The role of attentional shifting in the relation between error monitoring and anxiety in youth.

The error-related negativity (ERN), a well-established neural marker of anxiety, reflects enhanced attention to internal threat signals. While attention to threat plays a crucial role in the development and maintenance of anxiety, it is unclear how attentional control influences the ERN-anxiety association. To address this, 37 youths (Mage = 10.89 years) completed self-report measures of attentional control and anxiety symptoms. To obtain ERN amplitude, youth completed a flanker task while simultaneous EEG was collected. Attentional control, specifically attentional shifting rather than focusing, moderated the relation between ERN amplitude and anxiety. Youth who displayed smaller neural responses to making an error and higher ability to shift attention experienced lower levels of anxiety, relative to those who exhibited larger neural responses to making an error or lower attention-shifting ability. These findings highlight that response magnitude to internal threat and ability to flexibly shift attention may jointly contribute to anxiety in youth.

Repetitive negative thinking and depressive symptoms are differentially related to response inhibition: The influence of non-emotional, socio-emotional, and self-referential stimuli.

Identifying transdiagnostic correlates of response inhibition deficits is important for understanding risk for internalizing disorders. Little work has compared the relationships between internalizing symptoms and repetitive negative thinking (RNT) with response inhibition across non-emotional and emotional domains, and no work has compared these relationships for inhibition of socio-emotional relative to self-referential stimuli. Undergraduate students (N = 71, 18.44 ± 0.71 years) selected on extremes of internalizing symptoms completed the Perseverative Thinking Questionnaire (PTQ) and a Go/No-Go paradigm using non-emotional stimuli, other individuals' sad facial expressions, and participants' own sad facial expressions. Participants exhibited more commission errors for sad facial expressions than non-emotional trials, though commission errors for others' and participants' own sad facial expressions did not differ. Depressive symptoms were associated with poorer inhibition of non-emotional stimuli; however, PTQ scores were associated with more successful inhibition of non-emotional stimuli. Our results provide evidence that transdiagnostic RNT as assessed by the PTQ may be related to better inhibition in non-emotional domains, but negative emotional stimuli may interfere with successful inhibition for those with high RNT, while depressive symptoms were linked to poorer inhibition of non-emotional stimuli. These findings have implications for internalizing disorders, which often are accompanied by RNT.

Childhood wayfinding experience explains sex and individual differences in adult wayfinding strategy and anxiety.

BACKGROUND: Anyone who has ever found themselves lost while driving in an unfamiliar neighborhood or forgotten where they parked their car can appreciate the importance of being able to navigate their environment. Navigation, or wayfinding, is a large-scale spatial ability that involves keeping track of the relative positions of objects and features in space, which allows for determining the path to a goal location. Early experiences shape spatial skill development, and research finds sex differences in spatial behaviors from preschool through adulthood, with males consistently outperforming females. The basis for sex differences in spatial aptitude is still debated, but explanations include differences in childhood spatial experience, the use of strategies for solving large-scale spatial problems, and spatial anxiety. The current study seeks to understand childhood wayfinding factors that may influence sex and individual differences in wayfinding strategies and wayfinding anxiety in adulthood. METHOD: One hundred fifty-nine undergraduate psychology students reported their childhood wayfinding experience (i.e., time spent outside, distance traveled), current use of wayfinding strategies (i.e., route strategy, orientation strategy), and current wayfinding anxiety and general anxiety levels. RESULTS: Independent samples t tests revealed that, compared with females, males reported spending more time outside and traveling farther distances as children, having less current wayfinding anxiety and route strategy use, and having more current orientation strategy use. Mediation analyses found that distance traveled, but not time spent outdoors, during childhood mediated sex differences in route strategy use and wayfinding anxiety in adults, even when controlling for general anxiety. Furthermore, when controlling for participant sex and general anxiety, current wayfinding anxiety mediated the relationship between distance traveled during childhood and route strategy use in adults. CONCLUSION: The current findings provide potential environmental explanations for sex and individual differences in large-scale spatial behaviors, including wayfinding. Specifically, sex differences in early wayfinding experience may explain why males and females develop different strategies for navigating and different levels of wayfinding anxiety. Furthermore, regardless of sex, allowing children to explore and navigate their outdoor environments away from home may help lessen their fears about navigating and, in turn, improve the strategies they choose to traverse unfamiliar territories.

Using hippocampal-dependent eyeblink conditioning to predict individual differences in spatial reorientation strategies in 3- to 6-year-olds.

The hippocampus is a subcortical structure in the medial temporal lobe involved in cognitive functions such as spatial navigation and reorientation, episodic memory, and associative learning. While much is understood about the role of hippocampal function in learning and memory in adults, less is known about the relations between the hippocampus and the development of these cognitive skills in young children due to the limitations of using standard methods (e.g., MRI) to examine brain structure and function in developing populations. This study used hippocampal-dependent trace eyeblink conditioning (EBC) as a feasible approach to examine individual differences in hippocampal functioning as they relate to spatial reorientation and episodic memory performance in young children. Three- to six-year-old children (N = 50) completed tasks that measured EBC, spatial reorientation, and episodic memory, as well as non-hippocampal-dependent processing speed abilities. Results revealed that when age was held constant, individual differences in EBC performance were significantly related to individual differences in performance on the spatial reorientation test, but not on the episodic memory or processing speed tests. When the relations between hippocampal-dependent EBC and different reorientation strategies were explored, it was found that individual differences in hippocampal function predicted the use of geometric information for reorienting in space as opposed to a combined strategy that uses both geometric information and salient visual cues. The utilization of eyeblink conditioning to examine hippocampal function in young populations and its implications for understanding the dissociation between spatial reorientation and episodic memory development are discussed.

Neural Correlates of Attentional Processing of Threat in Youth with and without Anxiety Disorders.

Late-stage attentional processing of threatening stimuli, quantified through event-related potentials (ERPs), differentiates youth with and without anxiety disorders. It is unknown whether early-stage attentional processing of threatening stimuli differentiates these groups. Examining both early and late stage attentional processes in youth may advance knowledge and enhance efforts to identify biomarkers for translational prevention and treatment research. Twenty-one youth with primary DSM-IV-TR anxiety disorders (10 males, ages 8-15 years) and 21 typically developing Controls (15 males, ages 8-16 years) completed a dot probe task while electroencephalography (EEG) was recorded, and ERPs were examined. Youth with anxiety disorders showed significantly larger (more positive) P1 amplitudes for threatening stimuli than for neutral stimuli, and Controls showed the opposite pattern. Youth with anxiety showed larger (more negative) N170 amplitudes compared with Controls. Controls showed significantly larger (more positive) P2 and P3 amplitudes, regardless of stimuli valence, compared with youth with anxiety disorders. ERPs observed during the dot probe task indicate youth with anxiety disorders display distinct neural processing during early stage attentional orienting and processing of faces; this was not the case for Controls. Such results suggest these ERP components may have potential as biomarkers of anxiety disorders in youth.

Individual differences in non-clinical maternal depression impact infant affect and behavior during the still-face paradigm across the first year.

Maternal depression can significantly impact mothers' sensitivity to their infants' needs as well as infants' social and emotional development. The still-face paradigm (SFP) is widely used to assess infants' understanding of the contingency between their own behavior and that of their caregivers, as well as infants' ability to self-regulate arousal levels during sudden changes in maternal responsiveness. Infants of clinically depressed mothers display blunted levels of negative affect compared to infants of non-depressed mothers during the still-face (SF) phase. However, little is known about whether individual differences in elevated, non-clinical levels of maternal depression similarly affect mother-infant interactions. The current study examines the longitudinal effects of non-clinical maternal depression on infant and maternal behaviors during the SFP. Infants (N=63) were assessed at 5 and 9 months and maternal depression was assessed at 5 months using the Beck Depression Inventory (BDI). Infants of mothers with elevated levels of depression displayed less negative engagement during the SF phase compared to infants of mothers with lower levels of depression. This effect was present at 5 months, but not at 9 months. Findings demonstrate that non-clinical levels of maternal depressive symptomatology can have a significant impact on infants' affective regulation during the first half of the first year of life, but this does not necessarily have a long-lasting influence later in infancy. Interventions may want to target mothers with non-clinical depression to promote healthy infant social and emotional development.

Quantifying Motor Experience in the Infant Brain: EEG Power, Coherence, and Mu Desynchronization.

The emergence of new motor skills, such as reaching and walking, dramatically changes how infants engage with the world socially and cognitively. Several examples of how motor experience can cascade into cognitive and social development have been documented, yet a significant knowledge gap remains in our understanding of whether these observed behavioral changes are accompanied by underlying neural changes. We propose that electroencephalography (EEG) measures such as power, coherence, and mu desynchronization are optimal tools to quantify motor experience in the infant brain. In this mini-review, we will summarize existing infant research that has separately assessed the relation between motor, cognitive, or social development with coherence, power, or mu desynchronization. We will discuss how the reviewed neural changes seen in seemingly separate developmental domains may be linked based on existing behavioral evidence. We will further propose that power, coherence, and mu desynchronization be used in research exploring the links between motor experience and cognitive and social development.

A new biomarker to examine the role of hippocampal function in the development of spatial reorientation in children: a review.

Spatial navigation is an adaptive skill that involves determining the route to a particular goal or location, and then traveling that path. A major component of spatial navigation is spatial reorientation, or the ability to reestablish a sense of direction after being disoriented. The hippocampus is known to be critical for navigating, and has more recently been implicated in reorienting in adults, but relatively little is known about the development of the hippocampus in relation to these large-scale spatial abilities in children. It has been established that, compared to school-aged children, preschool children tend to perform poorly on certain spatial reorientation tasks, suggesting that their hippocampi may not be mature enough to process the demands of such a task. Currently, common techniques used to examine underlying brain activity, such as electroencephalography (EEG) and functional magnetic resonance imaging (fMRI), are not suitable for examining hippocampal development in young children. In the present paper, we argue instead for the use of eyeblink conditioning (EBC), a relatively under-utilized, inexpensive, and safe method that is easy to implement in developing populations. In addition, EBC has a well defined neural circuitry, which includes the hippocampus, making it an ideal tool to indirectly measure hippocampal functioning in young children. In this review, we will evaluate the literature on EBC and its relation to hippocampal development, and discuss the possibility of using EBC as an objective measure of associative learning in relation to large-scale spatial skills. We support the use of EBC as a way to indirectly access hippocampal function in typical and atypical populations in order to characterize the neural substrates associated with the development of spatial reorientation abilities in early childhood. As such, EBC is a potential, simple biomarker for success in tasks that require the hippocampus, including spatial reorientation.

Associations between infant temperament, maternal stress, and infants' sleep across the first year of life.

Effects of temperament and maternal stress on infant sleep behaviors were explored longitudinally. Negative temperament was associated with sleep problems, and with longer sleep latency and night wakefulness, whereas maternal stress was associated with day sleep duration, suggesting infant and maternal characteristics affect sleep differentially.

Eyeblink conditioning: a non-invasive biomarker for neurodevelopmental disorders.

Eyeblink conditioning (EBC) is a classical conditioning paradigm typically used to study the underlying neural processes of learning and memory. EBC has a well-defined neural circuitry, is non-invasive, and can be employed in human infants shortly after birth making it an ideal tool to use in both developing and special populations. In addition, abnormalities in the cerebellum, a region of the brain highly involved in EBC, have been implicated in a number of neurodevelopmental disorders including autism spectrum disorders (ASDs). In the current paper, we review studies that have employed EBC as a biomarker for several neurodevelopmental disorders including fetal alcohol syndrome, Down syndrome, fragile X syndrome, attention deficit/hyperactivity disorder, dyslexia, specific language impairment, and schizophrenia. In addition, we discuss the benefits of using such a tool in individuals with ASD.

Identification of emotional facial expressions among behaviorally inhibited adolescents with lifetime anxiety disorders.

The current study examined differences in emotion expression identification between adolescents characterised with behavioural inhibition (BI) in childhood with and without a lifetime history of anxiety disorder. Participants were originally assessed for BI during toddlerhood and for social reticence during childhood. During adolescence, participants returned to the laboratory and completed a facial emotion identification task and a clinical psychiatric interview. Results revealed that behaviorally inhibited adolescents with a lifetime history of anxiety disorder displayed a lower threshold for identifying fear relative to anger emotion expressions compared to non-anxious behaviorally inhibited adolescents and non-inhibited adolescents with or without anxiety. These findings were specific to behaviorally inhibited adolescents with a lifetime history of social anxiety disorder. Thus, adolescents with a history of both BI and anxiety, specifically social anxiety, are more likely to differ from other adolescents in their identification of fearful facial expressions. This offers further evidence that perturbations in the processing of emotional stimuli may underlie the aetiology of anxiety disorders.

On the causes of early life experience effects: evaluating the role of mom.

Early life experiences are thought to have long-lasting effects on cognitive, emotional, and social function during adulthood. Changes in neuroendocrine function, particularly the hypothalamic-pituitary-adrenal (HPA) axis, contribute to these systems-level behavioral effects. In searching for causal mechanisms underlying these early experience effects, pioneering research has demonstrated an important role for maternal care in offspring development, and this has led to two persistent ideas that permeate current research and thinking: first, environmental impact on the developing infant is mediated through maternal care behavior; second, the more care that a mother provides, the better off her offspring. While a good beginning, the reality is likely more complex. In this review, we critically examine these ideas and propose a computationally-motivated theoretical framework, and within this framework, we consider evidence supporting a hypothesis of maternal modulation. These findings may inform policy decisions in the context of child health and development.

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.

Effects of negative temperament on 5-month-old infants' behavior during the still-face paradigm.

Five-month-old infants characterized as low or high on temperamental negativity participated with their mothers in the still-face paradigm. Compared to low negative infants, high negative infants displayed greater negative engagement during reunion suggesting that infant temperament significantly contributes to individual differences in the still-face effect.

Reducing behavioral inhibition to novelty via systematic neonatal novelty exposure: the influence of maternal hypothalamic-pituitary-adrenal regulation.

BACKGROUND: Behavioral inhibition (BI) to novelty is thought to be a stable temperament type that appears early in life and is a major risk factor for anxiety disorders. In the rat, habituation of such inhibition can be facilitated via neonatal novelty exposure (NNE), thus reducing BI to novelty. Here, we tested the hypothesis that this early intervention effect is modulated by the context of maternal self-stress regulation. METHODS: The NNE was carried out during postnatal days 1-21, in which one half of each litter was exposed to a relatively novel nonhome environment for 3-min daily while the remaining one half stayed in the home cage. After weaning, BI to novelty was assessed in an open field with a measure of disinhibition defined as a greater increase in exploration across two brief trials. Maternal context was characterized by trait measures of hypothalamic-pituitary-adrenal (HPA) axis reactivity, including basal and stress-evoked corticosterone (CORT) responses. RESULTS: Family-to-family variations in the NNE effect were associated with variations in maternal HPA function-a low-basal CORT and high-evoked CORT response profile constituting the context for a novelty-induced facilitation of disinhibition (i.e., a greater increase in exploratory activity over repeated trials) and an opposite HPA profile constituting the context for a novelty-induced reduction of disinhibition. CONCLUSIONS: This result is consistent with the hypothesis that maternal self-stress regulation modulates the effect of early life intervention on BI to novelty and suggests that effective interventions should include strategies to help mothers improve their self-stress regulation.

The predictive nature of individual differences in early associative learning and emerging social behavior.

Across the first year of life, infants achieve remarkable success in their ability to interact in the social world. The hierarchical nature of circuit and skill development predicts that the emergence of social behaviors may depend upon an infant's early abilities to detect contingencies, particularly socially-relevant associations. Here, we examined whether individual differences in the rate of associative learning at one month of age is an enduring predictor of social, imitative, and discriminative behaviors measured across the human infant's first year. One-month learning rate was predictive of social behaviors at 5, 9, and 12 months of age as well as face-evoked discriminative neural activity at 9 months of age. Learning was not related to general cognitive abilities. These results underscore the importance of early contingency learning and suggest the presence of a basic mechanism underlying the ontogeny of social behaviors.

Maternal modulation of novelty effects on physical development.

Familiarity to the mother and the novelty afforded by the postnatal environment are two contrasting sources of neonatal influence. One hypothesis regarding their relationship is the maternal modulation hypothesis, which predicts that the same neonatal stimulation may have different effects depending on the maternal context. Here we tested this hypothesis using physical development, indexed by body weight, as an endpoint and found that, among offspring of mothers with a high initial swim-stress-induced corticosterone (CORT) response, neonatal novelty exposure induced an enhancement in early growth, and among offspring with mothers of a low initial CORT response, the same neonatal stimulation induced an impairment. At an older age, a novelty-induced increase in body weight was also found among offspring of mothers with high postnatal care reliability and a novelty-induced reduction found among offspring of mothers with low care reliability. These results support a maternal modulation of early stimulation effects on physical development and demonstrate that the maternal influence originates from multiple instead of any singular sources. These results (i) significantly extend the findings of maternal modulation from the domain of cognitive development to the domain of physical development; (ii) offer a unifying explanation for a previously inconsistent literature regarding early stimulation effects on body weight; and (iii) highlight the notion that the early experience effect involves no causal primacy but higher order interactions among the initial triggering events and subsequent events involving a multitude of maternal and nonmaternal influences.

Functional specificity in the modulation of novelty exposure effects by reliability of maternal care.

Using the within-litter neonatal novelty exposure procedure, we manipulated newborn pups' environmental novelty independently from natural variations in maternal care. To better translate animal models to human development studies, we introduce a measure for maternal care reliability. We examined how this reliability modulates novelty-exposure-induced effects on offspring cognitive, social, and emotional development and show that maternal care reliability acts in a function-specific manner. We discuss our results within the framework of a maternal reliability-based modulation model.

One-month-old human infants learn about the social world while they sleep.

Although infants display preferences for social stimuli early in their lives, we know relatively little about the mechanisms of infant learning about the social world. In the current set of studies, 1-month-old infants underwent an adapted eyeblink conditioning paradigm to examine learning to both 'social' and non-social cues. While infants were asleep, they were presented with either a 'social' stimulus (a female voice) or one of two non-social stimuli (tone or backward voice) followed by an airpuff presented to the eyelid. Infants in the experimental groups displayed increased learning across trials, regardless of stimulus type. However, infants conditioned to the 'social' stimulus showed increased learning compared to infants conditioned to either of the non-social stimuli. These results suggest a mechanism by which learning about the social world occurs early in life and the power of ecologically valid cues in facilitating that learning.

Dissociation between neonatal novelty-induced preferential maternal care and enhancement in cognitive, social, and emotional functions.

Early life stimulation is known to produce long-lasting changes in the brain and behavior. One such early stimulation method is the neonatal novelty exposure procedure which allows the isolation of the novelty effect from several prominent confounding factors inherent to the neonatal handling procedure. In two previous studies, we found long-lasting novelty effects on different sets of functional measures without accompanying preferential maternal care, even when the observation was made immediately after the novelty manipulation, a time when such preferential care is most likely to be expressed. Here, within a single cohort of Long-Evans male rats, we demonstrate that novelty exposure leads to enhancements across several functional domains, including increased disinhibition to novelty, enhanced spatial and social memory, and reduced aggression, again without the accompaniment of preferential maternal care. These findings extend novelty exposure effects to aggression and replicate previously known novelty exposure effects on spatial and social memory with extension to new developmental stages. Most importantly, these findings do not support the hypothesis that preferential maternal care towards novelty-exposed pups mediates the observed novelty effects. We discuss the possibility that the effects of neonatal novelty exposure are mediated via repeated activation of the hypothalamic-pituitary-adrenal (HPA) axis that serves to inoculate pups for future exposures to novelty and novelty-induced HPA activation and that maternal influence is likely to be expressed via its modulatory role-the mother sets the individual-family specific behavioral and hormonal context to allow the same early life experience to have a family-specific effect.