UEL Baby Dev Lab

Comparative strengths and challenges on face-to-face and computer-based attention tasks in autistic and neurotypical toddlers

Sacrey, L.-A., Zwaigenbaum, L., Elshamy, Y., Smith, I. M., Brian, J.A. & Wass, S.V. 2023. Autism Research

The objectives were to compare patterns of visual attention in toddlers diagnosed with autism spectrum disorder (ASD) as compared to their sex- and age-matched neurotypical (NT) peers. Participants included 23 toddlers with ASD and 19 NT toddlers (mean age: 25.52 versus 25.21 months, respectively) assessed using computerized tasks to measure sustained attention, disengaging attention, and cognitive control, as well as an in-person task to assess joint attention. Toddlers in the ASD group showed increased looking durations on the sustained attention task, as well as reduced frequencies of responding to and initiating joint attention compared to NT peers, but showed no differences on tasks of disengaging attention and cognitive control. The results suggest that toddlers with ASD have attentional strengths that may provide a foundation for building attention, communicative, and ultimately, academic skills.

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

Daubney , K., Suata, Z., Marriott Haresign, I., Thomas, M., Kushnerenko, E., & Wass, S. V. 2023. Developmental Cognitive Neuroscience

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.

The neural and physiological substrates of real-world attention change across development

Perapoch Amadó, M. Greenwood, E., Ives, J., Labendzki, P., Marriott-Haresign, I., Northrop T. J., Phillips, E. A. M., Viswanathan, N. K., Whitehorn, M., Jones, E. J. H., & Wass, S. V. 2023. eLife

The capacity to pay attention underpins all subsequent cognitive development. However, we understand little about how attention control is instantiated in the developing brain in real-world settings. We recorded naturalistic attention patterns, together with autonomic arousal and brain activity, in 5- and 10-month-old infants during free play. We examined whether changes in autonomic arousal and brain activity associate with changes in moment-by-moment attentional engagement, and whether they anticipate attention changes, or follow on from them. Early in infancy, slow-varying fluctuations in autonomic arousal forward-predicted attentional behaviours. Later in infancy, fluctuations in fronto-central theta power after but not before an attentional shift associated with changes in infants’ attentiveness, predicted the length of infants’ attention durations and modulated changes in arousal. Together, our results suggest that the modulation of real-world attention involves both arousal-based and cortical processes and what changes with developmental time is how these lower- and higher-order endogenous factors modulate real-world attention. As attentional systems mature, stronger associations emerge between attentional behaviour, cortical activity, and autonomic arousal.

Training attention control of very preterm infants: protocol for a feasibility study of the Attention Control Training (ACT).

Perra, O., Wass, S., McNulty, A., Sweet, D., Papageorgiou, K., Johnston, M., Patterson, A., Bilello, D., & Alderdice, F. 2020. Pilot and Feasibility Studies

Background: Children born preterm may display cognitive, learning, and behaviour difficulties as they grow up. In particular, very premature birth (gestation age between 28 and less than 32 weeks) may put infants at increased risk of intellectual deficits and attention deficit disorder. Evidence suggests that the basis of these problems may lie in difficulties in the development of executive functions. One of the earliest executive functions to emerge around 1 year of age is the ability to control attention. An eye-tracking-based cognitive training programme to support this emerging ability, the Attention Control Training (ACT), has been developed and tested with typically developing infants. The aim of this study is to investigate the feasibility of using the ACT with healthy very preterm (VP) infants when they are 12 months of age (corrected age). The ACT has the potential to address the need for supporting emerging cognitive abilities of VP infants with an early intervention, which may capitalise on infants’ neural plasticity. Methods/design: The feasibility study is designed to investigate whether it is possible to recruit and retain VP infants and their families in a randomised trial that compares attention and social attention of trained infants against those that are exposed to a control procedure. Feasibility issues include the referral/recruitment pathway, attendance, and engagement with testing and training sessions, completion of tasks, retention in the study, acceptability of outcome measures, quality of data collected (particularly, eye-tracking data). The results of the study will inform the development of a larger randomised trial. Discussion: Several lines of evidence emphasise the need to support emerging cognitive and learning abilities of preterm infants using early interventions. However, early interventions with preterm infants, and particularly very preterm ones, face difficulties in recruiting and retaining participants. These problems are also augmented by the health vulnerability of this population. This feasibility study will provide the basis for informing the implementation of an early cognitive intervention for very preterm infants.

Very preterm infants engage in an intervention to train their control of attention: results from the feasibility study of the Attention Control Training (ACT) randomised trial.

Perra, O., Wass, S., McNulty, A, Sweet, D., Papageorgiou, K. A., Johnston, M., Bilello, D., Patterson, A. and Alderdice, F 2021. Pilot and Feasibility Studies

Background: Very premature birth (gestational age between 28 and 31 + 6 weeks) is associated with increased risk of cognitive delay and attention deficit disorder, which have been linked to anomalies in the development of executive functions (EFs) and their precursors. In particular, very preterm (VP) infants display anomalies in controlling attention and gathering task-relevant information. Early interventions that support attention control may be pivotal in providing a secure base for VP children’s later attainments. The Attention Control Training (ACT) is a cognitive training intervention that targets infants’ abilities to select visual information according to varying task demands but had not been tested in VP infants. We conducted a feasibility study to test the processes we intend to use in a trial delivering the ACT to VP infants. Methods and design: We tested recruitment and retention of VP infants and their families in a randomised trial, as well as acceptability and completion of baseline and outcome measures. To evaluate these aims, we used descriptive quantitative statistics and qualitative methods to analyse feedback from infants’ caregivers. We also investigated the quality of eye-tracking data collected and indicators of infants’ engagement in the training, using descriptive statistics. Results: Twelve VP infants were recruited, and 10 (83%) completed the study. Participants’ parents had high education attainment. The rate of completion of baseline and outcome measures was optimal. VP infants demonstrated engagement in the training, completing on average 84 min of training over three visits, and displaying improved performance during this training. Eye-tracking data quality was moderate, but this did not interfere with infants’ engagement in the training.

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

Wass, S. V., Clackson, K., & De Barbaro, K. 2016. Developmental Psychobiology

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.

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

Noreika, V., Georgieva, S., Wass, S., & Leong, V. 2020. Infant Behaviour & Development

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.

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

I. Marriott Haresign, E.A.M Phillips, M. Whitehorn, F. Lamagna, M. Eliano, L. Goupil, E.J.H. Jones, S.V. Wass 2022. bioRxiv

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.

Applying gaze-contingent training within community settings to infants from diverse SES backgrounds

Ballieux, H., Wass, S., Tomalski, P., Kushnerenko, E., Karmiloff-Smith, A., Johnson, M., & Moore, D. 2016. Journal of Applied Developmental Psychology

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.

Anxious parents show higher physiological synchrony with their infants

Smith, C., Jones, E., Charman, T., Clackson, K., Mirza, F., & Wass, S. 2019. Psychological Medicine

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.

Parental frontal brain activity tracks infants’ attention during shared play

Wass, S., Marriott-Haresign, I., Whitehorn, M., Clackson, K., Georgieva, S., Noreika, V., & Leong, V. 2020. PsyArXiv

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.