Advancing early relational health: a collaborative exploration of a research agenda.

Here, we introduce the Early Relational Health (ERH) Learning Community's bold, large-scale, collaborative, data-driven and practice-informed research agenda focused on furthering our mechanistic understanding of ERH and identifying feasible and effective practices for making ERH promotion a routine and integrated component of pediatric primary care. The ERH Learning Community, formed by a team of parent/caregiver leaders, pediatric care clinicians, researchers, and early childhood development specialists, is a workgroup of Nurture Connection-a hub geared toward promoting ERH, i.e., the positive and nurturing relationship between young children and their parent(s)/caregiver(s), in families and communities nationwide. In response to the current child mental health crisis and the American Academy of Pediatrics (AAP) policy statement promoting ERH, the ERH Learning Community held an in-person meeting at the AAP national headquarters in December 2022 where members collaboratively designed an integrated research agenda to advance ERH. This agenda weaves together community partners, clinicians, and academics, melding the principles of participatory engagement and human-centered design, such as early engagement, co-design, iterative feedback, and cultural humility. Here, we present gaps in the ERH literature that prompted this initiative and the co-design activity that led to this novel and iterative community-focused research agenda, with parents/caregivers at the core, and in close collaboration with pediatric clinicians for real-world promotion of ERH in the pediatric primary care setting.

Factor Structure of the Postpartum Bonding Questionnaire in a US-Based Cohort of Mothers.

As research efforts in the field of pediatrics are oriented toward a better understanding of the synergistic relationship between different facets of early relational health (ERH) and child development and wellbeing, it is essential to focus on the quality of research instruments available for measuring different components of ERH. This study investigates the measurement characteristics of a widely used parent/caregiver-reported measure of bonding, the Postpartum Bonding Questionnaire (PBQ), in a US-based sample (n=610) of English-speaking biological mothers who completed the PBQ at 4 months postpartum. To evaluate the factor structure of the PBQ, confirmatory and exploratory statistical techniques were employed. The current study failed to replicate the PBQ's original 4-factor structure. Exploratory factor analysis results supported the creation of a 14-item abbreviated measure, the PBQ-14. The PBQ-14 showed evidence of good psychometric properties, including high internal consistency (ω=.87) and correlation with depression (r=.44, p<.001) assessed using the Patient Health Questionnaire (PHQ-9), as would be expected. The new unidimensional PBQ-14 is suitable for use in the US as a measure of general postnatal parent/caregiver-to-infant bonding.

The influence of social motivation on neural correlates of cognitive control in girls.

Motivation influences cognitive control, particularly in childhood and adolescence. Previous work finds that the error-related negativity (ERN), an event-related potential (ERP) linked to cognitive control following errors, is influenced by social motivation. However, it is unclear whether the influences of social motivation on the ERN extend to stimulus-locked neural correlates of cognitive control. This study reexamines how social motivation influences cognitive control in adolescence by exploring motivational influences on two stimulus-locked ERPs; the N2 and P3. Adolescent girls (8-17 years of age) completed a flanker task under two different conditions. In the social condition, girls were led to believe that they were evaluated by a peer during a flanker task. In the nonsocial condition, girls completed a flanker task while evaluated by a computer. Results revealed that all girls exhibited a larger P3 in social as compared to nonsocial contexts, whereas the N2 was not different between contexts. In addition, the largest P3 enhancements were observed among younger girls. These findings suggest that social motivation influences some ERP components related to cognitive control, and such influences change across development. Additionally, findings suggest the importance of including multiple ERPs when interpreting the functional significance of motivation on cognitive control.

Measurement of parental executive function in early childhood settings: Instrument reliability and validity in community-led research projects.

A growing number of early childhood (EC) parenting programs target adult executive function (EF) to build responsive parenting behaviors and to promote positive child development. Although measurement of EF is well understood in academic research, little work has examined EF measurement in community settings. The present study examined psychometric properties of the Behavior Rating Inventory of Executive Function-Adult Version among 203 parents whose children were enrolled in EC programs serving under-resourced communities. We calculated Cronbach's α and mean-item correlations to test internal consistency reliability. To test factor structure, we conducted exploratory factor analysis and confirmatory factor analyses. Results suggest adequate internal consistency and that factor structures, beyond the original proposed, are appropriate for our community sample. Together, findings indicate that self-report measures of adult EF may perform differently for families experiencing adversity, raising questions about the acceptability of clinical EF tools in in underserved communities.

Alpha electroencephalogram (EEG) asymmetry among toddlers in foster care.

The majority of children living in foster care in the United States have a history of maltreatment and/or disrupted caregiving. Maltreatment in early childhood adversely affects development at many levels, including neurobiology and behavior. One neurobiological measure associated with maltreatment is alpha electroencephalogram (EEG) asymmetry. Prior research has found greater right frontal asymmetry among children with a history of maltreatment. However, little research has been extended developmentally downward to examine alpha asymmetry and its behavioral correlates among toddlers in foster care; this was the purpose of the present study. Differences in EEG asymmetry were examined between a sample of foster toddlers (mean age = 3.21 years, n = 38) and a community comparison, low-income sample without a history of foster care (mean age = 3.04 years, n = 16). The toddlers in the foster care group exhibited greater right alpha asymmetry, primarily driven by differences in parietal asymmetry. Neither frontal nor parietal asymmetry were clearly related to internalizing or externalizing behaviors, measured concurrently or at previous time points. These findings reveal differences in alpha EEG asymmetry among toddlers in foster care, and highlight the need to better understand associations between neurobiological and behavioral functioning following early adversity.

Advancing clinical neuroscience through enhanced tools: Pediatric social anxiety as an example.

BACKGROUND: Clinical researchers face challenges when trying to quantify diverse processes engaged during social interactions. We report results from two studies, each demonstrating the potential utility of tools for examining processes engaged during social interactions. METHOD: In the first study, youth (n = 57) used a smartphone-based tool to rate mood and responses to social events. A subset (n = 20) completed the second, functional magnetic resonance imaging study. This second study related anxiety to error-evoked brain responses in two social conditions-while being observed and when alone. We also combined these tools to bridge clinical, social-contextual, and neural levels of measurement. RESULTS: Results from the first study showed an association between negatively-perceived social experiences and a range of negative emotions. In the second study there was a positive correlation during error monitoring between social-anxiety severity and context-specific activation of the pregenual anterior cingulate cortex. Finally, during imaging, the perceived quality of peer interactions as assessed using the smartphone-based tool, interacted with social context to predict levels of activation in the hippocampus and superior frontal gyrus. CONCLUSIONS: By improving measurement, enhanced tools may provide new means for studying relationships among anxiety, brain function, and social interactions.

Adolescent cognitive control, theta oscillations, and social observation.

Theta oscillations (4-8 Hz) provide an organizing principle of cognitive control, allowing goal-directed behavior. In adults, theta power over medial-frontal cortex (MFC) underlies conflict/error monitoring, whereas theta connectivity between MFC and lateral-frontal regions reflects cognitive control recruitment. However, prior work has not separated theta responses that occur before and immediately after a motor response, nor explained how medial-lateral connectivity drives different kinds of control behaviors. Theta's role during adolescence, a developmental window characterized by a motivation-control mismatch also remains unclear. As social observation is known to influence motivation, this might be a particularly important context for studying adolescent theta dynamics. Here, adolescents performed a flanker task alone or under social observation. Focusing first on the nonsocial context, we parsed cognitive control into dissociable subprocesses, illustrating how theta indexes distinct components of cognitive control working together dynamically to produce goal-directed behavior. We separated theta power immediately before/after motor responses, identifying behavioral links to conflict monitoring and error monitoring, respectively. MFC connectivity was separated before/after responses and behaviorally-linked to reactive and proactive control, respectively. Finally, distinct forms of post-error control were dissociated, based on connectivity with rostral/caudal frontal cortex. Social observation was found to exclusively upregulate theta measures indexing post-response error monitoring and proactive control, as opposed to conflict monitoring and reactive control. Linking adolescent cognitive control to theta oscillations provides a bridge between non-invasive recordings in humans and mechanistic studies of neural oscillations in animal models; links to social observation provide insight into the motivation-control interactions that occur during adolescence.

Approach, avoidance, and the detection of conflict in the development of behavioral inhibition.

Motivation has played an integral role in understanding personality development. Two motivational systems, one associated with seeking reward (approach motivation) and one associated with avoidance of threat (avoidance motivation), have been theorized to represent individual differences in behavioral responses to the environment. However, contextual factors, particularly those with a high degree of novelty, ambiguity, and unpredictability, may simultaneously activate both systems, thereby causing approach-avoidance conflict. The resulting behavior, commonly called inhibition, is characterized by an inability to engage in motivated, goal-directed behavior and is theorized to reflect a core component of anxiety. A form of inhibition observed in childhood, behavioral inhibition (BI), is a relatively stable temperamental profile characterized by negative affect in response to unfamiliar and unpredictable contexts and is a risk factor for anxiety. Our review draws from findings in clinical and cognitive neuroscience to argue that BI reflects an increased sensitivity of both approach and avoidance motivational systems, thereby increasing the likelihood of approach-avoidance conflict within the context of unfamiliar or unpredictable stimuli and environments. Such motivational conflict activates neural systems associated with conflict monitoring, which leads to increases in arousal (e.g., sympathetic nervous system activity) and onlooking behavior, two commonly observed characteristics of childhood BI.

Social influences of error monitoring in adolescent girls.

Adolescence is a developmental period characterized by increased social motivation and a heightened concern of peer evaluation. However, little research has examined social influences on neural functioning in adolescence. One psychophysiological measure of motivation, the error-related negativity (ERN), is an ERP following an error. In adults, the ERN is enhanced by contextual factors that influence motivation, such as social observation and evaluation. The current study examined relations among age and neural responses in social contexts in adolescence. Seventy-six adolescent girls (9-17 years old) completed a flanker task under two different conditions. In the social condition, adolescent girls were informed that two other adolescents would be observing and providing feedback about their performance. In the nonsocial condition, adolescent girls completed a flanker task alone and were told feedback was computer generated. Results revealed that younger adolescents exhibited a larger ERN in social contexts than nonsocial contexts. In contrast, there were no differences in the ERN between contexts among older adolescents. In addition, enhancements of the ERN in social contexts among younger adolescents diminished the relation between the ERN and age. These findings suggest that the ERN is sensitive to social contexts in early adolescence, and developmental changes in the ERN may be partially explained by contextual factors that influence motivation.

A Neurobehavioral Mechanism Linking Behaviorally Inhibited Temperament and Later Adolescent Social Anxiety.

OBJECTIVE: Behavioral inhibition (BI) is a temperament identified in early childhood that is a risk factor for later social anxiety. However, mechanisms underlying the development of social anxiety remain unclear. To better understand the emergence of social anxiety, longitudinal studies investigating changes at behavioral neural levels are needed. METHOD: BI was assessed in the laboratory at 2 and 3 years of age (N = 268). Children returned at 12 years, and an electroencephalogram was recorded while children performed a flanker task under 2 conditions: once while believing they were being observed by peers and once while not being observed. This methodology isolated changes in error monitoring (error-related negativity) and behavior (post-error reaction time slowing) as a function of social context. At 12 years, current social anxiety symptoms and lifetime diagnoses of social anxiety were obtained. RESULTS: Childhood BI prospectively predicted social-specific error-related negativity increases and social anxiety symptoms in adolescence; these symptoms directly related to clinical diagnoses. Serial mediation analysis showed that social error-related negativity changes explained relations between BI and social anxiety symptoms (n = 107) and diagnosis (n = 92), but only insofar as social context also led to increased post-error reaction time slowing (a measure of error preoccupation); this model was not significantly related to generalized anxiety. CONCLUSION: Results extend prior work on socially induced changes in error monitoring and error preoccupation. These measures could index a neurobehavioral mechanism linking BI to adolescent social anxiety symptoms and diagnosis. This mechanism could relate more strongly to social than to generalized anxiety in the peri-adolescent period.

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.

Contextual startle responses moderate the relation between behavioral inhibition and anxiety in middle childhood.

Behavioral inhibition (BI), a temperament characterized in early childhood by wariness and avoidance of novelty, is a risk factor for anxiety disorders. An enhanced startle response has been observed in adolescents characterized with BI in childhood, particularly when they also manifest concurrent symptoms of anxiety. However, no prior study has examined relations among BI, startle responsivity, and anxiety in a prospective manner. Data for the present study were from a longitudinal study of infant temperament. Maternal reports and observations of BI were assessed at ages 2 and 3. At age 7, participants completed a startle procedure, while electromyography was collected, where participants viewed different colors on a screen that were associated with either the delivery of an aversive stimulus (i.e., puff of air to the larynx; threat cue) or the absence of the aversive stimulus (i.e., safety cue). Parental reports of child anxiety were collected when children were 7 and 9 years of age. Results revealed that startle responses at age 7 moderated the relation between early BI and 9-year anxiety. These findings provide insight into one potential mechanism that may place behaviorally inhibited children at risk for anxiety.

Cognitive functioning in socially anxious adults: insights from the NIH Toolbox Cognition Battery.

Theory suggests that individuals with social anxiety manifest unique patterns of cognition with less efficient fluid cognition and unperturbed crystallized cognition; however, empirical support for these ideas remains inconclusive. The heterogeneity of past findings may reflect unreliability in cognitive assessments or the influence of confounding variables. The present study examined the relations among social anxiety and performance on the reliable, newly established NIH Toolbox Cognition Battery. Results indicate that high socially anxious adults performed as well as low anxious participants on all measures of fluid cognition. However, high socially anxious adults demonstrated enhanced crystallized cognitive abilities relative to a low socially anxious comparison group.

Individual differences in social anxiety affect the salience of errors in social contexts.

The error-related negativity (ERN) is an event-related potential that occurs approximately 50 ms after an erroneous response. The magnitude of the ERN is influenced by contextual factors, such as when errors are made during social evaluation. The ERN is also influenced by individual differences in anxiety, and it is elevated among anxious individuals. However, little research has examined how individual differences in anxiety interact with contextual factors to impact the ERN. Social anxiety involves fear and apprehension of social evaluation. In the present study, we explored how individual differences in social anxiety interact with social contexts to modulate the ERN. The ERN was measured in 43 young adults characterized as being either high or low in social anxiety, while they completed a flanker task in two contexts: alone and during social evaluation. The results revealed a significant interaction between social anxiety and context, such that the ERN was enhanced in a social relative to a nonsocial context only among highly socially anxious individuals. Furthermore, the degree of such enhancement significantly correlated with individual differences in social anxiety. These findings demonstrate that social anxiety is characterized by enhanced neural activity to errors in social-evaluative contexts.

Caregiver-mediated intervention for low-resourced preschoolers with autism: an RCT.

OBJECTIVES: To compare 2 short-term, community caregiver training interventions for preschool-aged children with Autism Spectrum Disorder who had low resources. Low resource was defined by the US Department of Housing and Urban Development low-income index or 1 "indicator," (e.g., Medicaid eligibility). Child outcomes focused on joint engagement, joint attention, and play. METHODS: Participants included 112 families of a child who had Autism Spectrum Disorder who met criteria for being low-resourced and who were randomly assigned to 1 of 2 3-month interventions, group caregiver education or individualized caregiver-mediated intervention (CMM). Children were assessed for social communication skills pre- and post-treatment, and followed up at 3 months. RESULTS: All children improved in joint engagement and initiating joint attention, with significantly greater improvement by the CMM group. Outcomes on play skills were mixed, with improvement of symbolic play for the CMM group and no change in functional play skills. Joint engagement maintained over time for the CMM group, and initiating joint attention maintained for both groups over time. CONCLUSIONS: This study is among the first randomized trials comparing 2 active interventions with a large sample of low-resourced families. Results suggest improvements in core autism deficits of joint engagement, joint attention, and symbolic play with relatively brief, caregiver-mediated interventions, but additional support is necessary to maintain and generalize these gains over time.

Individual differences in fear potentiated startle in behaviorally inhibited children.

Behavioral inhibition (BI) is a temperament characterized during early childhood by increased fearfulness to novelty, social reticence to unfamiliar peers, and heightened risk for the development of anxiety. Heightened startle responses to safety cues have been found among behaviorally inhibited adolescents who have an anxiety disorder suggesting that this measure may serve as a biomarker for the development of anxiety amongst this risk population. However, it is unknown if these aberrant startle patterns emerge prior to the manifestation of anxiety in this temperament group. The current study examined potentiated startle in 7-year-old children characterized with BI early in life. High behaviorally inhibited children displayed increased startle magnitude to safety cues, particularly during the first half of the task, and faster startle responses compared to low behaviorally inhibited children. These findings suggest that aberrant startle responses are apparent in behaviorally inhibited children during early childhood prior to the onset of a disorder and may serve as a possible endophenotype for the development of anxiety.