Infant sustained attention differs by context and social content in the first 2 years of life.

Sustained attention (SA) is an endogenous form of attention that emerges in infancy and reflects cognitive engagement and processing. SA is critical for learning and has been measured using different methods during screen-based and interactive contexts involving social and nonsocial stimuli. How SA differs by measurement method, context, and stimuli across development in infancy is not fully understood. This 2-year longitudinal study examines attention using one measure of overall looking behavior and three measures of SA-mean look duration, percent time in heart rate-defined SA, and heart rate change during SA-in N = 53 infants from 1 to 24 months across four unique task conditions: social videos, nonsocial videos, social interactions (face-to-face play), and nonsocial interactions (toy engagement). Results suggest that developmental changes in attention differ by measurement method, task context (screen or interaction), and task stimulus (social or nonsocial). During social interactions, overall looking and look durations declined after age 3-4 months, whereas heart rate-defined attention measures remained stable. All SA measures were greater for videos than for live interaction conditions throughout the first 6 months, but SA to social and nonsocial stimuli within each task context were equivalent. In the second year of life, SA measured with look durations was greater for social videos compared to other conditions, heart rate-defined SA was greater for social videos compared to nonsocial interactions, and heart rate change during SA was similar across conditions. Together, these results suggest that different measures of attention to social and nonsocial stimuli may reflect unique developmental processes and are important to compare and consider together, particularly when using infant attention as a marker of typical or atypical development. RESEARCH HIGHLIGHTS: Attention measure, context, and social content uniquely differentiate developmental trajectories of attention in the first 2 years of life. Overall looking to caregivers during dyadic social interactions declines significantly from 4 to 6 months of age while sustained attention (SA) to caregivers remains stable. Heart rate-defined SA generally differentiates stimulus context where infants show greater SA while watching videos than while engaging with toys.

Multimodal study of the neural sources of error monitoring in adolescents and adults.

The ability to monitor performance during a goal-directed behavior differs among children and adults in ways that can be measured with several tasks and techniques. As well, recent work has shown that individual differences in error monitoring moderate temperamental risk for anxiety and that this moderation changes with age. We investigated age differences in neural responses linked to performance monitoring using a multimodal approach. The approach combined functional MRI and source localization of event-related potentials (ERPs) in 12-year-old, 15-year-old, and adult participants. Neural generators of two components related to performance and error monitoring, the N2 and ERN, lay within specific areas of fMRI clusters. Whereas correlates of the N2 component appeared similar across age groups, age-related differences manifested in the location of the generators of the ERN component. The dorsal anterior cingulate cortex (dACC) was the predominant source location for the 12-year-old group; this area manifested posteriorly for the 15-year-old and adult groups. A fMRI-based ROI analysis confirmed this pattern of activity. These results suggest that changes in the underlying neural mechanisms are related to developmental changes in performance monitoring.

Frontal asymmetry assessed in infancy using functional near-infrared spectroscopy is associated with emotional and behavioral problems in early childhood.

Frontal asymmetry (FA), the difference in brain activity between the left versus right frontal areas, is thought to reflect approach versus avoidance motivation. This study (2012-2021) used functional near-infrared spectroscopy to investigate if infant (Mage  = 7.63 months; N = 90; n = 48 male; n = 75 White) FA in the dorsolateral prefrontal cortex relates to psychopathology in later childhood (Mage  = 62.05 months). Greater right FA to happy faces was associated with increased internalizing (η2  = .09) and externalizing (η2  = .06) problems at age 5 years. Greater right FA to both happy and fearful faces was associated with an increased likelihood of a lifetime anxiety diagnosis (R2 > .13). FA may be an informative and early-emerging marker for psychopathology.

Neural correlates of inhibitory control and associations with cognitive outcomes in Bangladeshi children exposed to early adversities.

There is strong support for the view that children growing up in low-income homes typically evince poorer performance on tests of inhibitory control compared to those growing up in higher income homes. Unfortunately, the vast majority of the work documenting this association has been conducted in high-income countries. It is not yet known whether the mechanisms found to mediate this association would generalize to children in low- and middle-income countries, where the risks of exposure to extreme poverty and a wide range of both biological and psychosocial hazards may be greater. We examined relations among early adversity, neural correlates of inhibitory control, and cognitive outcomes in 154 5-year-old children living in Dhaka, Bangladesh, an area with a high prevalence of poverty. Participants completed a go/no-go task assessing inhibitory control and their behavioral and event-related potential responses were assessed. Cortical source analysis was performed. We collected measures of poverty, malnutrition, maternal mental health, psychosocial adversity, and cognitive skills. Supporting studies in high-income countries, children in this sample exhibited a longer N2 latency and higher P3 amplitude to the no-go versus go condition. Unexpectedly, children had a more pronounced N2 amplitude during go trials than no-go trials. The N2 latency was related to their behavioral accuracy on the go/no-go task. The P3 mean amplitude, behavioral accuracy, and reaction time during the task were all associated with intelligence-quotient (IQ) scores. Children who experienced higher levels of psychosocial adversity had lower accuracy on the task and lower IQ scores.

Evaluating Head Models for Cortical Source Localization of the Face-Sensitive N290 Component in Infants.

Accurate cortical source localization of event-related potentials (ERPs) requires using realistic head models constructed from the participant's structural magnetic resonance imaging (MRI). A challenge in developmental studies is the limited accessibility of participant-specific MRIs. The present study compared source localization of infants' N290 ERP activities estimated using participant-specific head models with a series of substitute head models. The N290 responses to faces relative to toys were measured in 36 infants aged at 4.5, 7.5, 9, and 12 months. The substitutes were individual-based head models constructed from age-matched MRIs with closely matched ("close") or different ("far") head measures with the participants, age-appropriate average template, and age-inappropriate average templates. The greater source responses to faces than toys at the middle fusiform gyrus (mFG) estimated using participant-specific head models were preserved in individual-based head models, but not average templates. The "close" head models yielded the best fit with the participant-specific head models in source activities at the mFG and across face-processing-related regions of interest (ROIs). The age-appropriate average template showed mixed results, not supporting the stimulus effect but showed topographical distributions across the ROIs like the participant-specific head models. The "close" head models are the most optimal substitute for participant-specific MRIs.

Structural templates for imaging EEG cortical sources in infants.

Electroencephalographic (EEG) source reconstruction is a powerful approach that allows anatomical localization of electrophysiological brain activity. Algorithms used to estimate cortical sources require an anatomical model of the head and the brain, generally reconstructed using magnetic resonance imaging (MRI). When such scans are unavailable, a population average can be used for adults, but no average surface template is available for cortical source imaging in infants. To address this issue, we introduce a new series of 13 anatomical models for subjects between zero and 24 months of age. These templates are built from MRI averages and boundary element method (BEM) segmentation of head tissues available as part of the Neurodevelopmental MRI Database. Surfaces separating the pia mater, the gray matter, and the white matter were estimated using the Infant FreeSurfer pipeline. The surface of the skin as well as the outer and inner skull surfaces were extracted using a cube marching algorithm followed by Laplacian smoothing and mesh decimation. We post-processed these meshes to correct topological errors and ensure watertight meshes. Source reconstruction with these templates is demonstrated and validated using 100 high-density EEG recordings from 7-month-old infants. Hopefully, these templates will support future studies on EEG-based neuroimaging and functional connectivity in healthy infants as well as in clinical pediatric populations.

The Influence of the Head Model Conductor on the Source Localization of Auditory Evoked Potentials.

The accuracy of EEG source analysis reconstruction improves when a realistic head volume conductor is modeled. In this study we investigated how the progressively more complex head representations influence the spatial localization of auditory-evoked potentials (AEPs). Fourteen young-adult participants with normal hearing performed the AEP task. Individualized head models were obtained from structural MRI and diffusion-weighted imaging scans collected in a separate session. AEPs were elicited by 1 k Hz and 4 k Hz tone bursts during a passive-listening tetanizing paradigm. We compared the amplitude of the N1 and P2 components before and after 4 min of tetanic-stimulation with 1 k Hz sounds. Current density reconstruction values of both components were investigated in the primary auditory cortex and adjacent areas. Furthermore, we compared the signal topography and magnitude obtained with 10 different head models on the EEG forward solution. Starting from the simplest model (scalp, skull, brain), we investigated the influence of modeling the CSF, distinguishing between GM and WM conductors, and including anisotropic WM values. We localized the activity of AEPs within the primary auditory cortex, but not in adjacent areas. The inclusion of the CSF compartment had the strongest influence on the source reconstruction, whereas white matter anisotropy led to a smaller improvement. We conclude that individualized realistic head models provide the best solution for the forward solution when modeling the CSF conductor.

Peak selection and latency jitter correction in developmental event-related potentials.

Event-related potentials (ERPs) provide great insight into neural responses, yet developmental ERP work is plagued with inconsistent approaches to identifying and quantifying component latency. In this analytical review, we describe popular conventions for the selection of time windows for ERP analysis and assert that a data-driven strategy should be applied to the identification of component latency within individual participants' data. This may overcome weaknesses of more general approaches to peak selection; however, it does not account for trial-by-trial variability within a participant. This issue, known as ERP latency jitter, may blur the average ERP, misleading the interpretation of neural mechanisms. Recently, the ReSync MATLAB toolbox has been made available for correction of latency jitter. Although not created specifically for pediatric ERP data, this approach can be adapted for developmental researchers. We have demonstrated the use of the ReSync toolbox with individual infant and child datasets to illustrate its utility. Details about our peak detection script and the ReSync toolbox are provided. The adoption of data processing procedures that allow for accurate, study-specific component selection and reduce trial-by-trial asynchrony strengthens developmental ERP research by decreasing noise included in ERP analyses and improving the representation of the neural response.

A single-session behavioral protocol for successful event-related potential recording in children with neurodevelopmental disorders.

Event-related potentials (ERPs) are an ideal tool for measuring neural responses in a wide range of participants, including children diagnosed with neurodevelopmental disorders (NDDs). However, due to perceived barriers regarding participant compliance, much of this work has excluded children with low IQ and/or reduced adaptive functioning, significant anxiety symptoms, and/or sensory processing difficulties, including heterogeneous samples of children with autism spectrum disorder (ASD) and children with fragile X syndrome (FXS). We have developed a behavioral support protocol designed to obtain high-quality ERP data from children in a single session. Using this approach, ERP data were successfully collected from participants with ASD, FXS, and typical development (TD). Higher success rates were observed for children with ASD and TD than children with FXS. Unique clinical-behavioral characteristics were associated with successful data collection across these groups. Higher chronological age, nonverbal mental age, and receptive language skills were associated with a greater number of valid trials completed in children with ASD. In contrast, higher language ability, lower autism severity, increased anxiety, and increased sensory hyperresponsivity were associated with a greater number of valid trials completed in children with FXS. This work indicates that a "one-size-fits-all" approach cannot be taken to ERP research on children with NDDs, but that a single-session paradigm is feasible and is intended to promote increased representation of children with NDDs in neuroscience research through development of ERP methods that support inclusion of diverse and representative samples.

Face-sensitive brain responses in the first year of life.

Cortical areas in the ventral visual pathway become selectively tuned towards the processing of faces compared to non-face stimuli beginning around 3 months of age and continuing over the first year. Studies using event-related potentials in the EEG (ERPs) have found an ERP component, the N290, that displays specificity for human faces. Other components, such as the P1, P400, and Nc have been studied to a lesser degree in their responsiveness to human faces. However, little is known about the systematic changes in the neural responses to faces during the first year of life, and the localization of these responses in infants' brain. We examined ERP responses to pictures of faces and objects in infants from 4.5 months through 12 months in a cross-sectional study. We investigated the activity of all the components reported to be involved in infant face processing, with particular interest to their amplitude variation and cortical localization. We identified neural regions responsible for the component through the application of cortical source localization methods. We found larger P1 and N290 responses to faces than objects, and these components were localized in the lingual and middle/posterior fusiform gyri, respectively. The amplitude of the P400 was not differentially sensitive to faces over objects. The Nc component was different for faces and objects, was influenced by the infant's attentional state, and localized in medial-anterior brain areas. The implications of these results are discussed in the identification of developmental ERP precursors to face processing.

The developmental trajectory of fronto-temporoparietal connectivity as a proxy of the default mode network: a longitudinal fNIRS investigation.

The default mode network (DMN) is a network of brain regions that is activated while we are not engaged in any particular task. While there is a large volume of research documenting functional connectivity within the DMN in adults, knowledge of the development of this network is still limited. There is some evidence for a gradual increase in the functional connections within the DMN during the first 2 years of life, in contrast to other functional resting-state networks that support primary sensorimotor functions, which are online from very early in life. Previous studies that investigated the development of the DMN acquired data from sleeping infants using fMRI. However, sleep stages are known to affect functional connectivity. In the current longitudinal study, fNIRS was used to measure spontaneous fluctuations in connectivity within fronto-temporoparietal areas-as a proxy for the DMN-in awake participants every 6 months from 11 months till 36 months. This study validates a method for recording resting-state data from awake infants, and presents a data analysis pipeline for the investigation of functional connections with infant fNIRS data, which will be beneficial for researchers in this field. A gradual development of fronto-temporoparietal connectivity was found, supporting the idea that the DMN develops over the first years of life. Functional connectivity reached its maximum peak at about 24 months, which is consistent with previous findings showing that, by 2 years of age, DMN connectivity is similar to that observed in adults.

The neural correlates of orienting to walking direction in 6-month-old infants: An ERP study.

The ability to detect social signals represents a first step to enter our social world. Behavioral evidence has demonstrated that 6-month-old infants are able to orient their attention toward the position indicated by walking direction, showing faster orienting responses toward stimuli cued by the direction of motion than toward uncued stimuli. The present study investigated the neural mechanisms underpinning this attentional priming effect by using a spatial cueing paradigm and recording EEG (Geodesic System 128 channels) from 6-month-old infants. Infants were presented with a central point-light walker followed by a single peripheral target. The target appeared randomly at a position either congruent or incongruent with the walking direction of the cue. We examined infants' target-locked event-related potential (ERP) responses and we used cortical source analysis to explore which brain regions gave rise to the ERP responses. The P1 component and saccade latencies toward the peripheral target were modulated by the congruency between the walking direction of the cue and the position of the target. Infants' saccade latencies were faster in response to targets appearing at congruent spatial locations. The P1 component was larger in response to congruent than to incongruent targets and a similar congruency effect was found with cortical source analysis in the parahippocampal gyrus and the anterior fusiform gyrus. Overall, these findings suggest that a type of biological motion like the one of a vertebrate walking on the legs can trigger covert orienting of attention in 6-month-old infants, enabling enhancement of neural activity related to visual processing of potentially relevant information as well as a facilitation of oculomotor responses to stimuli appearing at the attended location.

Development of brain functional connectivity and its relation to infant sustained attention in the first year of life.

The study of brain functional connectivity is crucial to understanding the neural mechanisms underlying the improved behavioral performance and amplified ERP responses observed during infant sustained attention. Previous investigations on the development of functional brain connectivity during infancy are primarily confined to the use of functional and structural MRI techniques. The current study examined the relation between infant sustained attention and brain functional connectivity and their development during infancy with high-density EEG recordings. Fifty-nine infants were tested at 6 (N = 15), 8 (N =14), 10 (N = 17), and 12 (N = 13) months. Infant sustained attention was defined by measuring infant heart rate changes during infants' looking. Functional connectivity was estimated from the electrodes on the scalp and with reconstructed cortical source activities in brain regions. It was found that infant sustained attention was accompanied by attenuated functional connectivity in the dorsal attention and default mode networks in the alpha band. Graph theory analyses showed that there was an increase in path length and a decrease in clustering coefficient during infant sustained attention. The functional connectivity within the visual, somatosensory, dorsal attention, and ventral attention networks and graph theory measures of path length and clustering coefficient were found to increase with age. These findings suggest that infant sustained attention is accompanied by distinct patterns of brain functional connectivity. The current findings also suggest the rapid development of functional connectivity in brain networks during infancy.

Using functional near-infrared spectroscopy to assess social information processing in poor urban Bangladeshi infants and toddlers.

Children living in low-resource settings are at risk for failing to reach their developmental potential. While the behavioral outcomes of growing up in such settings are well-known, the neural mechanisms underpinning poor outcomes have not been well elucidated, particularly in the context of low- and middle-income countries. In this study, we measure brain metabolic responses to social and nonsocial stimuli in a cohort of 6- and 36-month-old Bangladeshi children. Study participants in both cohorts lived in an urban slum and were exposed to a broad range of adversity early in life including extreme poverty, malnutrition, recurrent infections, and low maternal education. We observed brain regions that responded selectively to social stimuli in both ages indicating that these specialized brain responses are online from an early age. We additionally show that the magnitude of the socially selective response is related to maternal education, maternal stress, and the caregiving environment. Ultimately our results suggest that a variety of psychosocial hazards have a measurable relationship with the developing social brain.

Infant Visual Attention and Stimulus Repetition Effects on Object Recognition.

This study examined behavioral, heart rate (HR), and event-related potential (ERP) correlates of attention and recognition memory for 4.5-, 6-, and 7.5-month-old infants (N = 45) during stimulus encoding. Attention was utilized as an independent variable using HR measures. The Nc ERP component associated with attention and the late slow wave (LSW) associated with recognition memory were analyzed. The 7.5-month-olds demonstrated a significant reduction in Nc amplitude with stimulus repetition. This reduction in Nc was not found for younger infants. Additionally, infants only demonstrated differential LSW amplitude based on stimulus type on attentive trials as defined by HR changes. These findings indicate that from 4.5 to 7.5 months, infants' attentional engagement is influenced by an increasingly broader range of stimulus characteristics.

The Lateral Occipital Cortex Is Selective for Object Shape, Not Texture/Color, at Six Months.

Understanding how the human visual system develops is crucial to understanding the nature and organization of our complex and varied visual representations. However, previous investigations of the development of the visual system using fMRI are primarily confined to a subset of the visual system (high-level vision: faces, scenes) and relatively late in visual development (starting at 4-5 years of age). The current study extends our understanding of human visual development by presenting the first systematic investigation of a mid-level visual region [the lateral occipital cortex (LOC)] in a population much younger than has been investigated in the past: 6 month olds. We use functional near-infrared spectroscopy (fNIRS), an emerging optical method for recording cortical hemodynamics, to perform neuroimaging with this very young population. Whereas previous fNIRS studies have suffered from imprecise neuroanatomical localization, we rely on the most rigorous MR coregistration of fNIRS data to date to image the infant LOC. We find surprising evidence that at 6 months the LOC has functional specialization that is highly similar to adults. Following Cant and Goodale (2007), we investigate whether the LOC tracks shape information and not other cues to object identity (e.g., texture/material). This finding extends evidence of LOC specialization from early childhood into infancy and earlier than developmental trajectories of high-level visual regions.SIGNIFICANCE STATEMENT Understanding visual development is crucial to understanding the nature of visual representations in the human brain. Previous studies of visual development have investigated children (4 years and older) and high-level visual areas. This study expands our knowledge of visual development by investigating the functional development of mid-level vision [lateral occipital cortex (LOC)] early in infancy. We find surprisingly adult-like functional specialization of the LOC by 6 months of age: infants exhibit shape selectivity, but not object selectivity, in this region.

Development of infant sustained attention and its relation to EEG oscillations: an EEG and cortical source analysis study.

The current study examined the relation between infant sustained attention and infant EEG oscillations. Fifty-nine infants were tested at 6 (N = 15), 8 (N = 17), 10 (N = 14), and 12 (N = 13) months. Three attention phases, stimulus orienting, sustained attention, and attention termination, were defined based on infants' heart rate changes. Frequency analysis using simultaneously recorded EEG focused on infant theta (2-6 Hz), alpha (6-9 Hz), and beta (9-14 Hz) rhythms. Cortical source analysis of EEG oscillations was conducted with realistic infant MRI models. Theta synchronization was found over fontal pole, temporal, and parietal electrodes during infant sustained attention for 10 and 12 months. Alpha desynchronization was found over frontal, central and parietal electrodes during sustained attention. This alpha effect started to emerge at 10 months and became well established by 12 months. No difference was found for the beta rhythm between different attention phases. The theta synchronization effect was localized to the orbital frontal, temporal pole, and ventral temporal areas. The alpha desynchronization effect was localized to the brain regions composing the default mode network including the posterior cingulate cortex and precuneus, medial prefrontal cortex, and inferior parietal gyrus. The alpha desynchronization effect was also localized to the pre- and post-central gyri. The present study demonstrates a connection between infant sustained attention and EEG oscillatory activities.

Top-down modulation in the infant brain: Learning-induced expectations rapidly affect the sensory cortex at 6 months.

Recent theoretical work emphasizes the role of expectation in neural processing, shifting the focus from feed-forward cortical hierarchies to models that include extensive feedback (e.g., predictive coding). Empirical support for expectation-related feedback is compelling but restricted to adult humans and nonhuman animals. Given the considerable differences in neural organization, connectivity, and efficiency between infant and adult brains, it is a crucial yet open question whether expectation-related feedback is an inherent property of the cortex (i.e., operational early in development) or whether expectation-related feedback develops with extensive experience and neural maturation. To determine whether infants' expectations about future sensory input modulate their sensory cortices without the confounds of stimulus novelty or repetition suppression, we used a cross-modal (audiovisual) omission paradigm and used functional near-infrared spectroscopy (fNIRS) to record hemodynamic responses in the infant cortex. We show that the occipital cortex of 6-month-old infants exhibits the signature of expectation-based feedback. Crucially, we found that this region does not respond to auditory stimuli if they are not predictive of a visual event. Overall, these findings suggest that the young infant's brain is already capable of some rudimentary form of expectation-based feedback.

Development of the error-monitoring system from ages 9-35: Unique insight provided by MRI-constrained source localization of EEG.

The ability to self-detect errors and dynamically adapt behavior is a cornerstone of higher-level cognition, requiring coordinated activity from a network of neural regions. However, disagreement exists over how the error-monitoring system develops throughout adolescence and early adulthood. The present report leveraged MRI-constrained EEG source localization to detail typical development of the error-monitoring system in a sample of 9-35 year-olds (n = 43). Participants performed a flanker task while high-density EEG was recorded; structural MRIs were also acquired for all participants. Analysis of the scalp-recorded EEG data revealed a frontocentral negativity (error-related negativity; ERN) immediately following errors for all participants, although the topography of the ERN varied with age. Source localization of the ERN time range revealed maximal activity within the posterior cingulate cortex (PCC) for all ages, consistent with recent evidence that the PCC provides a substantial contribution to the scalp-recorded ERN. Activity within a network of brain regions, including dorsal anterior cingulate, PCC, and parietal cortex, was predictive of improved performance following errors, regardless of age. However, additional activity within insula, orbitofrontal cortex and inferior frontal gyrus linearly increased with age. Together, these data suggest that the core error-monitoring system is online by early adolescence and remains relatively stable into adulthood. However, additional brain regions become embedded within this core network with age. These results serve as a model of typical development of the error-monitoring system from early adolescence into adulthood.

The Relation between Infant Covert Orienting, Sustained Attention and Brain Activity.

This study used measures of event-related potentials (ERPs) and cortical source analysis to examine the effect of covert orienting and sustained attention on 3- and 4.5-month-old infants' brain activity in a spatial cueing paradigm. Cortical source analysis was conducted with current density reconstruction using realistic head models created from age-appropriate infant MRIs. The validity effect was found in the P1 ERP component that was greater for valid than neutral trials in the electrodes contralateral to the visual targets when the stimulus onset asynchrony (SOA) was short. Cortical source analysis revealed greater current density amplitude around the P1 peak latency in the contralateral inferior occipital and ventral temporal regions for valid than neutral and invalid trials. The processing cost effect was found in the N1 ERP component that was greater for neutral than invalid trials in the short SOA condition. This processing cost effect was also shown in the current density amplitude around the N1 peak latency in the contralateral inferior and middle occipital and middle and superior temporal regions. Infant sustained attention was found to modulate infants' brain responses in covert orienting by enhancing the P1 ERP responses and current density amplitude in their cortical sources during sustained attention. These findings suggest that the neural mechanisms that underpin covert orienting already exist in 3- to 4.5-month-old, and they could be facilitated by infant sustained attention.