14 challenges and their solutions for conducting social neuroscience and longitudinal EEG research with infants.

The use of electroencephalography (EEG) to study infant brain development is a growing trend. In addition to classical longitudinal designs that study the development of neural, cognitive and behavioural functions, new areas of EEG application are emerging, such as novel social neuroscience paradigms using dual infant-adult EEG recordings. However, most of the experimental designs, analysis methods, as well as EEG hardware were originally developed for single-person adult research. When applied to study infant development, adult-based solutions often pose unique problems that may go unrecognised. Here, we identify 14 challenges that infant EEG researchers may encounter when designing new experiments, collecting data, and conducting data analysis. Challenges related to the experimental design are: (1) small sample size and data attrition, and (2) varying arousal in younger infants. Challenges related to data acquisition are: (3) determining the optimal location for reference and ground electrodes, (4) control of impedance when testing with the high-density sponge electrode nets, (5) poor fit of standard EEG caps to the varying infant head shapes, and (6) ensuring a high degree of temporal synchronisation between amplifiers and recording devices during dual-EEG acquisition. Challenges related to the analysis of longitudinal and social neuroscience datasets are: (7) developmental changes in head anatomy, (8) prevalence and diversity of infant myogenic artefacts, (9) a lack of stereotypical topography of eye movements needed for the ICA-based data cleaning, (10) and relatively high inter-individual variability of EEG responses in younger cohorts. Additional challenges for the analysis of dual EEG data are: (11) developmental shifts in canonical EEG rhythms and difficulties in differentiating true inter-personal synchrony from spurious synchrony due to (12) common intrinsic properties of the signal and (13) shared external perturbation. Finally, (14) there is a lack of test-retest reliability studies of infant EEG. We describe each of these challenges and suggest possible solutions. While we focus specifically on the social neuroscience and longitudinal research, many of the issues we raise are relevant for all fields of infant EEG research.This research was funded by an ESRC Transforming Social Sciences collaboration grant (ES/N006461/1) to VL and SW, and by ESRC FRL Fellowship (ES/N017560/1) to SW

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

Emotional communication between parents and children is crucial during early life, yet little is known about its neural underpinnings. Here, we adopt a dual connectivity approach to assess how positive and negative emotions modulate the interpersonal neural network between infants and their mothers during naturalistic interaction. Fifteen mothers were asked to model positive and negative emotions toward pairs of objects during social interaction with their infants (mean age 10.3 months) whilst the neural activity of both mothers and infants was concurrently measured using dual electroencephalography (EEG). Intra-brain and inter-brain network connectivity in the 6-9 Hz range (i.e. infant Alpha band) during maternal expression of positive and negative emotions was computed using directed (partial directed coherence, PDC) and non-directed (phase-locking value, PLV) connectivity metrics. Graph theoretical measures were used to quantify differences in network topology as a function of emotional valence. We found that inter-brain network indices (Density, Strength and Divisibility) consistently revealed strong effects of emotional valence on the parent-child neural network. Parents and children showed stronger integration of their neural processes during maternal demonstrations of positive than negative emotions. Further, directed inter-brain metrics (PDC) indicated that mother to infant directional influences were stronger during the expression of positive than negative emotional states. These results suggest that the parent-infant inter-brain network is modulated by the emotional quality and tone of dyadic social interactions, and that inter-brain graph metrics may be successfully applied to examine these changes in parent-infant inter-brain network topology.UK Economic and Social Research Council (ESRC) Transforming Social Sciences Grant ES/N006461/1 (to V.L. and S.W.), a Nanyang Technological University start-up Grant M4081585.SS0 (to V.L.), a Ministry of Education (Singapore) Tier 1 grant M4012105.SS0 (V.L.) and an ESRC Future Research Leaders Fellowship ES/N017560/1 (to S.W.)

Toward a Neuroscientific Understanding of Play: A Dimensional Coding Framework for Analyzing Infant-Adult Play Patterns.

Play during early life is a ubiquitous activity, and an individual's propensity for play is positively related to cognitive development and emotional well-being. Play behavior (which may be solitary or shared with a social partner) is diverse and multi-faceted. A challenge for current research is to converge on a common definition and measurement system for play - whether examined at a behavioral, cognitive or neurological level. Combining these different approaches in a multimodal analysis could yield significant advances in understanding the neurocognitive mechanisms of play, and provide the basis for developing biologically grounded play models. However, there is currently no integrated framework for conducting a multimodal analysis of play that spans brain, cognition and behavior. The proposed coding framework uses grounded and observable behaviors along three dimensions (sensorimotor, cognitive and socio-emotional), to compute inferences about playful behavior in a social context, and related social interactional states. Here, we illustrate the sensitivity and utility of the proposed coding framework using two contrasting dyadic corpora (N = 5) of mother-infant object-oriented interactions during experimental conditions that were either non-conducive (Condition 1) or conducive (Condition 2) to the emergence of playful behavior. We find that the framework accurately identifies the modal form of social interaction as being either non-playful (Condition 1) or playful (Condition 2), and further provides useful insights about differences in the quality of social interaction and temporal synchronicity within the dyad. It is intended that this fine-grained coding of play behavior will be easily assimilated with, and inform, future analysis of neural data that is also collected during adult-infant play. In conclusion, here, we present a novel framework for analyzing the continuous time-evolution of adult-infant play patterns, underpinned by biologically informed state coding along sensorimotor, cognitive and socio-emotional dimensions. We expect that the proposed framework will have wide utility amongst researchers wishing to employ an integrated, multimodal approach to the study of play, and lead toward a greater understanding of the neuroscientific basis of play. It may also yield insights into a new biologically grounded taxonomy of play interactions

Toward the Understanding of Topographical and Spectral Signatures of Infant Movement Artifacts in Naturalistic EEG

Electroencephalography (EEG) is perhaps the most widely used brain-imaging technique for pediatric populations. However, EEG signals are prone to distortion by motion. Compared to adults, infants’ motion is both more frequent and less stereotypical yet motion effects on the infant EEG signal are largely undocumented. Here, we present a systematic assessment of naturalistic motion effects on the infant EEG signal. EEG recordings were performed with 14 infants (12 analyzed) who passively watched movies whilst spontaneously producing periods of bodily movement and rest. Each infant produced an average of 38.3 s (SD = 14.7 s) of rest and 18.8 s (SD = 17.9 s) of single motion segments for the final analysis. Five types of infant motions were analyzed: Jaw movements, and Limb movements of the Hand, Arm, Foot, and Leg. Significant movement-related distortions of the EEG signal were detected using cluster-based permutation analysis. This analysis revealed that, relative to resting state, infants’ Jaw and Arm movements produced significant increases in beta (∼15 Hz) power, particularly over peripheral sites. Jaw movements produced more anteriorly located effects than Arm movements, which were most pronounced over posterior parietal and occipital sites. The cluster analysis also revealed trends toward decreased power in the theta and alpha bands observed over central topographies for all motion types. However, given the very limited quantity of infant data in this study, caution is recommended in interpreting these findings before subsequent replications are conducted. Nonetheless, this work is an important first step to inform future development of methods for addressing EEG motion-related artifacts. This work also supports wider use of naturalistic paradigms in social and developmental neuroscience

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

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

Speaker gaze increases information coupling between infant and adult brains

When infants and adults communicate, they exchange social signals of availability and communicative intention such as eye gaze. Previous research indicates that when communication is successful, close temporal dependencies arise between adult speakers’ and listeners’ neural activity. However, it is not known whether similar neural contingencies exist within adult-infant dyads. Here, we used dual-electroencephalography to assess whether direct gaze increases neural coupling between adults and infants during screen-based and live interactions. In Experiment 1 (N=17), infants viewed videos of an adult who was singing nursery rhymes with (a) Direct gaze (looking forward); (b) Indirect gaze (head and eyes averted by 20°); or (c) 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 conversely also influenced the adult more during Direct than Indirect gaze. Furthermore, infants vocalised more frequently during live Direct gaze, and individual infants who vocalized longer also elicited stronger synchronisation from the adult. This is the first demonstration that direct gaze strengthens bi-directional 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

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

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

Infant-parent emotional synchrony during social and non-social play

There is growing evidence that early experience of play is related to various developmental outcomes, the interchange of positive affect is considered a defining feature of infant-parent play, and may potentially be critical for facilitating early positive development. Despite this, we could find no existing studies comparing the expression of positive affect in different play contexts. The present study explored (1) differences in positive affect expression between social (i.e. joint) and non-social (i.e. separated) play, (2) differences between positive and negative emotion mirroring seen during parent-infant play, and (3) the temporal dynamics of emotional mirroring (parent to infant vs. infant to parent). 20 mother-infant dyads (aged 10.4 month) participated in social and non-social play, whilst their emotional expressions were monitored on video. Our results showed that both mothers and infants showed more positive affect and more affect synchrony during social play than non-social play. Regarding the temporal dynamics of emotional responding, mothers tended to follow, rather than lead, their infants’ positive emotional expressions. Further, mothers responded faster to their infants’ positive emotions during social play as compared to non-social play. By contrast, there were no significant differences on any of these measures for negative emotions. These results indicate that different mechanisms may underpin the exchange of positive and negative affect during parent-infant interactions, and different play contexts result in different levels of positive affect, suggesting social context of play may be a crucial factor in determining play’s developmental benefits

Do Helpful Mothers Help? Effects of Maternal Scaffolding and Infant Engagement on Cognitive Performance.

Infants are highly social and much early learning takes place in a social context during interactions with caregivers. Previous research shows that social scaffolding - responsive parenting and joint attention - can confer benefits for infants' long-term development and learning. However, little previous research has examined whether dynamic (moment-to-moment) adaptations in adults' social scaffolding are able to produce immediate effects on infants' performance. Here we ask whether infants' success on an object search task is more strongly influenced by maternal behavior, including dynamic changes in response behavior, or by fluctuations in infants' own engagement levels. Thirty-five mother-infant dyads (infants aged 10.8 months, on average) participated in an object search task that was delivered in a naturalistic manner by the child's mother. Measures of maternal responsiveness (teaching duration; sensitivity) and infant engagement (engagement score; visual attention) were assessed. Mothers varied their task delivery trial by trial, but neither measure of maternal responsiveness significantly predicted infants' success in performing the search task. Rather, infants' own level of engagement was the sole significant predictor of accuracy. These results indicate that while parental scaffolding is offered spontaneously (and is undoubtedly crucial for development), in this context children's endogenous engagement proved to be a more powerful determinant of task success. Future work should explore this interplay between parental and child-internal factors in other learning and social contexts

Perceptual and conceptual processing of visual objects across the adult lifespan

Abstract: Making sense of the external world is vital for multiple domains of cognition, and so it is crucial that object recognition is maintained across the lifespan. We investigated age differences in perceptual and conceptual processing of visual objects in a population-derived sample of 85 healthy adults (24–87 years old) by relating measures of object processing to cognition across the lifespan. Magnetoencephalography (MEG) was recorded during a picture naming task to provide a direct measure of neural activity, that is not confounded by age-related vascular changes. Multiple linear regression was used to estimate neural responsivity for each individual, namely the capacity to represent visual or semantic information relating to the pictures. We find that the capacity to represent semantic information is linked to higher naming accuracy, a measure of task-specific performance. In mature adults, the capacity to represent semantic information also correlated with higher levels of fluid intelligence, reflecting domain-general performance. In contrast, the latency of visual processing did not relate to measures of cognition. These results indicate that neural responsivity measures relate to naming accuracy and fluid intelligence. We propose that maintaining neural responsivity in older age confers benefits in task-related and domain-general cognitive processes, supporting the brain maintenance view of healthy cognitive ageing