Probing the content of affective semantic memory following caregiving-related early adversity.

Cognitive science has demonstrated that we construct knowledge about the world by abstracting patterns from routinely encountered experiences and storing them as semantic memories. This preregistered study tested the hypothesis that caregiving-related early adversities (crEAs) shape affective semantic memories to reflect the content of those adverse interpersonal-affective experiences. We also tested the hypothesis that because affective semantic memories may continue to evolve in response to later-occurring positive experiences, child-perceived attachment security will inform their content. The sample comprised 160 children (ages 6-12 at Visit 1; 87F/73 M), 66% of whom experienced crEAs (n = 105). At Visit 1, crEA exposure prior to study enrollment was operationalized as parental-reports endorsing a history of crEAs (abuse/neglect, permanent/significant parent-child separation); while child-reports assessed concurrent attachment security. A false memory task was administered online ∼2.5 years later (Visit 2) to probe the content of affective semantic memories-specifically attachment schemas. Results showed that crEA exposure (vs. no exposure) was associated with a higher likelihood of falsely endorsing insecure (vs. secure) schema scenes. Attachment security moderated the association between crEA exposure and insecure schema-based false recognition. Findings suggest that interpersonal-affective semantic schemas include representations of parent-child interactions that may capture the quality of one's own attachment experiences and that these representations shape how children remember attachment-relevant narrative events. Findings are also consistent with the hypothesis that these affective semantic memories can be modified by later experiences. Moving forward, the approach taken in this study provides a means of operationalizing Bowlby's notion of internal working models within a cognitive neuroscience framework. RESEARCH HIGHLIGHTS: Affective semantic memories representing insecure schema knowledge (child needs + needs-not-met) may be more salient, elaborated, and persistent among youths exposed to early caregiving adversity. All youths, irrespective of early caregiving adversity exposure, may possess affective semantic memories that represent knowledge of secure schemas (child needs + needs-met). Establishing secure relationships with parents following early-occurring caregiving adversity may attenuate the expression of insecure semantic memories, suggesting potential malleability. Affective semantic memories include schema representations of parent-child interactions that may capture the quality of one's own attachment experiences and shape how youths remember attachment-relevant events.

The effects of parental presence on amygdala and mPFC activation during fear conditioning: An exploratory study.

Learning safe versus dangerous cues is crucial for survival. During development, parents can influence fear learning by buffering their children's stress response and increasing exploration of potentially aversive stimuli. Rodent findings suggest that these behavioral effects are mediated through parental presence modulation of the amygdala and medial prefrontal cortex (mPFC). Here, we investigated whether similar parental modulation of amygdala and mPFC during fear learning occurs in humans. Using a within-subjects design, behavioral (final N = 48, 6-17 years, mean = 11.61, SD = 2.84, 60% females/40% males) and neuroimaging data (final N = 39, 6-17 years, mean = 12.03, SD = 2.98, 59% females/41% males) were acquired during a classical fear conditioning task, which included a CS+ followed by an aversive noise (US; 75% reinforcement rate) and a CS-. Conditioning occurred once in physical contact with the participant's parent and once alone (order counterbalanced). Region of interest analyses examined the unconditioned stress response by BOLD activation to the US (vs. implicit baseline) and learning by activation to the CS+ (vs. CS-). Results showed that during US presentation, parental presence reduced the centromedial amygdala activity, suggesting buffering of the unconditioned stress response. In response to learned stimuli, parental presence reduced mPFC activity to the CS+ (relative to the CS-), although this result did not survive multiple comparisons' correction. These preliminary findings indicate that parents modulate amygdala and mPFC activity during exposure to unconditioned and conditioned fear stimuli, potentially providing insight into the neural mechanisms by which parents act as a social buffer during fear learning. RESEARCH HIGHLIGHTS: (1)This study used a within-participant experimental design to investigate how parental presence (vs. absence) affects youth's neural responses in a classical fear conditioning task. (2)Parental presence reduced the youth's centromedial amygdala activation to the unconditioned stimulus (US), suggesting parental buffering of the neural unconditioned response (UR). (3)Parental presence reduced the youth's mPFC activation to a conditioned threat cue (CS+) compared to a safety cue (CS-), suggesting possible parental modulation of fear learning.

Perceived and Observed Treatment Gains Following PEERS: A Preliminary Study with Latinx Adolescents with ASD.

The Program for the Education and Enrichment of Relational Skills (PEERS) social skills intervention has demonstrated effectiveness for adolescents with autism spectrum disorder (ASD). However, studies have been limited by a lack of objective outcome measures and an underrepresentation of Latinx families. This pilot study extends the PEERS literature by utilizing an observational measure of conversational skills (Contextual Assessment of Social Skills; CASS) with a diverse sample of 13 adolescents with ASD (with parent groups conducted in English and Spanish simultaneously) and a control group of 11 neurotypical adolescents. Consistent with previous research, adolescents with ASD and their parents perceived improvements in social functioning following intervention, which were maintained four months later and corroborated by improvements in conversational skills.

Systemic Racism in EEG Research: Considerations and Potential Solutions.

The current theoretical paper discusses the unintended systemic racism and racial biases that impact neuroscience, specifically in research utilizing electroencephalography (EEG). As a popular technique in affective science research, EEG requires adherence between the electrode and scalp to measure brain activity. To obtain high-quality data, various factors such as hair length, hair type, body movement, and/or extraneous noise from the environment are taken into consideration. As EEG researchers attempt to gather good-quality data, the recruitment and retention of Black American participants is challenging due to hairstyles commonly worn by Black American participants (e.g., cornrows, braids) and hair type. Taken together, the systemic lack of data from Black American participants renders research findings less generalizable and causes disparities in theoretical knowledge applicable to this population. To address this disparity, innovative solutions invented by bioengineers are discussed.

Fear modulates parental orienting during childhood and adolescence.

Adults quickly orient toward sources of danger and deploy fight-or-flight tactics to manage threatening situations. In contrast, infants who cannot implement the safety strategies available to adults and depend heavily on caregivers for survival are more likely to turn toward familiar adults, such as their parents, to help them navigate threatening circumstances. However, work has yet to investigate how readily children and adolescents orient toward their parents in threatening or fearful contexts. The current work addressed this question using a visual search paradigm that included arrays of parents' and strangers' faces as target and distractor stimuli, preceded by a fear or neutral emotional priming procedure. Linear mixed-effects models showed that children and adolescents (N = 88, age range = 4-17 years; 42M/46F) were faster to search for the face of their parent than of a stranger. However, fear priming attenuated this effect of the parent on search times, such that children and adolescents were significantly slower to orient toward their parent in an array of strangers' faces if they were first primed with fear as opposed to a neutral video. This work indicates that fear priming may phasically interfere with parental orienting during childhood and adolescence, possibly because fear reallocates attention away from parents and toward (potentially threatening) unfamiliar people in the environment to facilitate the development of independent threat learning and coping systems.

Heterogeneity in caregiving-related early adversity: Creating stable dimensions and subtypes.

Early psychosocial adversities exist at many levels, including caregiving-related, extrafamilial, and sociodemographic, which despite their high interrelatedness may have unique impacts on development. In this paper, we focus on caregiving-related early adversities (crEAs) and parse the heterogeneity of crEAs via data reduction techniques that identify experiential cooccurrences. Using network science, we characterized crEA cooccurrences to represent the comorbidity of crEA experiences across a sample of school-age children (n = 258; 6-12 years old) with a history of crEAs. crEA dimensions (variable level) and crEA subtypes (subject level) were identified using parallel factor analysis/principal component analysis and graph-based Louvain community detection. Bagging enhancement with cross-validation provided estimates of robustness. These data-driven dimensions/subtypes showed evidence of stability, transcended traditional sociolegally defined groups, were more homogenous than sociolegally defined groups, and reduced statistical correlations with sociodemographic factors. Finally, random forests showed both unique and common predictive importance of the crEA dimensions/subtypes for childhood mental health symptoms and academic skills. These data-driven outcomes provide additional tools and recommendations for crEA data reduction to inform precision medicine efforts in this area.

Being the third wheel: Toddlers use bystander learning to acquire cue-specific valence knowledge.

Observing others is an important means of gathering information by proxy regarding safety and danger, a form of learning that is available as early as infancy. In two experiments, we examined the specificity and retention of emotional eavesdropping (i.e., bystander learning) on cue-specific discriminant learning during toddlerhood. After witnessing one adult admonish another for playing with Toy A (with no admonishment for Toy B), toddlers learned to choose Toy B for themselves regardless of whether they were tested immediately or 2 weeks later (Experiment 1). However, if asked to make a toy choice for someone else (i.e., when toddlers' personal risk was lower), approximately half the toddlers instead selected Toy A (Experiment 2). However, such choices were accompanied by toddlers' social monitoring of the adults, suggesting that toddlers may have been attempting to safely gain (via surrogacy) more information about risk contingencies. These findings suggest that toddlers can learn to discriminate valence in a cue-specific manner through social observation.

Shifting children's attentional focus to emotions during art museum experiences.

Art exposure can influence children's emotional growth, but little is known about tools that aid emotional development in art museums. We implemented attentional and social manipulations to test whether (1) modifications to unscripted instructions and (2) caregiver prompts shape children's attentional focus towards either the emotional or elemental content (e.g., colour and medium) of paintings. These manipulations occurred within an on-going art museum education programme. Afterwards, children's (N = 60; ages 3-13 years) attentional focus towards emotions or elements was assessed by asking them to select words that best described the art. Children focused on emotion more, but the instructional manipulation successfully influenced word choices towards the targeted focus. Caregiver prompts also influenced focus towards the elements and away from emotions. These findings highlight that children's attention to art's emotional content can be altered by social context, which here was demonstrated within a museum programme.

Investigating Changes in Reward-Related Neural Correlates After PEERS Intervention in Adolescents With ASD: Preliminary Evidence of a "Precision Medicine" Approach.

Background: The Social Motivation Hypothesis proposes that individuals with autism spectrum disorder (ASD) experience social interactions as less rewarding than their neurotypical (TD) peers, which may lead to reduced social initiation. Existing studies of the brain's reward system in individuals with ASD report varied findings for anticipation of and response to social rewards. Given discrepant findings, the anticipation of and response to social rewards should be further evaluated, particularly in the context of intervention outcome. We hypothesized that individual characteristics may help predict neural changes from pre- to post-intervention. Methods: Thirteen adolescents with ASD received the Program for the Education and Enrichment of Relational Skills (PEERS) intervention for 16 weeks; reward-related EEG was collected before and after intervention. Fourteen TD adolescents were tested at two timepoints but did not receive intervention. Event-related potentials were calculated to measure anticipation of (stimulus-preceding negativity; SPN) and response to (reward-related positivity; RewP) social and non-social rewards. Additionally, measures of social responsiveness, social skills, and intervention-engagement were collected. Group differences were analyzed as well as individual differences using prediction models. Result: Parent-reported social responsiveness and social skills improved in adolescents with ASD after participation in PEERS. ASD adolescents displayed marginally decreased anticipation of social rewards at post-intervention compared to pre-intervention. Regression models demonstrated that older adolescents and those with lower parent-reported social motivation prior to participation in PEERS displayed marginally increased social reward anticipation (more robust SPN) from pre- to post-intervention. Participants who displayed more parent-reported social motivation before intervention and were more actively engaged in the PEERS intervention evidenced increased social reward processing (more robust RewP) from pre- to post-intervention. Conclusion: Findings suggest that there may be differences in saliency between wanting/anticipating social rewards vs. liking/responding to social rewards in individuals with ASD. Our findings support the hypothesis that identification of individual differences may predict which adolescents are poised to benefit the most from particular interventions. As such, reported findings set the stage for the advancement of "precision medicine." This investigation is a critical step forward in our ability to understand and predict individual response to interventions in individuals with ASD.

Adaptation in the face of adversity: Decrements and enhancements in children's cognitive control behavior following early caregiving instability.

Cognitive control is typically described as disrupted following exposure to early caregiving instability. While much of the work within this field has approached cognitive control broadly, evidence from adults retrospectively reporting early-life instability has shown more nuanced effects on cognitive control, even demonstrating enhancements in certain subdomains. That is, exposure to unstable caregiving may disrupt some areas of cognitive control, yet promote adaptation in others. Here, we investigated three domains of cognitive control in a sample of school-age children (N = 275, Age = 6-12 years) as a function of early caregiving instability, defined as the total number of caregiving switches. Results demonstrated that caregiving instability was associated with reduced response inhibition (Go/No-Go) and attentional control (Flanker), but enhanced cognitive flexibility (Dimensional Change Card Sort Task Switching). Conversely, there were no statistically significant associations with group (i.e., institutional care versus foster care) or maltreatment exposure and these patterns. These findings build on the specialization framework, suggesting that caregiving instability results in both decrements and enhancements in children's cognitive control, consistent with the hypothesis that cognitive control development is scaffolded by early environmental pressures.

Child-parent cardiac transference is decreased following disrupted/absent early care.

Parental input shapes youth self-regulation development, and a lack of sensitive caregiving is a risk factor for youth mental health problems. Parents may shape youth regulation through their influence over biological (including neural) and behavioral development during childhood at both micro (moment-to-moment) and macro (global) levels. Prior studies have shown that micro-level parent-child interactions shape youth's biology contributing to youth mental health. However, it remains unclear whether prior disrupted/absent care affects those moment-to-moment parent-youth interactions in ways that increase risk for youth psychopathology. In the current study, we calculated transfer entropy on cardiac data from parent-youth dyads where the youth had either been exposed to disrupted care prior to adoption or not. Transfer Entropy (TE) tracks information flow between two signals, enhancing quantification of directional coupling, allowing for the examination of parent-child and child-parent influences. Using this novel approach, we identified lower cardiac information transfer from youth-to-parents in dyads where the youth had been exposed to disrupted/absent early care. Moreover we showed that the degree to which the parent's physiology changed in response to youth's physiology was negatively related to the youth's mental health, representing a potential pathway for elevated mental health risk in populations exposed to disrupted/absent early care.

Age-Related Increases in Posterior Hippocampal Granularity Are Associated with Remote Detailed Episodic Memory in Development.

Episodic memory is critical to human functioning. In adults, episodic memory involves a distributed neural circuit in which the hippocampus plays a central role. As episodic memory abilities continue to develop across childhood and into adolescence, studying episodic memory maturation can provide insight into the development and construction of these hippocampal networks, and ultimately clues to their function in adulthood. While past developmental studies have shown that the hippocampus helps to support memory in middle childhood and adolescence, the extent to which ongoing maturation within the hippocampus contributes to developmental change in episodic memory abilities remains unclear. In contrast, slower maturing regions, such as the PFC, have been suggested to be the neurobiological locus of memory improvements into adolescence. However, it is also possible that the methods used to detect hippocampal development during middle childhood and adolescence are not sensitive enough. Here, we examine how temporal covariance (or differentiation) in voxel representations within anterior and posterior hippocampus change with age to support the development of detailed recollection in male and female developing humans. We find age-related increases in the distinctiveness of temporal activation profiles in the posterior, but not anterior, hippocampus. Second, we show that this measure of granularity, when present during postencoding rest periods, correlates with the recall of detailed memories of preceding stimuli several weeks postencoding, suggesting that granularity may promote memory stabilization.SIGNIFICANCE STATEMENT Studying hippocampal maturation can provide insight into episodic memory development, as well as clues to episodic functioning in adulthood. Past work has shown evidence both for and against hippocampal contributions to age-related improvements in memory performance, but has relied heavily on univariate approaches (averaging activity across hippocampal voxels), which may not be sensitive to nuanced developmental change. Here we use a novel approach, examining time signatures in individual hippocampal voxels to reveal regionally specific (anterior vs posterior hippocampus) differences in the distinctiveness (granularity) of temporal activation profiles across development. Importantly, posterior hippocampus granularity during windows of putative memory stabilization was associated with long-term memory specificity. This suggests that the posterior hippocampus gradually builds the capacity to support detailed episodic recall.

Longitudinal changes in amygdala, hippocampus and cortisol development following early caregiving adversity.

Although decades of research have shown associations between early caregiving adversity, stress physiology and limbic brain volume (e.g., amygdala, hippocampus), the developmental trajectories of these phenotypes are not well characterized. In the current study, we used an accelerated longitudinal design to assess the development of stress physiology, amygdala, and hippocampal volume following early institutional care. Previously Institutionalized (PI; N = 93) and comparison (COMP; N = 161) youth (ages 4-20 years old) completed 1-3 waves of data collection, each spaced approximately 2 years apart, for diurnal cortisol (N = 239) and structural MRI (N = 156). We observed a developmental shift in morning cortisol in the PI group, with blunted levels in childhood and heightened levels in late adolescence. PI history was associated with reduced hippocampal volume and reduced growth rate of the amygdala, resulting in smaller volumes by adolescence. Amygdala and hippocampal volumes were also prospectively associated with future morning cortisol in both groups. These results indicate that adversity-related physiological and neural phenotypes are not stationary during development but instead exhibit dynamic and interdependent changes from early childhood to early adulthood.

An exploration of amygdala-prefrontal mechanisms in the intergenerational transmission of learned fear.

Humans learn about their environments by observing others, including what to fear and what to trust. Observational fear learning may be especially important early in life when children turn to their parents to gather information about their world. Yet, the vast majority of empirical research on fear learning in youth has thus far focused on firsthand classical conditioning, which may fail to capture one of the primary means by which fears are acquired during development. To address this gap in the literature, the present study examined observational fear learning in youth (n = 33; age range: 6-17 years) as they watched videos of their parent and an "unfamiliar parent" (i.e., another participant's parent) undergo fear conditioning. Youth demonstrated stronger fear learning when observing their parent compared to an unfamiliar parent, as indicated by changes in their self-reported liking of the stimuli to which their parents were conditioned (CS+, a geometric shape paired with an aversive noise; CS-, a geometric shape never paired with an aversive noise) and amygdala responses. Parent trait anxiety was associated with youth learning better (i.e., reporting a stronger preference for the CS- relative to CS+), and exhibiting stronger medial prefrontal-amygdala connectivity. Neuroimaging data were additionally acquired from a subset of parents during firsthand conditioning, and parental amygdala and mPFC activation were associated with youth's neural recruitment. Together, these results suggest that youth preferentially learn fears via observation of their parents, and this learning is associated with emotional traits and neural recruitment in parents.