UEL Baby Dev Lab


I.Marriott Haresign, E.A.M.Phillips, M.Whitehorn, L.Goupil, V.Noreika, V.Leong, S.V.Wass

Simulated data showing how event locked phase modulations could give rise to phase-based IBE between two brains. (a) Time series data x and y were subjected to a phase reset at + 200 ms so that they become purely phase locked. Note grey lines show single trial data while blue and green lines indicate data averaged over trials. The increased consistency in phase angle circa + 200 ms between x and y yields (c) a notable increase in the phase-locking between x and y ~200 ms. (b) Simulated data showing a situation in which the phase modulations in one signal (x) predict the phase modulations in another signal (y) and how this lagged/ directed relationship in phase can be captured (d) using phase transfer entropy.

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.

I. Marriott Haresign, E.A.M Phillips, M. Whitehorn, F. Lamagna, M. Eliano, L. Goupil, E.J.H. Jones, S.V. Wass

Distribution of gaze onsets in our sample. A) Distribution of time infants spent looking at different areas. B) Distribution of time dyads spend in mutual and non-mutual gaze during interaction. C) Distribution of look durations for mutual and non-mutual gaze defined from infants’ look behaviour. D) Distribution of time adults spent looking at different areas. E) Distribution of infant sender/ adult receiver mutual and non-mutual gaze onsets. F) Distribution of adult sender/ infant receiver mutual and non-mutual gaze onsets.

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.

Goupil, L., Johansson, P., Halls, L., & Aucouturier, J. J.

Figure 2: (A) Valence, (B) arousal, (C) confidence, (D) fundamental frequency of the nonmodified voice (i.e. input of the manipulation) and (E) fundamental frequency of the modified voice (i.e. output of the manipulation) depending on condition (happy vs. sad) and implicit detection (i.e., acoustic compensation). Ratings were normalized with respect to neutral trials. Error bars represent confidence intervals - * p < 0.05, **p < 0.01, ***p < 0.001.

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.

Goupil, L., Saint-Germier, P., Rouvier, G., Schwarz, D., & Canonne, C.

Figure 2: Raw data. The y-axis corresponds to individual musicians, and the x-axis represents time in seconds. Colors show musicians' reports about their directional intentions upon re-listening to the performance following the collective improvisation. Black horizontal lines show the musical actions of each musicians. Red vertical dotted lines show the boundaries of the musical sequences identified by the expert annotator. Data for the directional intentions of OMB, OMJ and OMH are missing due to a technical error.

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.

Louise Goupil, Thomas Wolf, Pierre Saint‐Germier, Jean‐Julien Aucouturier, Clément Canonne

Fig. 4 Mains results of Experiment 3. (A) Expert and naive listeners' appreciation ratings were averaged separately for each participant, prompt number, and prompt type, before being averaged in the group. Black asterisks show post hoc Tukey HSD comparisons. As reported in the main text, appreciation ratings were highest in the shared goal (WE-3). Participants also preferred the ME-1 condition over the ME-2 (p = .04), ME-3 (p = .04), and WE-2 (p = .001) conditions. Similarly, they preferred the WE-1 condition over the WE-2 condition (p = .007, all other comparisons were nonsignificant). Thus, listeners also preferred conditions in which fewer prompts were present (WE-1 and ME-1 conditions did not differ p > .5). This may be due to the fact that these interactions are less artificial than the others (i.e., only one of the musicians receives a prompt while the other musicians remain unconstrained). Note that musicians in these more natural conditions may also spontaneously form shared intentions, as suggested by the results observed in the first experiment. (B) The percentage of hierarchical, collective, progressive, predictable, and on-time assessment was computed for each of the five qualitative questions, separately for each participant, prompt number, and prompt type, before being averaged in the group. Black asterisks show the logistic regression model comparisons, and the blue asterisk represents the fact that all comparisons were significant with respect to the indicated condition. p < .05; **p < .01; ***p < .001. Error bars show 95% confidence intervals.

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.

Goupil, L., Johansson, P., Hall, L., & Aucouturier, J. J.

Fig. 1. Experimental paradigm. Participants read vignettes depicting familiar emotional scenarios, and then deliberated out loud about how they would feel in these situations. They then summarized their emotional state on a valence scale, an arousal scale and a confidence scale. While they spoke, their voice was covertly manipulated to make it sound happy (i.e., higher fundamental frequency, brighter spectrum) or sad (i.e., lower fundamental frequency, darker spectrum), or remained unchanged (i.e., neutral).

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.

Goupil, L., Ponsot, E., Richardson D., Reyes, G., & Aucouturier, J. J.

a Normalized (z-scored) ratings in the certainty (top, blue; N = 20) and honesty (bottom, green; N = 20) tasks for each participant and prosody type (shown by different hues). Bar plots represent individual participants’ mean normalized ratings for each prosodic archetype, with error bars showing the 95% confidence interval. Data were sorted by effect magnitude. Squared markers below the plot show the listener’s gender (black: female; gray: male). Asterisks show the results of paired two-sided sample t tests comparing reliable versus unreliable prosodies for each individual listener, with *p < 0.05; **p < 0.01; ***p < 0.001 (individual p values are reported in the Source data file). At the level of the group, in the certainty task, both honest and certain prosodies were judged as more certain than doubtful (honest: p < 0.001 Bonferroni corrected post hoc Tukey HSD, d = 3.72; certain: p < 0.001, d = 4.14) and lying (honest: p < 0.001, d = 3.23; certain: p < 0.001, d = 3.72) prosodies. In the honesty task, greater inter-individual differences were observed (see detailed report in the main text). b Normalized ratings were split depending on participants’ responses at the explicit questions assessing their conceptual knowledge about epistemic prosody, which revealed that the relationship between prosody type and ratings did not vary with participants’ conceptual knowledge about certainty and honesty in general, with the exception of concepts about speed in the honesty task (shown by the green asterisk that represent the significant interaction between concepts about speed and prosody type on ratings of honesty). Data are presented as mean values with error bars showing the 95% confidence interval. Triple asterisks (***) show the significant results of the rmANOVA testing the interaction between concepts about speed and prosody in the honesty task, with normalized ratings as a dependent variable, p = 0.0007 (all other interactions were not significant). Source data and exact individual p values for a are provided as a Source data file.

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.

Wass, S., Phillips, E., Smith, C., Fatimehin, E., & Goupil, L.

Figure 3 – Arousal stability and coupling around vocalisations. a) Infant arousal stability relative to caregiver vocalisations; b) infant arousal stability relative to infant vocalisations; c) infant arousal stability relative to infant cries; d) infant arousal stability relative to infant speech-like vocalisations; e) caregiver arousal stability relative to caregiver vocalisations; f) caregiver arousal stability relative to infant vocalisations; g) caregiver arousal stability relative to infant cries; h) caregiver arousal stability relative to infant speech-like vocalisations; i) infant-caregiver arousal coupling relative to caregiver vocalisations; j) infant-caregiver arousal coupling relative to infant vocalisations; k) infant-caregiver arousal

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.

Ballieux, H., Wass, S., Tomalski, P., Kushnerenko, E., Karmiloff-Smith, A., Johnson, M., & Moore, D.

Fig. 1. Schematics of the four training tasks administered. Dashed rectangles indicate active areas and arrows indicate objects that were moving on screen (both were not visible in the original materials). a) Task 1 (Butterfly): the butterfly (indicated in red) scrolled from left to right as long as the child looked directly at it, with static and moving (indicated in blue) distractors presented in the child's peripheral visual field. If the child looked to any of the distractors, they disappeared and the scrolling stopped. b) Task 2 (Stars): a target (indicated red) was presented on screen along with a number of static and moving (indicated blue) distractors. If the child looked to the target within a time window, he or she received a reward. Both target and distractors changed between trials. c) Task 3 (Windows): a target (indicated red) was presented in one location on screen. All four windows then closed and fixation target (the red flower) appeared for a variable inter-stimulus interval. After the fixation target disappeared, a look back to the cued window triggered a reward. d) Task 4 (Suspects): a target (indicated red) was presented along with a range of distractors. If the child looked to the target within a time window, he or she received a reward. Once per block of 12 trials the target changed. Targets from the previous block (indicated yellow) were presented concurrently with the current target, as distractors.

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.

Wass, S., & Leong, V.

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.

deBarbaro, K., Clackson, K., & Wass, S.

FIGURE 1 Schematics showing the three tasks administered. (a) Habituation task. (b) Visualrecognition memory task. (c) Stress reactivity task.

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.

Leong, V., Byrne, E., Clackson, K., Gergieva, S., Lam, S., & Wass S.

Fig. 1. Illustration of experimental protocols and connectivity analysis. (A) In experiment 1, infants viewed a video screen showing an experimenter reciting nursery rhymes. Three gaze conditions were presented interleaved: direct, indirect (head averted by 20°), and direct-oblique (head averted by 20°, direct gaze). The infant’s live EEG was compared with the adult’s prerecorded EEG. (B) In experiment 2, infant and adult sat opposite each other. Direct and indirect gaze (head averted by 20°) conditions were presented. (C) The adult–infant network comprised left (L) and right (R) electrodes each from the infant and adult. Interpersonal neural connectivity was assessed across all pairwise connections between electrodes using partial directed coherence. (D) Examples of infant and adult EEG data, which were analyzed within Theta (3–6 Hz) and Alpha (6–9 Hz) bands.

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.

Wass, S., de Barbaro, K., Clackson, K., & Leong, V.

Figure 2. Fourier-derived power spectra for changes in arousal, split using a median split into low and high visual sustained attention groups. (A) Individual data. (B) Same as A, but averaged into high and low sustained attention groups. (C) Scatterplot showing the relationship between arousal power and look duration. (D) Scatterplot showing the relationship between heart rate (HR) change to stressor and look duration. (E) Scatterplot showing the relationship between HR change to stressor and arousal power. On each scatterplot, linear best-fit lines illustrate the significant bivariate relationships observed between the variables. See the online article for the color version of this figure.

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.

Wass, S.

Fig. 2. Schematic from Aston-Jones and Cohen. At mid-level, Tonic LC activity, phasic (event-related) LC changes are greater and the capacity to maintain focused attention is increased. At both hypo- and hyper-tonic arousal, phasic LC changes are reduced and the capacity to maintain focused attention is lower (Figure from Aston-Jones and Cohen, 2005).

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.

Wass, S., Clackson, K., & Leong, V.

Figure 1 Schematic illustrating different ways of conceptualizing spontaneous changes in arousal.(a) Model 1—a random, stochastically varying model. (b) Histogram showing arousal levels across theentire sample in Model 1. A Gaussian distribution has been superimposed in red for illustrativepurposes. (c) Model 2—an oscillatory “inertia” model, in which arousal at one moment is contingenton arousal at the previous moment, together with random, stochastic changes. (d) Histogram showingarousal levels across the entire sample in Model 2. Again, these are normally distributed. (e) Model 3—similar to Model 2, but with the addition that episodes of high arousal are more likely to bemaintained than episodes of low arousal. (f) Histogram showing arousal levels across the entiresample in Model 3. A Gaussian distribution has been superimposed in red, for illustrative purposes.The histogram shows that results are positively skewed.

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.

Wass, S., Clackson, K., Georgieva, S., Brightman, L., Nutbrown, L., & Leong, V.

Figure 5 (a) Bivariate relationship between infant attention durations to Object during Solo Play and Joint Play. (b) Bivariate relationship between parent and infant attention durations to object during Joint Play. (c) Bivariate relationship between PACF and look durations during Solo Play and Joint Play; (d) PACF—comparison of the PACF values for look durations towards the object in the Joint Play and Solo Play conditions for the infant alone

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.

Wass, S., Noreika, V., Georgieva, S., Clackson, K., Brightman, L., Nutbrown, R., Santamaria Covarrubias, L., & Leong, V.

Figure 2. Neural Activity in the Parent Entrains to Attentional Fluctuations in the Child. (A) Schematic illustrating the analysis; (B) cross-correlation between child EEG and child gaze, showing an association between child neural activity and child attention; (C) cross-correlation between adult EEG and adult gaze, also showing an association between adult neural activity and adult attention; (D) cross-correlation between adult EEG and child gaze, showing an association between the adult’s neural activity and the child’s attention. Subsequent analyses showed that the association between the adult’s neural activity and the child’s attention was independent of the adult’s own attention. Whereas the child EEG–child gaze and adult EEG–adult gaze relationships were predictive (i.e., strongest associations were found between neural activity at a given moment and attention c. 750 ms after that moment), the adult EEG–child gaze associations were reactive (i.e., strongest associations were found between the child’s attention at a given moment and the adult’s neural activity c. 750 ms after that moment). Reproduced, with permission, from [43]. Abbreviation: EEG, electroencephalography.

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.

Wass, S., Smith, C., Clackson, K., Gibb, C., Eitzenberger, J., & Mirza, F.

Figure 3. Results of Analyses 3–5 (A) Analysis 3—moments in which the infant’s autonomic arousal exceeded the 95th percentile for that individual were identified. The average adult arousal levels during the period from 540 s before to 540 s after that moment were calculated. For all figures, error bars show the SE, and segments in red indicate the areas of significant (p < 0.05) event-related change as identified by the permutation-based temporal clustering analysis (STAR Methods). (B) Analysis 3—changes in adult arousal levels during the period from 540 s before to 540 after an infant’s most negative affect vocalizations. (C) Analysis 3—changes in adult arousal levels during the period from 540 s before to 540 after an infant’s most positive affect vocalizations. (D) Analysis 4—changes in infant-adult arousal cross-correlation relative to peak negative and positive affect vocalizations. Stars indicate the areas of significant (p < 0.05) event-related change as identified by the permutation-based temporal clustering analysis. (E) Analysis 5—schematic illustrating the procedure used to generate the results in (G). First, we identified instances of peak (>95th percentile) arousal from the infant. Second, we examined how the adult’s arousal changed in the 60 s after, relative to before, that moment. Third, we examined how the change in adult’s arousal predicted the infant’s subsequent arousal across a variety of time windows between 0–60 and 240–300 s after the event. (F) Analysis 5—sample scatterplot illustrating the relationship observed during one recovery window. (G) Analysis 5—plot showing the recovery window (seconds post-event in the infant data) on the x axis and the β value of the linear mixed effects model on the y axis. Red dashed line indicates the p value cutoff for individual linear mixed effects models; results were subsequently corrected for multiple comparisons using a permutation-based cluster analysis. Results indicated that greater increases in adult arousal relative to the event were associated with lower infant arousal during the minutes after the event.

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.

Wass, S.

.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.

Wass, S., Daubney, K., Golan, J., Logan, F., & Kushnerenko, E.

Fig. 2. a and b) - topoplots for responses to the Standard trials, split by the participants’ mean HR across the entire testing session. The figure above each time plot indicates the mean time of each bin, in ms, relative to stimulus onset. Only the time intervals 100–200 ms and 250–350 ms, corresponding to the main ERP peaks, are shown. Results for other time intervals are shown in the SM (Fig. S6). The colour bar indicates the voltage, in μV. a) High HR group; b) Low HR group. c) ERP response to the Standard trials, subdivided into the low HR group (red) and the high HR group (blue) and downsampled to 20 ms. Shaded areas represent the error bars, calculated as the Standard Error of the Mean. d) Scatterplot showing the significant relationship observed between mean HR and peak amplitude of the N250 on Standard trials.

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.

Smith, C., Jones, E., Charman, T., Clackson, K., Mirza, F., & Wass, S.

Fig. 4. (a)–(b) Vector plot illustrating transitions between arousal bins, contingent on starting arousal state. (a) Shows non-anxious (low GAD-7) group; (b) shows anxious (high GAD-7) group. Data were averaged into 60-s epochs and binned from 1 (low) to 6 (high), for infant and parent separately. Thus, an epoch classified as (1, 1) indicates an epoch in which both infant and parent were in a low arousal state. The red line indicates the average direction of travel between that and the subsequent epoch, averaged across all epochs in that bin. Thus, for the position (1, 1) on plot (a), the red line shows a displacement of +0.3 on the x-axis and +0.4 on the y-axis, indicating that the average epoch starting at (1, 1) showed an increase of +0.3 in infant arousal and +0.7 in adult arousal to the subsequent epoch. (c) schematic illustrating the analysis whose results are shown in (d). Each vector plot was divided into four quadrants: Parent low/Infant low (yellow, 1), Parent low/ Infant high (red, 2), Parent high/Infant low (brown, 3), and Parent high/Infant high (green, 4). In order to investigate how infant arousal and adult arousal interacted to predict the change in adult arousal, we subtracted the average adult change scores in quadrant 4 from quadrant 3, and quadrant 2 minus quadrant 1. This was performed separately for the two groups. (d) bar chart showing the results of the analysis: when the adult’s arousal starts high, their arousal decreases more in instances where the infant’s arousal is high, than when it is low (low GAD-7 group only). * indicates the significance of the analyses comparing the observed values to a chance level of 0. *p < 0.05, †p = 0.05.

Interpersonal processes influence our physiological states and associated affect. Physiological arousal dysregulation, a core feature of anxiety disorders, has been identified in children of parents with elevated anxiety. However, little is understood about how parent–infant interpersonal regulatory processes differ when the dyad includes a more anxious parent.

We investigated moment-to-moment fluctuations in arousal within parent-infant dyads using miniaturised microphones and autonomic monitors. We continually recorded arousal and vocalisations in infants and parents in naturalistic home settings across day-long data segments.

Our results indicated that physiological synchrony across the day was stronger in dyads including more rather than less anxious mothers. Across the whole recording epoch, less anxious mothers showed responsivity that was limited to ‘peak’ moments in their child's arousal. In contrast, more anxious mothers showed greater reactivity to small-scale fluctuations. Less anxious mothers also showed behaviours akin to ‘stress buffering’ – downregulating their arousal when the overall arousal level of the dyad was high. These behaviours were absent in more anxious mothers.

Our findings have implications for understanding the differential processes of physiological co-regulation in partnerships where a partner is anxious, and for the use of this understanding in informing intervention strategies for dyads needing support for elevated levels of anxiety.

Wass, S., Smith, C., Daubney, K., Suata, Z., Clackson, K., Begum, A., & Mirza, F.

Figure 3(A) Cross-correlation plot showing the relationship between auditory noise and autonomic arousal in the home data. For allplots, red shows the low-noise group and blue the high-noise group. Shaded areas show the standard error of the means. (B) Histogramsshowing the cross-correlation values for time lag = 0 only from (A). (C) RR interval changes to a novel attention-eliciting event in thelaboratory battery. Shaded areas show the S.E. Star indicates the area of significant difference identified by the permutation test*p<.05. (D) Look durations during the period5 to 0, 0 to 15 and 15 to 30 s relative to stimulus change. Stars indicate areas ofsignificant difference–*p<.05; (*)p<.10. (E) Look durations during the secondary sustained attention task (described Appendix S1,section 1.6)

Previous research has suggested that children exposed to more early-life stress show worse mental health outcomes and impaired cognitive performance in later life, but the mechanisms subserving these relationships remain poorly understood.

Using miniaturised microphones and physiological arousal monitors (electrocardiography, heart rate variability and actigraphy), we examined for the first time infants’ autonomic reactions to environmental stressors (noise) in the home environment, in a sample of 82 12-month-old infants from mixed demographic backgrounds. The same infants also attended a laboratory testing battery where attention- and emotion-eliciting stimuli were presented. We examined how children's environmental noise exposure levels at home related to their autonomic reactivity and to their behavioural performance in the laboratory.

Individual differences in total noise exposure were independent of other socioeconomic and parenting variables. Children exposed to higher and more rapidly fluctuating environmental noise showed more unstable autonomic arousal patterns overall in home settings. In the laboratory testing battery, this group showed more labile and short-lived autonomic changes in response to novel attention-eliciting stimuli, along with reduced visual sustained attention. They also showed increased arousal lability in response to an emotional stressor.

Our results offer new insights into the mechanisms by which environmental noise exposure may confer increased risk of adverse mental health and impaired cognitive performance during later life.

Wass, S., Whitehorn, M., Marriott-Haresign, I/, Phillips, E., & Leong, V.

Figure 3. Schematic Illustrating a Mechanistic Role for Interpersonal Entrainment during Early Learning. In a mutual responsive interaction, there is a mutual timely exchange of phase-resetting cues between partners. Social ostensive signals may act as synchronizing cues that trigger transient increases in interpersonal entrainment through phase-resetting, leading subsequently produced maternal speech to arrive at a high receptivity phase for optimal encoding by the infant.

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.

Wass, S., Marriott-Haresign, I., Whitehorn, M., Clackson, K., Georgieva, S., Noreika, V., & Leong, V.

Figure 5: Time-lagged associations between attention and brain activity. a-d show results at anterior locations (see text); e-h show the posterior locations. a & e show infant attention to infant brain (these are similar to those shown in Figure 2, but included here for comparison); b & f show adult attention to adult brain activity; c & g show infant attention to adult brain activity; d & h show adult attention to infant brain activity. In each case, the x-axis indicates the variable time delays used to calculate the time-laggedrelationship between attention and brain activity, from -10 (brain activity preceding attention by 10 seconds) to +10 (brain activity post attention by 10 seconds). The y-axis indicates the different frequencies of brain activity, from 2 to 16Hz. Colour bar shows the strength of the association between attention and neural activity, indexed as a Mann Whitney Z value.

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.

Marriott-Haresign, I., Phillips, E., Whitehorn, M., Noreika, V., Jones, E., Leong, V., & Wass, S.

Fig. 3. Application of different ICA classification systems to ocular artifact correction in a visual processing ERP study. A) Two-sample frames from which the time-locked gaze shift (-100ms) were identified, and a schematic showing the experimental set up in which mothers were asked to perform a puppet show with their infants. B)Grand average ERPs over frontal pole, central and occipital scalp regions. Different lines show data cleaned by the different systems, e.g., iMARA- retrained infant classifier, MARA- original classifier, Manual classification and also uncleaned 'raw' data. C)Topoplots of ERP amplitudes, comparing the different cleaning methods to the raw data.

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.

Reindl, V., Wass, S., Leong, V., Scharke, W., Wistuba, S., Wirth, C., Konrad, K., & Gerloff, C.

Fig. 1. Multimodal data analysis workflow. To examine the relationship between different biobehavioral synchrony measures in a single multivariate generative model, we proposed a symmetric data fusion approach, analyzing synchrony in fNIRS and IBI signals concurrently. Top: After motion artifact correction and detrending of the fNIRS signals, the salient wavelet coherence was calculated as the connectivity estimator. Subsequently, for each dyad and condition, individual bipartite graphs were constructed by defining the salient wavelet coherence as weighted edges connecting different regions (nodes) from adult and child. To avoid spurious connections, the graphs were reduced by a block-wise permutation procedure comparing individual graphs with the graphs of shuffled adult-child pairs. The number of surviving connections between brains was calculated for the network (global density) as well as for each node / fNIRS channel (nodal density). To reduce the dimensionality of the nodal metrics while preserving interpretability, nodal density vectors were encoded via non-negative matrix factorization. Bottom: ANS synchrony was calculated by the cross-correlation of the participant’s IBI time series after R-peak correction and ARIMA modeling. Subsequent analyses were performed using (multivariate) Bayesian hierarchical models.

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.

Phillips, E., Wass, S.

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.

Marriott-Haresign, I., Phillips, E., Whitehorn, M., Goupil, L., & Wass, S.

Figure 3. Simulated data showing different mechanisms that that could give rise to increases in interbrain granger causality between parents and infants. (a) shows the two correlated (single-trial amplitude) transient signals x and y. Y was generated from previous samples of x with a lag of 100ms, such that (d) there is a substantial event locked increase in GC from x to y but no GC influence from y to x. (b) shows time-frequency power from signal x from panel a. (c) shows time-frequency power from signal y from panel a. (e) shows spectral GC from y to x and (g) from x to y.

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.

Wass, S.

Figure 5. Schematic illustrating the different types of allostatic and metastatic processes that can be identified in time series data. The schematics show different possible relationships between a dependent variable (DV) (such as infant arousal) and an independent variable (IV) (such as parent arousal). (a) Allostatic mechanism where increased values of the IV associate with decreases in the DV (i.e., DVt+1 = DVt − IVt). The sequence shows an increase in the IV, which occurs in response an increase in the DV, leading to a decrease in the DV. (b) Allostatic mechanism where DVt+1 = DVt + IVt. A decrease in the IV, which occurs in response to an increase in the DV, leads to a decrease in the DV. (c) Metastatic relationship where increased values of the IV associate with decreases in the DV (i.e., DVt+1 = DVt − IVt). A decrease in the IV, which occurs in response to an increase in the DV, leads to a further increase in the DV. (d) Metastatic relationship where DVt+1 = DVt + IVt. In increase in the IV, which occurs in response to an increase in the DV, is followed by a further increase in the DV.

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.

Wass, S., Smith, C., Clackson, K., & Mirza, F.

Fig 1 (a) The Yerkes and Dodson Law (Yerkes & Dodson, 1908). Diamond, Campbell, Park, Halonen, and Zoladz (2007) describe this version of the Law as that found in five decades of publications and books on memory, such as in Hebb (1955), Loftus (1980), and Radvansky (2006). (b) Diamond et al.'s (2007) depiction of the original version of the Law, based on the actual findings of Yerkes and Dodson on fear conditioning in mice. The original version captures the observation that strong emotionality can enhance performance under simple learning conditions. Under more difficult learning conditions, strong emotionality attenuates performance. Simple learning conditions would involve, for example, focused attention on a restricted range of cues, while complex or difficult learning conditions would involve, for example, divided attention, multi-tasking, or greater working memory demands. Figure is adapted from Diamond et al. (2007, Figure 2).

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.

Whiting, S., Wass, S., Green, S., & Thomas, M.

Fig 1 (a) The Yerkes and Dodson Law (Yerkes & Dodson, 1908). Diamond, Campbell, Park, Halonen, and Zoladz (2007) describe this version of the Law as that found in five decades of publications and books on memory, such as in Hebb (1955), Loftus (1980), and Radvansky (2006). (b) Diamond et al.'s (2007) depiction of the original version of the Law, based on the actual findings of Yerkes and Dodson on fear conditioning in mice. The original version captures the observation that strong emotionality can enhance performance under simple learning conditions. Under more difficult learning conditions, strong emotionality attenuates performance. Simple learning conditions would involve, for example, focused attention on a restricted range of cues, while complex or difficult learning conditions would involve, for example, divided attention, multi-tasking, or greater working memory demands. Figure is adapted from Diamond et al. (2007, Figure 2).

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.

Wass, S., Phillips, E., Smith, C., & Goupil, L.

Figure 3. (a) Likelihood of high-intensity caregiver vocalizations around caregiver arousal peaks. Y-axis shows the effect size of the difference between the observed and the control data for the high GAD-7 (blue) and the low GAD-7 (red) groups, calculated as described in the Methods. Yellow circles indicate results showing a significant difference between the observed and the control data. (b) Violin plot showing the proportion of high-intensity caregiver vocalizations. No significant difference was observed between groups. (c) Violin plot showing one sample time-window of the analysis iterated across multiple time windows in (d) and (e). The plot shows the likelihood of a high-intensity vocalization in the time window 10 min prior to a high-intensity vocalization. The effect size of the real versus control comparison has been drawn separately for the high and low GAD-7 groups in (d). (d) Line plot showing the same comparison as shown in (c), but iterated across multiple time windows (i.e., examining the likelihood of the high-intensity vocalization in the time window 9 min prior to a high-intensity vocalization, and so on). Where a circle has been drawn, this indicates a timepoint where a significant difference was observed between the real and control data, following the statistical steps described in the Methods. (e) the same plot examining low-intensity vocalizations. For both groups, significant increases are only observed for the time window up to 5 min before and after each vocalization.

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.

Samuel V Wass, Celia G Smith, Louise Stubbs, Kaili Clackson, & Farhan U Mirza

Figure 2 Panel a: Sample illustrations showing respiratory sinus arrhythmia (RSA) in the heart rate data (see e for group comparison). The sample illustrates the change in heart rate during the first 40 min of sleep in two infants—one showing low RSA (top) and one high RSA (bottom). Panel b: Excerpts showing a 15-s segment of data from the same two samples. Panel c: Poincaré plots of the two samples, illustrating greater interbeat variability in the lower sample. Panel d: Fourier plots of the two samples, illustrating increased power in the 0.5-Hz range, corresponding to the respiration cycle. Panel e: Scatterplot show- ing mean RSA during all data recorded while the infants were at home and awake, subdivided into HD/LD groups using a median split. Horizontal bars show the per-group means. Panel f: Schematic illustrating the visual recognition memory task. Panel g: Schematic illustrating the sustained attention task. Panel h: Schematic showing the still face task. Panel i: Illustration of how eye-tracker data were coded for visual recognition memory task. Panel j: Sustained attention—change in heart rate over time relative to the appearance of an attractive, attention-eliciting stimulus, subdivided by HD/LD group; k) change in heart rate over time during free play/still face task, subdivided by HD/LD group. For Panels j and k, star shows the area identified as showing significant group differences in the cluster-based permutation analysis. For Panels j and k, shaded areas show the standard error. BPM = beats per minute; RMSSD = root mean square of successive differences. See the online article for the color version of this figure.

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.

Smith, C., Jones, E., Wass, S., Pasco, G., Johnson, M., Charman, & Wan, M.

Figure 1: Schematic showing the relationships between variables in the moderation analyses (Hypotheses 1–2) and mediation analysis (Hypothesis 3). Labels a, b and c’ are path coefficients representing standardised coefficients; the c-prime path refers to the direct effect. *p < 0.01

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.

Wass, S.

Fig. 1. Schematic illustrating the Aston-Jones framework. Extreme low, and high, levels of tonic arousal are both associated with lower effortful control and with lower phasic arousal responses to sought-for stimuli. Figure redrawn from Aston-Jones & Cohen, 2005.

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.

Wass, S.

Figure 5: Schematic illustrating negative and positive feedback loops, as commonly used in electronics, which can be used as a metaphor for understanding allostatic (dynamic self-regulatory processes) and metastatic (dynamic dysregulatory processes). The circuit represents a system with gain (G) and feedback (β). Vin and Vout show the input and output. The summing junction at its input subtracts the feedback signal from the input signal to form the error signal Vin − βG, which drives the system. In an allostatic system, the feedback term β is negative. This is also known as negative, or degenerative feedback –similar to allostasis. In a positive feed-back system, the feedback term is positive and so feedback increases the overall gain of a system. This is also knownas positive, or amplificatory feedback –similar to metastasis.

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.

Wass, S., Perapoch Amadó, M., & Ives, J.

Figure 2: Illustrating three differed mechanisms through which information presented might be optimised to arrive at times of peak neuronal excitability. a) a classical ‘top-down’ entrainment model, top-down modulation changes the phase of the underlying neuronal activity to align the neuronal oscillatory activity with the attended-to sensory stream; b) top-down modulation in anticipation to aperiodic stimuli; c) an illustration of the ‘dumb’ oscillator mechanism described in section 5.2.2. Phase changes evoked by the previous stimulus might continue to ‘reverberate’ via a damped response, thus ensuring that the subsequent stimulus also arrives at an optimal phase for encoding

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.

Phillips, E., Goupil, L., Marriott-Haresign, I., Bruce-Gardyne, E., Csolsim, F. A., Whitehorn, M., Leong, M., Wass., S.

Figure 6. Example data collected during one five minute interaction for one dyad, camera angles used for coding and EEG montage. a) Raw data sample, showing (from top) infant EEG over fronto-central electrodes, after pre-processing, infant gaze behaviour, infant vocalisations, adult EEG over fronto-central electrodes, adult gaze behaviour, adult vocalisations. b) Example of interpolated looks (thin black lines) superimposed on parent and infant looking behaviour before interpolation (thick grey lines). Coloured dashed lined indicate different look types in the infant gaze time series (top). Spike trains for infant and caregiver looks, coloured according to look type (bottom). c) Example camera angles for caregiver and infant (right and left), as well as zoomed in images of caregiver and infant faces, used for coding. d) Topographical map showing electrode locations on the bio-semi 32-cap; fronto-central electrodes included in the infant time-frequency analysis are highlighted in grey.

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).

Wass, S., Goupil, L., Smith, C., & Greenwood, E.

Line graphs showing average infant arousal around different types of vocalisations, split by median split into children from low (blue) and high (red) chaos households. a) Negative affect vocalisations; b) positive affect vocalisations; c) low intensity vocalisations; d) high intensity vocalisations. Shaded areas show standard error *- sections identified as showing significant group differences by the permutation-based cluster analysis *<.05.

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.