The development of the relationship between auditory and visual neural sensitivity and autonomic arousal from 6 m to 12 m.

The differential sensitivity hypothesis argues that environmental sensitivity has the bivalent effect of predisposing individuals to both the risk-inducing and development-enhancing influences of early social environments. However, the hypothesis requires that this variation in environmental sensitivity be general across domains. In this study, we focused on neural sensitivity and autonomic arousal to test domain generality. Neural sensitivity can be assessed by correlating measures of perceptual sensitivity, as indexed by event-related potentials (ERP) in electrophysiology. The sensitivity of autonomic arousal can be tested via heart rate changes. Domain generality was tested by comparing associations in perceptual sensitivity across auditory and visual domains, and associations between sensitivity in sensory domains and heart rate. We contrasted ERP components in auditory (P3) and visual (P1, N290 and P4) detection-of-difference tasks for N = 68 infants longitudinally at 6 and 12 months of age. Domain generality should produce correlated individual differences in sensitivity across the two modalities, with higher levels of autonomic arousal associating with increased perceptual sensitivity. Having controlled for multiple comparisons, at 6 months of age, the difference in amplitude of the P3 component evoked in response to standard and deviant tones correlated with the difference in amplitude of the P1 N290 and P4 face-sensitive components evoked in response to fearful and neutral faces. However, this correlation was not found at 12 months of age. Similarly, autonomic arousal correlated with neural sensitivity at 6 months but not at 12 months. The results suggest bottom-up neural perceptual sensitivity is domain-general across auditory and visual domains and is related to autonomic arousal at 6 months but not at 12 months of age. We interpret the development of the association of these markers of ES within a neuroconstructivist framework and with respect to the concept of interactive specialisation. By 12 months of age, more experience of visual processing may have led to top-down endogenous attention mechanisms that process visual information in a way that no longer associates with automatic auditory perceptual sensitivity.

Gaze onsets during naturalistic infant-caregiver interaction associate with 'sender' but not 'receiver' neural responses, and do not lead to changes in inter-brain synchrony.

Temporal coordination during infant-caregiver social interaction is thought to be crucial for supporting early language acquisition and cognitive development. Despite a growing prevalence of theories suggesting that increased inter-brain synchrony associates with many key aspects of social interactions such as mutual gaze, little is known about how this arises during development. Here, we investigated the role of mutual gaze onsets as a potential driver of inter-brain synchrony. We extracted dual EEG activity around naturally occurring gaze onsets during infant-caregiver social interactions in N = 55 dyads (mean age 12 months). We differentiated between two types of gaze onset, depending on each partners' 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.

Oscillatory entrainment to our early social or physical environment and the emergence of volitional control.

An individual's early interactions with their environment are thought to be largely passive; through the early years, the capacity for volitional control develops. Here, we consider: how is the emergence of volitional control characterised by changes in the entrainment observed between internal activity (behaviour, physiology and brain activity) and the sights and sounds in our everyday environment (physical and social)? We differentiate between contingent responsiveness (entrainment driven by evoked responses to external events) and oscillatory entrainment (driven by internal oscillators becoming temporally aligned with external oscillators). We conclude that ample evidence suggests that children show behavioural, physiological and neural entrainment to their physical and social environment, irrespective of volitional attention control; however, evidence for oscillatory entrainment beyond contingent responsiveness is currently lacking. Evidence for how oscillatory entrainment changes over developmental time is also lacking. Finally, we suggest a mechanism through which periodic environmental rhythms might facilitate both sensory processing and the development of volitional control even in the absence of oscillatory entrainment.

Measuring the temporal dynamics of inter-personal neural entrainment in continuous child-adult EEG hyperscanning data.

Current approaches to analysing EEG hyperscanning data in the developmental literature typically consider interpersonal entrainment between interacting physiological systems as a time-invariant property. This approach obscures crucial information about how entrainment between interacting systems is established and maintained over time. Here, we describe methods, and present computational algorithms, that will allow researchers to address this gap in the literature. We focus on how two different approaches to measuring entrainment, namely concurrent (e.g., power correlations, phase locking) and sequential (e.g., Granger causality) measures, can be applied to three aspects of the brain signal: amplitude, power, and phase. We guide the reader through worked examples using simulated data on how to leverage these methods to measure changes in interbrain entrainment. For each, we aim to provide a detailed explanation of the interpretation and application of these analyses when studying neural entrainment during early social interactions.

Infant Effortful Control Mediates Relations Between Nondirective Parenting and Internalising-Related Child Behaviours in an Autism-Enriched Infant Cohort.

Internalising problems are common within Autism Spectrum Disorder (ASD); early intervention to support those with emerging signs may be warranted. One promising signal lies in how individual differences in temperament are shaped by parenting. Our longitudinal study of infants with and without an older sibling with ASD investigated how parenting associates with infant behavioural inhibition (8-14 months) and later effortful control (24 months) in relation to 3-year internalising symptoms. Mediation analyses suggest nondirective parenting (8 months) was related to fewer internalising problems through an increase in effortful control. Parenting did not moderate the stable predictive relation of behavioural inhibition on later internalising. We discuss the potential for parenting to strengthen protective factors against internalising in infants from an ASD-enriched cohort.

Anxious parents show higher physiological synchrony with their infants.

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.

Automatic classification of ICA components from infant EEG using MARA.

Automated systems for identifying and removing non-neural ICA components are growing in popularity among EEG researchers of adult populations. 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.

Elevated physiological arousal is associated with larger but more variable neural responses to small acoustic change in children during a passive auditory attention task.

Little is known of how autonomic arousal relates to neural responsiveness during auditory attention. We presented N = 21 5-7-year-old children with an oddball auditory mismatch paradigm, whilst concurrently measuring heart rate fluctuations. Children with higher mean autonomic arousal, as indexed by higher heart rate (HR) and decreased high-frequency (0.15-0.8 Hz) variability in HR, showed smaller amplitude N250 responses to frequently presented (70%), 500 Hz standard tones. Follow-up analyses showed that the modal evoked response was in fact similar, but accompanied by more large and small amplitude responses and greater variability in peak latency in the high HR group, causing lower averaged responses. Similar patterns were also observed when examining heart rate fluctuations within a testing session, in an analysis that controlled for between-participant differences in mean HR. In addition, we observed larger P150/P3a amplitudes in response to small acoustic contrasts (750 Hz tones) in the high HR group. Responses to large acoustic contrasts (bursts of white noise), however, evoked strong early P3a phase in all children and did not differ by high/low HR. Our findings suggest that elevated physiological arousal may be associated with high variability in auditory ERP responses in young children, along with increased responsiveness to small acoustic changes.

Temporal dynamics of arousal and attention in 12-month-old infants.

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.

Tonic and phasic co-variation of peripheral arousal indices in infants.

Tonic and phasic differences in peripheral autonomic nervous system (ANS) indicators strongly predict differences in attention and emotion regulation in developmental populations. However, virtually all previous research has been based on individual ANS measures, which poses a variety of conceptual and methodlogical challenges to comparing results across studies. Here we recorded heart rate, electrodermal activity (EDA), pupil size, head movement velocity and peripheral accelerometry concurrently while a cohort of 37 typical 12-month-old infants completed a mixed assessment battery lasting approximately 20 min per participant. We analysed covariation of these autonomic indices in three ways: first, tonic (baseline) arousal; second, co-variation in spontaneous (phasic) changes during testing; third, phasic co-variation relative to an external stimulus event. We found that heart rate, head velocity and peripheral accelerometry showed strong positive co-variation across all three analyses. EDA showed no co-variation in tonic activity levels but did show phasic positive co-variation with other measures, that appeared limited to sections of high but not low general arousal. Tonic pupil size showed significant positive covariation, but phasic pupil changes were inconsistent. We conclude that: (i) there is high covariation between autonomic indices in infants, but that EDA may only be sensitive at extreme arousal levels, (ii) that tonic pupil size covaries with other indices, but does not show predicted patterns of phasic change and (iii) that motor activity appears to be a good proxy measure of ANS activity. The strongest patterns of covariation were observed using epoch durations of 40s per epoch, although significant covariation between indices was also observed using shorter epochs (1 and 5s).

Parsing eye-tracking data of variable quality to provide accurate fixation duration estimates in infants and adults.

Researchers studying infants' spontaneous allocation of attention have traditionally relied on hand-coding infants' direction of gaze from videos; these techniques have low temporal and spatial resolution and are labor intensive. Eye-tracking technology potentially allows for much more precise measurement of how attention is allocated at the subsecond scale, but a number of technical and methodological issues have given rise to caution about the quality and reliability of high temporal resolution data obtained from infants. We present analyses suggesting that when standard dispersal-based fixation detection algorithms are used to parse eye-tracking data obtained from infants, the results appear to be heavily influenced by interindividual variations in data quality. We discuss the causes of these artifacts, including fragmentary fixations arising from flickery or unreliable contact with the eyetracker and variable degrees of imprecision in reported position of gaze. We also present new algorithms designed to cope with these problems by including a number of new post hoc verification checks to identify and eliminate fixations that may be artifactual. We assess the results of our algorithms by testing their reliability using a variety of methods and on several data sets. We contend that, with appropriate data analysis methods, fixation duration can be a reliable and stable measure in infants. We conclude by discussing ways in which studying fixation durations during unconstrained orienting may offer insights into the relationship between attention and learning in naturalistic settings.