Parental emotionality is related to preschool children's neural responses to emotional faces.

The ability to accurately decode others' facial expressions is essential for successful social interaction. Previous theories suggest that aspects of parental emotionality-the frequency, persistence and intensity of parents' own emotions-can influence children's emotion perception. Through a combination of mechanisms, parental emotionality may shape how children's brains specialize to respond to emotional expressions, but empirical data are lacking. The present study provides a direct empirical test of the relation between the intensity, persistence and frequency of parents' own emotions and children's neural responses to perceiving emotional expressions. Event-related potentials (ERPs) were recorded as typically developing 3- to 5-year-old children (final Ns = 59 and 50) passively viewed faces expressing different emotional valences (happy, angry and fearful) at full and reduced intensity (100% intense expression and 40% intense expression). We examined relations between parental emotionality and children's mean amplitude ERP N170 and negative central responses. The findings demonstrate a clear relation between parental emotionality and children's neural responses (in the N170 mean amplitude and latency) to emotional expressions and suggest that parents may influence children's emotion-processing neural circuitry.

Utility of linear mixed effects models for event-related potential research with infants and children.

Event-related potentials (ERPs) are advantageous for investigating cognitive development. However, their application in infants/children is challenging given children's difficulty in sitting through the multiple trials required in an ERP task. Thus, a large problem in developmental ERP research is high subject exclusion due to too few analyzable trials. Common analytic approaches (that involve averaging trials within subjects and excluding subjects with too few trials, as in ANOVA and linear regression) work around this problem, but do not mitigate it. Moreover, these practices can lead to inaccuracies in measuring neural signals. The greater the subject exclusion, the more problematic inaccuracies can be. We review recent developmental ERP studies to illustrate the prevalence of these issues. Critically, we demonstrate an alternative approach to ERP analysis-linear mixed effects (LME) modeling-which offers unique utility in developmental ERP research. We demonstrate with simulated and real ERP data from preschool children that commonly employed ANOVAs yield biased results that become more biased as subject exclusion increases. In contrast, LME models yield accurate, unbiased results even when subjects have low trial-counts, and are better able to detect real condition differences. We include tutorials and example code to facilitate LME analyses in future ERP research.

Infants' neural responses to emotional faces are related to maternal anxiety.

BACKGROUND: Postnatal maternal anxiety is common (estimates as high as 40% prevalence) and is associated with altered mother-infant interactions (e.g., reduced maternal emotional expression and engagement). Neural circuitry supporting infants' face and emotion processing develops in their first year. Thus, early exposure to maternal anxiety may impact infants' developing understanding of emotional displays. We examine whether maternal anxiety is associated with individual differences in typically developing infants' neural responses to emotional faces. METHODS: One hundred and forty two mother-infant dyads were assessed when infants were 5, 7, or 12 months old. Infants' electroencephalographic (EEG) data were recorded while passively viewing female happy, fearful, and angry faces. Three event-related potential (ERP) components, each linked to face and emotion processing, were evaluated: NC, N290, and P400. Infant ERP amplitude was related to concurrent maternal-report anxiety assessed with the Spielberger State-Trait Anxiety Inventory (Trait form). RESULTS: Greater maternal anxiety predicted more negative NC amplitude for happy and fearful faces in left and mid-central scalp regions, beyond covarying influences of maternal depression symptoms, infant negative emotionality, and infant age. CONCLUSIONS: Postnatal maternal anxiety is related to infants' neural processing of emotional expressions. Infants of mothers endorsing high trait anxiety may need additional attentional resources to process happy and fearful faces (expressions less likely experienced in mother-infant interactions). Future research should investigate mechanisms underlying this association, given possibilities include experiential, genetic, and prenatal factors.

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.

Continuity in the neural system supporting children's theory of mind development: Longitudinal links between task-independent EEG and task-dependent fMRI.

Children's explicit theory of mind (ToM) understandings change over early childhood. We examined whether there is longitudinal stability in the neurobiological bases of ToM across this time period. A previous study found that source-localized resting EEG alpha attributable to the dorsal medial prefrontal cortex (DMPFC) and right temporoparietal junction (RTPJ) was associated with children's performance on a battery of theory of mind tasks. Here, we investigated a small subset of children (N = 12) in that original study as a preliminary investigation of whether behavioral measures of ToM performance, and/or EEG localized to the DMPFC or RTPJ predicted ToM-specific fMRI responses 3.5 years later. Results showed that preschoolers' behavioral ToM-performance positively predicted later ToM-specific fMRI responses in the DMPFC. Preschoolers' resting EEG attributable to the DMPFC also predicted later ToM-specific fMRI responses in the DMPFC. Given the small sample, results represent a first exploration and require replication. Intriguingly, they suggest that early maturation of the area of the DMPFC related to ToM reasoning is positively linked with its specific recruitment for ToM reasoning later in development, affording implications for characterizing conceptual ToM development, and its underlying neural supports.

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.

An fMRI study of action observation and action execution in childhood.

Although many studies have examined the location and function of the mirror neuron system (MNS) in human adults, we know relatively little about its development. The current study fills this gap by using fMRI to examine for the first time the development of the brain regions implicated in action execution, action observation, and their overlap. We examined age-related differences in brain activation by contrasting a group of children (n = 21) and adults (n = 18). Surfaced-based analyses of action execution and action observation revealed that brain activity for action observation and execution in children is similar to adults, though adults displayed greater activity than children within the right superior parietal lobe during action execution and the occipital lobe during action observation compared to control. Further, within-individual measures of overlapping activation between action observation and execution revealed age-related differences, such that adults, compared to children, displayed more spatial overlap. Moreover, the extent of the overlap in activation across conditions was related to better motor skills and action representation abilities in children. These data indicate that the MNS changes between middle childhood and adulthood. The data also demonstrate the functional significance of the putative MNS to motor skills and action representation during development.

Neural correlates of facial emotion processing in infancy.

In the present study we examined the neural correlates of facial emotion processing in the first year of life using ERP measures and cortical source analysis. EEG data were collected cross-sectionally from 5- (N = 49), 7- (N = 50), and 12-month-old (N = 51) infants while they were viewing images of angry, fearful, and happy faces. The N290 component was found to be larger in amplitude in response to fearful and happy than angry faces in all posterior clusters and showed largest response to fear than the other two emotions only over the right occipital area. The P400 and Nc components were found to be larger in amplitude in response to angry than happy and fearful faces over central and frontal scalp. Cortical source analysis of the N290 component revealed greater cortical activation in the right fusiform face area in response to fearful faces. This effect started to emerge at 5 months and became well established at 7 months, but it disappeared at 12 months. The P400 and Nc components were primarily localized to the PCC/Precuneus where heightened responses to angry faces were observed. The current results suggest the detection of a fearful face in infants' brain can happen shortly (~200-290 ms) after the stimulus onset, and this process may rely on the face network and develop substantially between 5 to 7 months of age. The current findings also suggest the differential processing of angry faces occurred later in the P400/Nc time window, which recruits the PCC/Precuneus and is associated with the allocation of infants' attention.

Does intention matter? Relations between parent pointing, infant pointing, and developing language ability.

Infants' pointing is associated with concurrent and later language development. The communicative intention behind the point-i.e., imperative versus declarative-can affect both the nature and strength of these associations, and is therefore a critical factor to consider. Parents' pointing is associated with both infant pointing and infant language; however, less work has examined the intent behind parents' points. We explore relations between parents' and infants' pointing at the level of communicative intention, and examine how pointing relates to concurrent and longitudinal infant language skills. In a sample of 52 mother-infant dyads, we measured mother and infant pointing at infant age 12-months, and infant expressive and receptive language at 12-, 18-, and 24-months. We found that mothers produced points with a variety of intentions, however we did not find relations between mother and infant pointing within the different communicative intentions. Replicating previous research, infant declarative pointing was related both concurrently and longitudinally to their language ability. Mothers' declarative pointing was related to their infants' concurrent language, while their imperative pointing was not. Further, there was an interaction between parent and infant declarative pointing, such that the positive relation between parents' declarative pointing and their infants' concurrent receptive language was present only for those infants who were also producing declarative points themselves. Findings suggest that parents' declarative pointing may support both their infants' early word learning and, perhaps, provides a model for their infant to begin using points as well. This study constitutes an important initial exploration of these relations.

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.

Action mechanisms for social cognition: behavioral and neural correlates of developing Theory of Mind.

Many psychological theories posit foundational links between two fundamental constructs: (1) our ability to produce, perceive, and represent action; and (2) our ability to understand the meaning and motivation behind the action (i.e. Theory of Mind; ToM). This position is contentious, however, and long-standing competing theories of social-cognitive development debate roles for basic action-processing in ToM. Developmental research is key to investigating these hypotheses, but whether individual differences in neural and behavioral measures of motor action relate to social-cognitive development is unknown. We examined 3- to 5-year-old children's (N = 26) EEG mu-desynchronization during production of object-directed action, and explored associations between mu-desynchronization and children's behavioral motor skills, behavioral action-representation abilities, and behavioral ToM. For children with high (but not low) mu-desynchronization, motor skill related to action-representation abilities, and action-representation mediated relations between motor skill and ToM. Results demonstrate novel foundational links between action-processing and ToM, suggesting that basic motor action may be a key mechanism for social-cognitive development, thus shedding light on the origins and emergence of higher social cognition.

Assessing human mirror activity with EEG mu rhythm: A meta-analysis.

A fundamental issue in cognitive neuroscience is how the brain encodes others' actions and intentions. In recent years, a potential advance in our knowledge on this issue is the discovery of mirror neurons in the motor cortex of the nonhuman primate. These neurons fire to both execution and observation of specific types of actions. Researchers use this evidence to fuel investigations of a human mirror system, suggesting a common neural code for perceptual and motor processes. Among the methods used for inferring mirror system activity in humans are changes in a particular frequency band in the electroencephalogram (EEG) called the mu rhythm. Mu frequency appears to decrease in amplitude (reflecting cortical activity) during both action execution and action observation. The current meta-analysis reviewed 85 studies (1,707 participants) of mu that infer human mirror system activity. Results demonstrated significant effect sizes for mu during execution (Cohen's d = 0.46, N = 701) as well as observation of action (Cohen's d = 0.31, N = 1,508), confirming a mirroring property in the EEG. A number of moderators were examined to determine the specificity of these effects. We frame these meta-analytic findings within the current discussion about the development and functions of a human mirror system, and conclude that changes in EEG mu activity provide a valid means for the study of human neural mirroring. Suggestions for improving the experimental and methodological approaches in using mu to study the human mirror system are offered.

Children's belief- and desire-reasoning in the temporoparietal junction: evidence for specialization from functional near-infrared spectroscopy.

Behaviorally, children's explicit theory of mind (ToM) proceeds in a progression of mental-state understandings: developmentally, children demonstrate accurate explicit desire-reasoning before accurate explicit belief-reasoning. Given its robust and cross-cultural nature, we hypothesize this progression may be paced in part by maturation/specialization of the brain. Neuroimaging research demonstrates that the right temporoparietal junction (TPJ) becomes increasingly selective for ToM reasoning as children age, and as their ToM improves. But this research has narrowly focused on beliefs or on undifferentiated mental-states. A recent ERP study in children included a critical contrast to desire-reasoning, and demonstrated that right posterior potentials differentiated belief-reasoning from desire-reasoning. Taken together, the literature suggests that children's desire-belief progression may be paced by specialization of the right TPJ for belief-reasoning specifically, beyond desire-reasoning. In the present study, we tested this hypothesis directly by examining children's belief- and desire-reasoning using functional near-infrared spectroscopy in conjunction with structural magnetic resonance imaging to pinpoint brain activation in the right TPJ. Results showed greatest activation in the right TPJ for belief-reasoning, beyond desire-reasoning, and beyond non-mental reasoning (control). Findings replicate and critically extend prior ERP results, and provide clear evidence for a specific neural mechanism underlying children's progression from understanding desires to understanding beliefs.

Neural correlates of belief- and desire-reasoning in 7- and 8-year-old children: an event-related potential study.

Theory of mind requires belief- and desire-understanding. Event-related brain potential (ERP) research on belief- and desire-reasoning in adults found mid-frontal activations for both desires and beliefs, and selective right-posterior activations only for beliefs. Developmentally, children understand desires before beliefs; thus, a critical question concerns whether neural specialization for belief-reasoning exists in childhood or develops later. Neural activity was recorded as 7- and 8-year-olds (N = 18) performed the same diverse-desires, diverse-beliefs, and physical control tasks used in a previous adult ERP study. Like adults, mid-frontal scalp activations were found for belief- and desire-reasoning. Moreover, analyses using correct trials alone yielded selective right-posterior activations for belief-reasoning. Results suggest developmental links between increasingly accurate understanding of complex mental states and neural specialization supporting this understanding.

Dopaminergic functioning and preschoolers' theory of mind.

Representational theory of mind (RTM) development follows a universal developmental timetable whereby major advances in reasoning about mental representations occur between the ages of 3 and 5 years old. This progression appears to be only absent in the case of specific neurodevelopmental impairments, such as autism. Taken together, this suggests that neuromaturational factors may play a role in RTM development. Recent EEG work has shown that one neuromaturational factor pacing this universal developmental timetable is the functional maturation of medial prefrontal cortex. The neurotransmitter dopamine (DA) is thought to play a crucial role in typical frontal lobe development. Therefore, the goal of the present study was to investigate the role that DA may play in RTM development. Ninety-one 48-62-month olds were given a battery of RTM tasks along with EEG measurement. EEG recordings were analyzed for eyeblinks, a reliable indicator of DA functioning, and we calculated their average eyeblinks per minute (EBR). Regression analyses showed that EBR was associated with RTM after controlling for children's performance on a Stroop-like measure, language ability, gender, and age. These findings provide evidence that DA functioning is associated with RTM in the preschool years, and are discussed with respect to how DA might provide a mechanism that helps to account for both neurobiological and experiential factors that are known to affect the timetable of preschoolers' RTM development.

Neurodevelopmental correlates of theory of mind in preschool children.

Baseline electroencephalogram (EEG) data were collected from twenty-nine 4-year-old children who also completed batteries of representational theory-of-mind (RTM) tasks and executive functioning (EF) tasks. Neural sources of children's EEG alpha (6-9 Hz) were estimated and analyzed to determine whether individual differences in regional EEG alpha activity predicted children's RTM performance, while statistically controlling for children's age and EF skills. Results showed that individual differences in EEG alpha activity localized to the dorsal medial prefrontal cortex (dMPFC) and the right temporal-parietal juncture (rTPJ) were positively associated with children's RTM performance. These findings suggest that the maturation of dMPFC and rTPJ is a critical constituent of preschoolers' explicit theory-of-mind development.