Bursting with Potential: How Sensorimotor Beta Bursts Develop from Infancy to Adulthood.

Beta activity is thought to play a critical role in sensorimotor processes. However, little is known about how activity in this frequency band develops. Here, we investigated the developmental trajectory of sensorimotor beta activity from infancy to adulthood. We recorded EEG from 9-month-old, 12-month-old, and adult humans (male and female) while they observed and executed grasping movements. We analyzed "beta burst" activity using a novel method that combines time-frequency decomposition and principal component analysis. We then examined the changes in burst rate and waveform motifs along the selected principal components. Our results reveal systematic changes in beta activity during action execution across development. We found a decrease in beta burst rate during movement execution in all age groups, with the greatest decrease observed in adults. Additionally, we identified three principal components that defined waveform motifs that systematically changed throughout the trial. We found that bursts with waveform shapes closer to the median waveform were not rate-modulated, whereas those with waveform shapes further from the median were differentially rate-modulated. Interestingly, the decrease in the rate of certain burst motifs occurred earlier during movement and was more lateralized in adults than in infants, suggesting that the rate modulation of specific types of beta bursts becomes increasingly refined with age.SIGNIFICANCE STATEMENT We demonstrate that, like in adults, sensorimotor beta activity in infants during reaching and grasping movements occurs in bursts, not oscillations like thought traditionally. Furthermore, different beta waveform shapes were differentially modulated with age, including more lateralization in adults. Aberrant beta activity characterizes various developmental disorders and motor difficulties linked to early brain injury, so looking at burst waveform shape could provide more sensitivity for early identification and treatment of affected individuals before any behavioral symptoms emerge. More generally, comparison of beta burst activity in typical versus atypical motor development will also be instrumental in teasing apart the mechanistic functional roles of different types of beta bursts.

Visual Preference for Socially Relevant Spatial Relations in Humans and Monkeys.

As a powerful social signal, a body, face, or gaze facing toward oneself holds an individual's attention. We asked whether, going beyond an egocentric stance, facingness between others has a similar effect and why. In a preferential-looking time paradigm, human adults showed spontaneous preference to look at two bodies facing toward (vs. away from) each other (Experiment 1a, N = 24). Moreover, facing dyads were rated higher on social semantic dimensions, showing that facingness adds social value to stimuli (Experiment 1b, N = 138). The same visual preference was found in juvenile macaque monkeys (Experiment 2, N = 21). Finally, on the human development timescale, this preference emerged by 5 years, although young infants by 7 months of age already discriminate visual scenes on the basis of body positioning (Experiment 3, N = 120). We discuss how the preference for facing dyads-shared by human adults, young children, and macaques-can signal a new milestone in social cognition development, supporting processing and learning from third-party social interactions.

Longitudinal effects of early psychosocial deprivation on macaque executive function: Evidence from computational modelling.

Executive function (EF) describes a group of cognitive processes underlying the organization and control of goal-directed behaviour. Environmental experience appears to play a crucial role in EF development, with early psychosocial deprivation often linked to EF impairment. However, many questions remain concerning the developmental trajectories of EF after exposure to deprivation, especially concerning specific mechanisms. Accordingly, using an 'A-not-B' paradigm and a macaque model of early psychosocial deprivation, we investigated how early deprivation influences EF development longitudinally from adolescence into early adulthood. The contribution of working memory and inhibitory control mechanisms were examined specifically via the fitting of a computational model of decision making to the choice behaviour of each individual. As predicted, peer-reared animals (i.e. those exposed to early psychosocial deprivation) performed worse than mother-reared animals across time, with the fitted model parameters yielding novel insights into the functional decomposition of group-level EF differences underlying task performance. Results indicated differential trajectories of inhibitory control and working memory development in the two groups. Such findings not only extend our knowledge of how early deprivation influences EF longitudinally, but also provide support for the utility of computational modelling to elucidate specific mechanisms linking early psychosocial deprivation to long-term poor outcomes.

Effects of Infant Cleft Lip on Adult Gaze and Perceptions of "Cuteness".

OBJECTIVE: Early mother-infant interactions are impaired in the context of infant cleft lip and are associated with adverse child psychological outcomes, but the nature of these interaction difficulties is not yet fully understood. The aim of this study was to explore adult gaze behavior and cuteness perception, which are particularly important during early social exchanges, in response to infants with cleft lip, in order to investigate potential foundations for the interaction difficulties seen in this population. METHODS: Using an eye tracker, eye movements were recorded as adult participants viewed images of infant faces with and without cleft lip. Participants also rated each infant on a scale of cuteness. RESULTS: Participants fixated significantly longer on the mouths of infants with cleft lip, which occurred at the expense of fixation on eyes. Severity of cleft lip was associated with the strength of fixation bias, with participants looking even longer at the mouths of infants with the most severe clefts. Infants with cleft lip were rated as significantly less cute than unaffected infants. Men rated infants as less cute than women overall but gave particularly low ratings to infants with cleft lip. CONCLUSIONS: Results demonstrate that the limited disturbance in infant facial configuration of cleft lip can significantly alter adult gaze patterns and cuteness perception. Our findings could have important implications for early interactions and may help in the development of interventions to foster healthy development in infants with cleft lip.

Beyond aerodigestion: Exaptation of feeding-related mouth movements for social communication in human and nonhuman primates.

Three arguments are advanced from human and nonhuman primate infancy research for the exaptation of ingestive mouth movements (tongue protrusion and lip smacking) for the purposes of social communication: their relation to affiliative behaviours, their sensitivity to social context, and their role in social development. Although these behaviours may have an aerodigestive function, such an account of their occurrence is only partial.

Behavioural inhibition and early neural processing of happy and angry faces interact to predict anxiety: a longitudinal ERP study.

Limited prospective research has examined whether attention biases to emotion moderate associations between Behavioural Inhibition (BI) and anxiety in preschool-aged children. Furthermore, there has been an over-reliance on behavioral measures in previous studies. Accordingly, we assessed anxiety in a sample of preschool-aged children (3-4 years) at baseline, and again approximately 6 and 11 months later, after they started school. At baseline, children completed an assessment of BI and an EEG task where they were presented with angry, happy, and neutral faces. EEG analyses focused on ERPs (P1, P2, N2) associated with specific stages of attention allocation. Interactions between BI and emotion bias (ERP amplitude for emotional versus neutral faces) were found for N2 and P1. For N2, BI was significantly associated with higher overall anxiety when an angry bias was present. Interestingly for P1, BI was associated with higher overall anxiety when a happy bias was absent. Finally, interactions were found between linear time and happy and angry bias for P1, with a greater linear decrease in anxiety over time when biases were high. These results suggest that attention to emotional stimuli moderates the BI-anxiety relationship across early development.

In the mind of the beholder: The effects of familiarisation on the perception of atypical infant facial configurations.

Infant facial attractiveness is an important facilitator for adult-infant caregiving behaviour. Disruption to typical infant facial configurations can, however, attenuate their perceived attractiveness, as rated by adult observers. Previous research has either focused on how ratings are affected by observer characteristics (e.g., male/female), or alterations to infant faces, either experimentally, or naturalistically induced, such as the presence of a cleft lip. Little research has however been conducted on the effects of observer experience on adult ratings of infant facial attractiveness. Such effects could inform clinical work and policies aimed at promoting positive perception of facial malformations. The present study thus explored the effects of familiarisation on how typical and atypical infant facial configurations are evaluated by adults. We recruited two groups of female participants and compared their subjective attractiveness ratings of infant faces (24 typical and 24 cleft-affected), at baseline, and at one-week post-test. Between the two assessments, one group (n = 41) underwent a week-long training phase, where they were familiarised with cleft lip/palate-related visual and informational stimuli, while the control group (n = 44) received no training. Significantly higher ratings were provided for faces of typically developing versus cleft-affected infants by both groups of participants at baseline. At post-test, this pattern of ratings was repeated in participants belonging to the control group, while familiarised participants showed an increase, compared to baseline, in their ratings of cleft-affected faces and no difference between their evaluation of the latter and that of typically developing faces. These findings extend our understanding of the observer's experience in the evaluation of infant faces, beyond the effects of the structural characteristics of the observed faces. Results also highlight familiarity as a potentially protective influence against the negative consequences of alterations to typical facial configurations, suggesting avenues for intervention in supporting adult caregivers in the context of neonatal facial malformations.

Dialogic Book-Sharing as a Privileged Intersubjective Space.

Parental reading to young children is well-established as being positively associated with child cognitive development, particularly their language development. Research indicates that a particular, "intersubjective," form of using books with children, "Dialogic Book-sharing" (DBS), is especially beneficial to infants and pre-school aged children, particularly when using picture books. The work on DBS to date has paid little attention to the theoretical and empirical underpinnings of the approach. Here, we address the question of what processes taking place during DBS confer benefits to child development, and why these processes are beneficial. In a novel integration of evidence, ranging from non-human primate communication through iconic gestures and pointing, archaeological data on Pre-hominid and early human art, to experimental and naturalistic studies of infant attention, cognitive processing, and language, we argue that DBS entails core characteristics that make it a privileged intersubjective space for the promotion of child cognitive and language development. This analysis, together with the findings of DBS intervention studies, provides a powerful intellectual basis for the wide-scale promotion of DBS, especially in disadvantaged populations.

Detection and analysis of cortical beta bursts in developmental EEG data.

Developmental EEG research often involves analyzing signals within various frequency bands, based on the assumption that these signals represent oscillatory neural activity. However, growing evidence suggests that certain frequency bands are dominated by transient burst events in single trials rather than sustained oscillations. This is especially true for the beta band, with adult 'beta burst' timing a better predictor of motor behavior than slow changes in average beta amplitude. No developmental research thus far has looked at beta bursts, with techniques used to investigate frequency-specific activity structure rarely even applied to such data. Therefore, we aimed to: i) provide a tutorial for developmental EEG researchers on the application of methods for evaluating the rhythmic versus transient nature of frequency-specific activity; and ii) use these techniques to investigate the existence of sensorimotor beta bursts in infants. We found that beta activity in 12-month-olds did occur in bursts, however differences were also revealed in terms of duration, amplitude, and rate during grasping compared to adults. Application of the techniques illustrated here will be critical for clarifying the functional roles of frequency-specific activity across early development, including the role of beta activity in motor processing and its contribution to differing developmental motor trajectories.

Facial Expression Time Processing in Typical Development and in Patients with Congenital Facial Palsy.

Temporal dynamics of behavior, particularly facial expressions, are fundamental for communication between individuals from very early in development. Facial expression processing has been widely demonstrated to involve embodied simulative processes mediated by the motor system. Such processes may be impaired in patients with congenital facial palsy, including those affected by Moebius syndrome (MBS). The aims of this study were to investigate (a) the role of motor mechanisms in the processing of dynamic facial expression timing by testing patients affected by congenital facial palsy and (b) age-dependent effects on such processing. Accordingly, we recruited 38 typically developing individuals and 15 individuals with MBS, ranging in age from childhood to adulthood. We used a time comparison task where participants were asked to identify which one of two dynamic facial expressions was faster. Results showed that MBS individuals performed worse than controls in correctly estimating the duration of facial expressions. Interestingly, we did not find any performance differences in relation to age. These findings provide further evidence for the involvement of the motor system in processing facial expression duration and suggest that a sensorimotor matching mechanism may contribute to such timing perception from childhood.

Early social adversity modulates the relation between attention biases and socioemotional behaviour in juvenile macaques.

Affect-biased attention may play a fundamental role in early socioemotional development, but factors influencing its emergence and associations with typical versus pathological outcomes remain unclear. Here, we adopted a nonhuman primate model of early social adversity (ESA) to: (1) establish whether juvenile, pre-adolescent macaques demonstrate attention biases to both threatening and reward-related dynamic facial gestures; (2) examine the effects of early social experience on such biases; and (3) investigate how this relation may be linked to socioemotional behaviour. Two groups of juvenile macaques (ESA exposed and non-ESA exposed) were presented with pairs of dynamic facial gestures comprising two conditions: neutral-threat and neutral-lipsmacking. Attention biases to threat and lipsmacking were calculated as the proportion of gaze to the affective versus neutral gesture. Measures of anxiety and social engagement were also acquired from videos of the subjects in their everyday social environment. Results revealed that while both groups demonstrated an attention bias towards threatening facial gestures, a greater bias linked to anxiety was demonstrated by the ESA group only. Only the non-ESA group demonstrated a significant attention bias towards lipsmacking, and the degree of this positive bias was related to duration and frequency of social engagement in this group. These findings offer important insights into the effects of early social experience on affect-biased attention and related socioemotional behaviour in nonhuman primates, and demonstrate the utility of this model for future investigations into the neural and learning mechanisms underlying this relationship across development.

Oxytocin promotes prosocial behavior and related neural responses in infant macaques at-risk for compromised social development.

Although positive effects of oxytocin (OT) on social functioning are well-demonstrated, little is known about the mechanisms through which OT may drive early social development, or its therapeutic efficacy in infancy. To address these critical issues, we investigated the effects of exogenous OT on neural (EEG) and behavioral responses during observation of live facial gestures in infant macaques with limited social exposure (i.e. nursery-reared). Three key findings were revealed. First, OT increased alpha suppression over posterior scalp regions during observation of facial gestures but not non-biological movement, suggesting that OT targets self-other matching and attentional cortical networks involved in social perception from very early infancy. Second, OT increased infant production of matching facial gestures and attention towards the most socially-relevant facial stimuli, both behaviors typically silenced by early social deprivation. Third, infants with higher cortisol levels appeared to benefit the most from OT, displaying greater improvements in prosocial behaviors after OT administration. Altogether, these findings suggest that OT promotes prosocial behaviors and associated neural responses likely impacted by early social adversity, and demonstrate the potential of OT administration to ameliorate social difficulties in the context of neurodevelopmental and early-emerging psychiatric disorders, at a developmental stage when brain plasticity is greatest.

Trajectories of anxiety when children start school: The role of behavioral inhibition and attention bias to angry and happy faces.

Extensive research has examined attention bias to threat in the context of anxiety in adults, but little is understood about this association in young children, and there is a dearth of longitudinal research examining whether attention bias to threat predicts anxiety over time in childhood. In the current study, a sample of 180 children participated in a longitudinal study, first as preschoolers and again as they transitioned to formal schooling. At baseline, children aged 3-4 years completed a free-viewing eye-tracking task with angry-neutral and happy-neutral face pairs and an assessment of behavioral inhibition (BI). At follow-up, parents provided daily reports of their child's state anxiety over a 2-week period as their child started school and completed a measure of their child's anxiety symptoms. Results indicated that, on average, preschool-aged children exhibit a bias for emotional faces that is stronger for angry than happy faces. There was little evidence that this bias was associated with anxiety symptoms. However, BI interacted with dwell bias for angry faces to predict trajectories of anxiety over the transition to school. An unexpected interaction between BI and dwell bias for happy faces was also found, with dwell for happy faces associated with lower anxiety for children higher in BI. The findings are consistent with recent developmental models of the BI-anxiety relationship and indicate that attention bias modification may not be suitable for young children, for whom attention bias to threat may be normative. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Building blocks of joint attention: Early sensitivity to having one's own gaze followed.

Detecting when one's own gaze has been followed is a critical component of joint attention, but little is known about its development. To address this issue, we used electroencephalography (EEG) to record infant neural responses at 6.5 and 9.5 months during observation of an adult either turning to look at the same object as the infant (congruent actor), or turning to look at a different object (incongruent actor). We also used a preferential looking paradigm to investigate whether infants would demonstrate a preference for the congruent versus incongruent actor. Greater suppression of alpha band activity in the congruent compared to incongruent condition was revealed at both ages in central and parietal regions. However, the effect of congruency on alpha suppression was stronger at 9.5 months, and only at this age did infants demonstrate a preference towards looking at the congruent actor. Together, these results suggest that although infants are sensitive to others' gaze following from early on, important neural and behavioural developments occur between 6.5 and 9.5 months.

Early maternal mirroring predicts infant motor system activation during facial expression observation.

Processing facial expressions is an essential component of social interaction, especially for preverbal infants. In human adults and monkeys, this process involves the motor system, with a neural matching mechanism believed to couple self- and other-generated facial gestures. Here, we used electroencephalography to demonstrate recruitment of the human motor system during observation and execution of facial expressions in nine-month-old infants, implicating this system in facial expression processing from a very young age. Notably, examination of early video-recorded mother-infant interactions supported the common, but as yet untested, hypothesis that maternal mirroring of infant facial gestures is central to the development of a neural matching mechanism for these gestures. Specifically, the extent to which mothers mirrored infant facial expressions at two months postpartum predicted infant motor system activity during observation of the same expressions at nine months. This suggests that maternal mirroring strengthens mappings between visual and motor representations of facial gestures, which increases infant neural sensitivity to particularly relevant cues in the early social environment.

Maternal gaze to the infant face: Effects of infant age and facial configuration during mother-infant engagement in the first nine weeks.

BACKGROUND: Adult gaze plays an important role in early infant development, and infants are highly sensitive to its presence and direction. Little is known, however, about how adults look at infants while interacting with them. Using eye-tracking technology, this study investigated maternal gaze during naturalistic interactions, and how it was influenced by infant age, focusing on the transition from the first to the second month when social expressiveness emerges, and by infant facial configuration, focusing on the effect of cleft lip. METHODS: Thirty infants (10 with a cleft lip), and their mothers, were seen at 1, 3, 5, 7, and 9 weeks. Mothers were asked to interact with their infants while wearing eye-tracking glasses. Fixation duration and count were calculated for general (infant face, body, and surrounding environment), and infant facial (eyes, mouth, other) areas. RESULTS: At all ages, mothers gazed almost exclusively towards their infant's face, but this was reduced in the presence of a cleft lip. Within the infant's face, the eyes attracted the greatest attention, for all mothers, at all ages. From the first to the second month, all mothers increased their visual attention towards their infant's mouth. Regardless of infant age, the presence of a cleft lip was associated with decreased maternal gaze to the infant's mouth. CONCLUSIONS: This study provides novel findings concerning maternal gaze to infant faces during naturalistic interactions. Maternal gaze changes with infant age, in line with established shifts in social development, and according to infant facial configuration. Decreased gaze to the mouth area associated with infant cleft lip might affect maternal responsiveness, and suggests new dimensions to target in supporting these mothers.

Mu desynchronization during observation and execution of facial expressions in 30-month-old children.

Simulation theories propose that observing another's facial expression activates sensorimotor representations involved in the execution of that expression, facilitating recognition processes. The mirror neuron system (MNS) is a potential mechanism underlying simulation of facial expressions, with like neural processes activated both during observation and performance. Research with monkeys and adult humans supports this proposal, but so far there have been no investigations of facial MNS activity early in human development. The current study used electroencephalography (EEG) to explore mu rhythm desynchronization, an index of MNS activity, in 30-month-old children as they observed videos of dynamic emotional and non-emotional facial expressions, as well as scrambled versions of the same videos. We found significant mu desynchronization in central regions during observation and execution of both emotional and non-emotional facial expressions, which was right-lateralized for emotional and bilateral for non-emotional expressions during observation. These findings support previous research suggesting movement simulation during observation of facial expressions, and are the first to provide evidence for sensorimotor activation during observation of facial expressions, consistent with a functioning facial MNS at an early stage of human development.