of the signal and (13) shared external perturbation. Finally, (14) there is a lack of
test-retest reliability studies of infant EEG. We describe each of these challenges and suggest possible
solutions. While we focus specifically on the social neuroscience and longitudinal research, many of the
issues we raise are relevant for all fields of infant EEG research.
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.
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.
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 parentinfant 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.
Previous infant entrainment research has shown neural entrainment to a wide range of stimuli and amplitude modulated frequencies. However, it is unknown if infants neurally entrain more strongly to some frequencies more than others, and to which low amplitude modulated frequency infants show the strongest entrainment. The current study seeks to address this by testing the neural entrainment of N=23 4–6-month-old infants and N=22 control group adult caregivers while they listened to a range of sinusoidally amplitude modulated beep stimuli at rest (no sound), 2, 4, 6, 8, 10 and 12 Hz. Analysis examined differences across power and phase, regions of interest predetermined by previous literature and by segmented time windows. Results showed that the strongest entrainment was at 2Hz for both adult and infant participants; that there was no significant difference in power and phase, entrainment was occipital temporal and slightly left fronto-central in adults and right fronto-central and left occipito-temporal in infants, leading to some regions of interest used in previous studies being significant in infants and all regions of interest being significant in adults. Segmenting by time window did not show any significant increase or decrease in entrainment over time, but longer time windows showed a stronger entrainment response. In conclusion, it is important to choose appropriate stimulation frequencies when investigating entrainment between stimulation frequencies or across ages; whole head recording is recommended to see the full extent of activation; there is no preference on power vs phase analyses; and longer recordings show stronger effects.
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.
Infant-directed singing has unique acoustic characteristics that may allow even very young infants to respond to the rhythms carried through the caregiver’s voice. The goal of this study was to examine neural and movement responses to live and dynamic maternal singing in 7-month-old infants and their relation to linguistic development. In total, 60 mother-infant dyads were observed during two singing conditions (playsong and lullaby). In Study 1 ( n = 30), we measured infant EEG and used an encoding approach utilizing ridge regressions to measure neural tracking. In Study 2 ( n = 30), we coded infant rhythmic movements. In both studies, we assessed children’s vocabulary when they were 20 months old. In Study 1, we found above-threshold neural tracking of maternal singing, with superior tracking of lullabies than playsongs. We also found that the acoustic features of infant-directed singing modulated tracking. In Study 2, infants showed more rhythmic movement to playsongs than lullabies. Importantly, neural coordination (Study 1) and rhythmic movement (Study 2) to playsongs were positively related to infants’ expressive vocabulary at 20 months. These results highlight the importance of infants’ brain and movement coordination to their caregiver’s musical presentations, potentially as a function of musical variability.
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.
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.
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.
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.
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 [6], 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 [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.
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.
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.
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.
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.
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.
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 [3], 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.
.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.
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.
Background
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.
Methods
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.
Results
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.
Conclusion
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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).
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.