UEL Baby Dev Lab

Attention and social communication skills of very preterm infants after training attention control: Bayesian analyses of a feasibility study

Perra, O., Alderdice, F., Sweet, D., McNulty, A., Johnston, M., Bilello, D., ... & Wass, S. 2022. Plos ine

Very preterm (VP) infants (born 28 to <32 weeks of gestation) are at risk of cognitive delays and lower educational attainments. These risks are linked to anomalies in attention and information processing that emerge in the first years of life. Early interventions targeting attention functioning may equip VP infants with key building blocks for later attainments.Methods
We tested the feasibility of a randomised trial where VP infants took part in a computerised cognitive procedure to train attention control. Ten healthy VP infants aged approximately 12 months (corrected age) and randomly allocated with 1:1 ratio to the training (interactive computerised presentations) or an active control procedure completed the study. Before and after the training programme, participating infants completed a battery of screen-based attention tests, naturalistic attention and communication tasks, and temperament assessments. In a previous study we analysed the data concerning feasibility (e.g. recruitment and retention). In the paper presented here we considered the infants’ performance and used Bayesian regression in order to provide credible treatment estimates considering the data collected. Results Estimates indicate moderate treatment effects in visual memory: compared to controls, trained infants displayed improvements equivalent to 0.59 SD units. Trained infants also
improved in their abilities to attend to less salient stimuli presentations by 0.82 SD units, compared to controls. However, results did not indicate relevant gains in attention habituation or disengagement. We also reported moderate improvements in focused attention during naturalistic tasks, and in directing other people’s attention to shared objects.

Measures of attention in Rett syndrome: Internal consistency reliability.

Rose, S. A., Wass, S. V., Jankowski, J. J., & Djukic, A. 2021. Neuropsychology

Rett syndrome (RTT), an x-linked neurodevelopmental disorder caused by spontaneous mutations in the MECP2 gene, is characterized by profound impairments in expressive language and purposeful hand use. We have pioneered the use of gaze-based tasks to by-pass these limitations and developed measures suitable for clinical trials with RTT. Here we estimated internal consistency reliability for three aspects of attention that are key to cognitive growth and that we previously identified as impaired in RTT.
Using a sample of 66 children with RTT (2-19 years), we assessed Sustained Attention (butterfly task: Butterfly traverses the screen only when fixated and distractors are ignored); Disengaging/Shifting Attention ("gap/overlap" task: Shifts of gaze from central to peripheral targets are compared in conditions where the central stimulus remains or disappears at the onset of the peripheral target); Selective Attention (search task: the target is embedded in arrays differing in size and distractor type).
Reliability was acceptable to excellent on almost all key measures from tasks assessing Sustained Attention and Disengaging/Shifting Attention, with split-half coefficients and Cronbach alphas ranging from .70 to .93. Reliability increased as more trials were aggregated, with acceptable levels often reached with as few as six to nine trials. Measures from Selective Attention showed only limited reliability.
Finding that critical aspects of attention can be reliably assessed in RTT with gaze-based tasks constitutes a major advance in the development of cognitive measures appropriate for clinical and translational work. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Endogenous oscillatory rhythms and interactive contingencies jointly influence infant attention during early infant-caregiver interaction

Phillips, E. A., Goupil, L., Whitehorn, M., Bruce-Gardyne, E., Csolsim, F. A., Kaur, N., ... & Wass, S. V. 2023. BioRxiv

Almost all early cognitive development takes place in social contexts. At the moment, however, we know little about the neural and cognitive mechanisms that drive infant attention during social interactions. Recording EEG during naturalistic caregiver-infant interactions (N=66), we compare two different accounts. Attentional scaffolding perspectives emphasise the role of the caregiver in structuring the child’s behaviour, whilst active learning models focus on motivational factors, endogenous to the infant, that guide their attention. Our results show that, already by 12-months, intrinsic cognitive processes control infants’ attention: fluctuations in endogenous oscillatory neural activity associated with changes in infant attentiveness, and predicted the length of infant attention episodes towards objects. In comparison, infant attention was not forwards-predicted by caregiver gaze, or modulations in the spectral and temporal properties of their caregiver’s speech. Instead, caregivers rapidly modulated their behaviours in response to changes in infant attention and cognitive engagement, and greater reactive changes associated with longer infant attention. Our findings suggest that shared attention develops through interactive but asymmetric, infant-led processes that operate across the caregiver-child dyad.

A psychophysiological investigation of the interplay between orienting and executive control during stimulus conflict: A heart rate variability study.

Sørensen, L., Wass, S., Osnes, B., Schanche, E., Adolfsdottir, S., Svendsen, J. L., ... & Sonuga-Barke, E. 2019. Physiology & Behaviour

Background: It has been hypothesized that resting state cardiac vagal activity (CVA) - an indicator of parasympathetic nervous system activity - is a specific psychophysiological marker of executive control function.
Here, we propose an alternative hypothesis - that CVA is associated with early stage attention orientation,
promoting the flexible uptake of new information, on which the later operation of such executive control
functions depends. We therefore predicted that CVA would predict the interaction between orienting and executive control. This was tested using the revised version of the Attention Network Test (ANT-R) that was
developed to distinguish between orienting and executive attention during a stimulus conflict task.
Methods: Healthy adults (N = 48) performed the ANT-R and their resting CVA was measured over a 5 min period
using ECG recordings.
Results: Multiple regression analyses indicated that, when other factors were controlled for, CVA was more
strongly associated with the interaction between the orienting and executive control terms than with either
factor individually.
Conclusion: Higher levels of CVA are specifically implicated in the modulation of executive control by intrinsic
orientation operating at early stages of conflict detection. These initial findings of higher CVA on orienting
attention in conflict detection need to be replicated in larger samples.

Interpersonal neural synchrony and responsivity during early learning interactions.

Wass, S. V., Whitehorn, M., Haresign, I. M., Phillips, E., & Leong, V. 2020. Trends in Cognitive Science

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.

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., ... & 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., ... & 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.

Changes in behavior and salivary cortisol after targeted cognitive training in typical 12-month-old infants

Wass, S. V., Cook, C., & Clackson, K. 2017. Developmental Psychology

Previous research has suggested that early development may be an optimal period to implement cognitive training interventions, particularly those relating to attention control, a basic ability that is essential for the development of other cognitive skills. In the present study, we administered gaze-contingent training (95 minutes across 2 weeks) targeted at voluntary attention control to a cohort of typical 12-month-old children (N = 24) and sham training to a control group (N = 24). We assessed training effects on (a) tasks involving non-trained aspects of attention control: visual sustained attention, habituation speed, visual recognition memory, sequence learning and reversal learning; (b) general attentiveness (on-task behaviours during testing) and (c) salivary cortisol levels. Assessments were administered immediately following the cessation of training and at a 6-week follow-up. On the immediate post-test infants showed significantly more sustained visual attention, faster habituation and improved sequence learning. Significant effects were also found for increased general attentiveness and decreased salivary cortisol. Some of these effects were still evident at the 6-week follow-up (significantly improved sequence learning and marginally improved […] sustained attention). These findings extend the emerging literature showing that attention training is possible in infancy.

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.

Attention training for infants at familial risk of ADHD (INTERSTAARS): study protocol for a randomised controlled trial

Goodwin, A., Salomone, S., Bolton, P., Charman, T., Jones, E. J., Pickles, A., ... & Johnson, M. H. 2016. Trials

Background: Attention deficit hyperactivity disorder (ADHD) is a prevalent neurodevelopmental disorder that can
negatively impact on an individual’s quality of life. It is pathophysiologically complex and heterogeneous with
different neuropsychological processes being impaired in different individuals. Executive function deficits, including
those affecting attention, working memory and inhibitory control, are common. Cognitive training has been promoted
as a treatment option, based on the notion that by strengthening the neurocognitive networks underlying these
executive processes, ADHD symptoms will also be reduced. However, if implemented in childhood or later, when the
full disorder has become well-established, cognitive training has only limited value. INTERSTAARS is a trial designed to
test a novel approach to intervention, in which cognitive training is implemented early in development, before the
emergence of the disorder. The aim of INTERSTAARS is to train early executive skills, thereby increasing resilience and
reducing later ADHD symptoms and associated impairment.
Methods/design: Fifty 10–14-month-old infants at familial risk of ADHD will participate in INTERSTAARS. Infants
will be randomised to an intervention or a control group. The intervention aims to train early attention skills
by using novel eye-tracking technology and gaze-contingent training paradigms. Infants view animated games
on a screen and different events take place contingent on where on the screen the infant is looking. Infants
allocated to the intervention will receive nine weekly home-based attention training sessions. Control group
infants will also receive nine weekly home visits, but instead of viewing the training games during these visits
they will view non-gaze-contingent age-appropriate videos. At baseline and post treatment, infant attention
control will be assessed using a range of eye-tracking, observational, parent-report and neurophysiological
measures. The primary outcome will be a composite of eye-tracking tasks used to assess infant attention skills.
Follow-up data will be collected on emerging ADHD symptoms when the infants are 2 and 3 years old.
Discussion: This is the first randomised controlled trial to assess the potential efficacy of cognitive training as
a prevention measure for infants at familial risk of ADHD. If successful, INTERSTAARS could offer a promising
new approach for developing early interventions for ADHD.

First evidence of the feasibility of gaze-contingent attention training for school children with autism.

Powell, G., Wass, S. V., Erichsen, J. T., & Leekam, S. R. 2016. Autism

A number of authors have suggested that attention control may be a suitable target for cognitive training in children with autism spectrum disorder. This study provided the first evidence of the feasibility of such training using a battery of tasks intended to target visual attentional control in children with autism spectrum disorder within school-based settings. Twenty-seven children were recruited and randomly assigned to either training or an active control group. Of these, 19 completed the initial assessment, and 17 (9 trained and 8 control) completed all subsequent training sessions. Training of 120 min was administered per participant, spread over six sessions (on average). Compliance with the training tasks was generally high, and evidence of within-task training improvements was found. A number of untrained tasks to assess transfer of training effects were administered pre- and post-training. Changes in the trained group were assessed relative to an active control group. Following training, significant and selective changes in visual sustained attention were observed. Trend training effects were also noted on disengaging visual attention, but no convincing evidence of transfer was found to non-trained assessments of saccadic reaction time and anticipatory looking. Directions for future development and refinement of these new training techniques are discussed.

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.

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

Wass, S., Daubney, K., Golan, J., Logan, F., & Kushnerenko, E. 2019. Developmental cognitive neuroscience

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.

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.

Bidirectional Mechanisms rather than Alternatives: The Role of Sustained Attention in Interactive Contexts Can Only Be Understood through Joint Attention

Phillips, E., Wass, S. 2021. Human Development

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.

Allostasis and metastasis: the yin and yang of childhood self-regulation

Wass, S. 2021. PsyArXiv

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.

The origins of effortful control: How early development within arousal/regulatory systems influences attentional and affective control

Wass, S. 2021. Academic Press

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.

Proactive or reactive? Neural oscillatory insight into the leader-follower dynamics of early infant-caregiver interaction

Phillips, E., Goupil, L., Marriott-Haresign, I., Bruce-Gardyne, E., Csolsim, F. A., Whitehorn, M., Leong, M., Wass., S. 2021. PsyArXiv

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).