Smiling synchronization predicts interaction enjoyment in peer dyads of autistic and neurotypical youth.

LAY ABSTRACT: For autistic and neurotypical youth, having positive social interactions with other youth is an important part of well-being. Other researchers have found that one factor that can make people feel like social interactions have gone well is synchronization. Synchronization happens when peoples' body movements and facial expressions align while they're interacting. We focus on smiling synchronization here because other studies have found that when neurotypical individuals synchronize their smiles more in a social interaction, they say they enjoy that social interaction more. However, no studies have directly tested whether smiling synchrony influences social interaction enjoyment in autistic and neurotypical youth. We measured smiling synchrony in pairs of interacting autistic and neurotypical youth who were meeting each other for the first time. Some pairs were autistic youth interacting with other autistic youth (autistic with autistic participant pairs), some pairs were autistic youth interacting with neurotypical youth (autistic with neurotypical participant pairs), and other pairs were neurotypical youth interacting with neurotypical youth (neurotypical with neurotypical participant pairs). We found that autistic with neurotypical participant pairs had lower smiling synchrony than neurotypical with neurotypical participant pairs. Youth who were in dyads that had more smiling synchrony said they enjoyed interacting with their partner more and that they wanted to interact with their partner again. Our research shows that smiling synchrony is one part of interactions between autistic and neurotypical youth that influences how well youth say the interaction went. Identifying natural opportunities for autistic and neurotypical youth to share positive feelings could be one way to promote positive social interactions between autistic and neurotypical youth.

Examining Adolescents' Mental Health Before and During the COVID-19 Pandemic.

The current study characterized the impact of the COVID-19 pandemic and stay-at-home orders on adolescents' internalizing symptoms and assessed predictors of adolescents' internalizing symptoms during the pandemic. Seventy-nine adolescents (18 autistic, 61 nonautistic) and their parents who participated in a previous study and were at least 10 years old (M = 13.8, SD = 1.7) were invited to participate in three online follow-up surveys post-stay-at-home order (May through November 2020). Measures of children's anxiety and depressive symptoms, parenting practices, family togetherness, conflict, financial problems, and parental mental health during the pandemic were collected. Nonautistic adolescents experienced a significant decrease in anxiety symptoms across the beginning of the pandemic and a significant increase in depressive symptoms from pre- to post-stay-at-home order. Permissive parenting and financial problems predicted adolescents' depressive symptoms. Parental mental health difficulties and permissive parenting predicted adolescents' anxiety symptoms. Results underscore the need to support parents and youth.

Partner similarity and social cognitive traits predict social interaction success among strangers.

Social interactions are a ubiquitous part of engaging in the world around us, and determining what makes an interaction successful is necessary for social well-being. This study examined the separate contributions of individual social cognitive ability and partner similarity to social interaction success among strangers, measured by a cooperative communication task and self-reported interaction quality. Sixty participants engaged in a 1-h virtual social interaction with an unfamiliar partner (a laboratory confederate) including a 30-min cooperative 'mind-reading' game and then completed several individual tasks and surveys. They then underwent a separate functional MRI session in which they passively viewed video clips that varied in content. The neural responses to these videos were correlated with those of their confederate interaction partners to yield a measure of pairwise neural similarity. We found that trait empathy (assessed by the interpersonal reactivity index) and neural similarity to partner both predicted communication success in the mind-reading game. In contrast, perceived similarity to partner and (to a much lesser extent) trait mind-reading motivation predicted self-reported interaction quality. These results highlight the importance of sharing perspectives in successful communication as well as differences between neurobiological similarity and perceived similarity in supporting different types of interaction success.

Neural sensitivity to social reward predicts links between social behavior and loneliness in youth during the COVID-19 pandemic.

Neural reward network sensitivity in youth is proposed to differentially impact the effects of social environments on social outcomes. The COVID-19 pandemic provided an opportunity to test this hypothesis within a context of diminished in-person social interaction. We examined whether neural sensitivity to interactive social reward moderates the relationship between a frequency of interactive or passive social activity and social satisfaction. Survey reports of frequency of interactions with friends, passive social media use, and loneliness and social satisfaction were gathered in 2020 during mandated precautions limiting in-person contact. A subset of participants (age = 10-17) previously participated in a functional magnetic resonance imaging (fMRI) study examining social-interactive reward during a simulated peer interaction (survey n = 76; survey + fMRI n = 40). We found evidence of differential response to social context, such that youth with higher neural reward sensitivity showed a negative association between a frequency of interactive connections with friends and a combined loneliness and social dissatisfaction component (LSDC) score, whereas those with lower sensitivity showed the opposite effect. Further, high reward sensitivity was associated with greater LSDC as passive social media use increased, whereas low reward sensitivity showed the opposite. This indicates that youth with greater sensitivity to social-interactive reward may be more susceptible to negative effects of infrequent contact than their low reward-sensitive counterparts, who instead maintain social well-being through passive viewing of social content. These differential outcomes could have implications for supporting youth during times of major social disruption as well as ensuring mental health and well-being more broadly.

Social reward network connectivity differs between autistic and neurotypical youth during social interaction.

A core feature of autism is difficulties with social interaction. Atypical social motivation is proposed to underlie these difficulties. However, prior work testing this hypothesis has shown mixed support and has been limited in its ability to understand real-world social-interactive processes in autism. We attempted to address these limitations by scanning neurotypical and autistic youth (n = 86) during a text-based reciprocal social interaction that mimics a "live" chat and elicits social reward processes. We focused on task-evoked functional connectivity (FC) of regions responsible for motivational-reward and mentalizing processes within the broader social reward circuitry. We found that task-evoked FC between these regions was significantly modulated by social interaction and receipt of social-interactive reward. Compared to neurotypical peers, autistic youth showed significantly greater task-evoked connectivity of core regions in the mentalizing network (e.g., posterior superior temporal sulcus) and the amygdala, a key node in the reward network. Furthermore, across groups, the connectivity strength between these mentalizing and reward regions was negatively correlated with self-reported social motivation and social reward during the scanner task. Our results highlight an important role of FC within the broader social reward circuitry for social-interactive reward. Specifically, greater context-dependent FC (i.e., differences between social engagement and non-social engagement) may indicate an increased "neural effort" during social reward and relate to differences in social motivation within autistic and neurotypical populations.

Posterior superior temporal cortex connectivity is related to social communication in toddlers.

The second year of life is a time when social communication skills typically develop, but this growth may be slower in toddlers with language delay. In the current study, we examined how brain functional connectivity is related to social communication abilities in a sample of 12-24 month-old toddlers including those with typical development (TD) and those with language delays (LD). We used an a-priori, seed-based approach to identify regions forming a functional network with the left posterior superior temporal cortex (LpSTC), a region associated with language and social communication in older children and adults. Social communication and language abilities were assessed using the Communication and Symbolic Behavior Scales (CSBS) and Mullen Scales of Early Learning. We found a significant association between concurrent CSBS scores and functional connectivity between the LpSTC and the right posterior superior temporal cortex (RpSTC), with greater connectivity between these regions associated with better social communication abilities. However, functional connectivity was not related to rate of change or language outcomes at 36 months of age. These data suggest an early marker of low communication abilities may be decreased connectivity between the left and right pSTC. Future longitudinal studies should test whether this neurobiological feature is predictive of later social or communication impairments.

Irritability in early to middle childhood: Cross-sectional and longitudinal associations with resting state amygdala and ventral striatum connectivity.

BACKGROUND: Irritability is a common symptom that may affect children's brain development. This study aims to (1) characterize age-dependent and age-independent neural correlates of irritability in a sample of 4-8 year old children, and (2) examine early irritability as a predictor of change in brain connectivity over time. METHODS: Typically developing children, ages 4-8 years, with varying levels of irritability were included. Resting state fMRI and parent-rated irritability (via Child Behavior Checklist; CBCL) were collected at up to three time points, resulting in a cross-sectional sample at baseline (N = 176, M = 6.27, SD = 1.49), and two subsamples consisting of children who were either 4 or 6 years old at baseline that were followed longitudinally for two additional timepoints, one- and two-years post-baseline. That is, a "younger" cohort (age 4 at baseline, n = 34, M age = 4.44, SD = 0.25) and an "older" cohort (age 6 at baseline, n = 29, M age = 6.50, SD = 0.30). Across our exploratory analyses, we examined how irritability related to seed-based intrinsic connectivity via whole-brain connectivity ANCOVAs using the left and right amygdala, and left and right ventral striatum as seed regions. RESULTS: Cross-sectionally, higher levels of irritability were associated with greater amygdala connectivity with the posterior cingulate, controlling for child age. No age-dependent effects were observed in the cross-sectional analyses. Longitudinal analyses in the younger cohort revealed that early higher vs. lower levels of irritability, controlling for later irritability, were associated with decreases in amygdala and ventral striatum connectivity with multiple frontal and parietal regions over time. There were no significant findings in the older cohort. CONCLUSIONS: Findings suggest that irritability is related to altered neural connectivity during rest regardless of age in early to middle childhood and that early childhood irritability may be linked to altered changes in neural connectivity over time. Understanding how childhood irritability interacts with neural processes can inform pathophysiological models of pediatric irritability and the development of targeted mechanistic interventions.

Social-interactive reward elicits similar neural response in autism and typical development and predicts future social experiences.

Challenges in initiating and responding to social-interactive exchanges are a key diagnostic feature of autism spectrum disorder, yet investigations into the underlying neural mechanisms of social interaction have been hampered by reliance on non-interactive approaches. Using an innovative social-interactive neuroscience approach, we investigated differences between youth with autism and youth with typical development in neural response to a chat-based social-interactive reward, as well as factors such as age and self-reported social enjoyment that may account for heterogeneity in that response. We found minimal group differences in neural and behavioral response to social-interactive reward, and variation within both groups was related to self-reported social enjoyment during the task. Furthermore, neural sensitivity to social-interactive reward predicted future enjoyment of a face-to-face social interaction with a novel peer. These findings have important implications for understanding the nature of social reward and peer interactions in typical development as well as for future research informing social interactions in individuals on the autism spectrum.

Longitudinal Change in Adolescent Depression and Anxiety Symptoms from before to during the COVID-19 Pandemic.

This study aimed to examine changes in depression and anxiety symptoms from before to during the first 6 months of the COVID-19 pandemic in a sample of 1,339 adolescents (9-18 years old, 59% female) from three countries. We also examined if age, race/ethnicity, disease burden, or strictness of government restrictions moderated change in symptoms. Data from 12 longitudinal studies (10 U.S., 1 Netherlands, 1 Peru) were combined. Linear mixed effect models showed that depression, but not anxiety, symptoms increased significantly (median increase = 28%). The most negative mental health impacts were reported by multiracial adolescents and those under 'lockdown' restrictions. Policy makers need to consider these impacts by investing in ways to support adolescents' mental health during the pandemic.

Theory of mind in naturalistic conversations between autistic and typically developing children and adolescents.

LAY ABSTRACT: Conversation is a key part of everyday social interactions. Previous studies have suggested that conversational skills are related to theory of mind, the ability to think about other people's mental states, such as beliefs, knowledge, and emotions. Both theory of mind and conversation are common areas of difficulty for autistic people, yet few studies have investigated how people, including autistic people, use theory of mind during conversation. We developed a new way of measuring cToM using two rating scales: cToM Positive captures behaviors that show consideration of a conversation partner's mental states, such as referring to their thoughts or feelings, whereas cToM Negative captures behaviors that show a lack of theory of mind through violations of neurotypical conversational norms, such as providing too much, too little, or irrelevant information. We measured cToM in 50 pairs of autistic and typically developing children (ages 8-16 years) during 5-min "getting to know you" conversations. Compared to typically developing children, autistic children displayed more frequent cToM Negative behaviors but very similar rates of cToM Positive behaviors. Across both groups, cToM Negative (but not Positive) ratings were related to difficulties in recognizing emotions from facial expressions and a lower tendency to talk about others' mental states spontaneously (i.e., without being instructed to do so), which suggests that both abilities are important for theory of mind in conversation. Altogether, this study highlights both strengths and difficulties among autistic individuals, and it suggests possible avenues for further research and for improving conversational skills.

A tale of two connectivities: intra- and inter-subject functional connectivity jointly enable better prediction of social abilities.

Naturalistic functional magnetic resonance imaging (fMRI) paradigms, such as movie viewing, are attracting increased attention, given their ability to mimic the real-world cognitive demands on attention and multimodal sensory integration. Moreover, naturalistic paradigms allow for characterizing brain network responses associated with dynamic social cognition in a model-free manner using inter-subject functional connectivity (ISFC). While intra-subject functional connectivity (FC) characterizes the individual's brain functional architecture, ISFC characterizes the neural coupling driven by time-locked extrinsic dynamic stimuli across individuals. Here, we hypothesized that ISFC and FC provide distinct and complementary information about individual differences in social cognition. To test this hypothesis, we examined a public movie-viewing fMRI dataset with 32 healthy adults and 90 typically developing children. Building three partial least squares regression (PLS) models to predict social abilities using FC and/or ISFC, we compared predictive performance to determine whether combining two connectivity measures could improve the prediction accuracy of individuals' social-cognitive abilities measured by a Theory of Mind (ToM) assessment. Our results indicated that the joint model (ISFC + FC) yielded the highest predictive accuracy and significantly predicted individuals' social cognitive abilities (rho = 0.34, p < 0.001). We also confirmed that the improved accuracy was not due to the increased feature dimensionality. In conclusion, we demonstrated that intra-/inter-subject connectivity encodes unique information about social abilities, and a joint investigation could help us gain a more complete understanding of the complex processes supporting social cognition.

Neural similarity between mentalizing and live social interaction during the transition to adolescence.

Social interactions are essential for human development, yet little neuroimaging research has examined their underlying neurocognitive mechanisms using socially interactive paradigms during childhood and adolescence. Recent neuroimaging research has revealed activity in the mentalizing network when children engage with a live social partner, even when mentalizing is not required. While this finding suggests that social-interactive contexts may spontaneously engage mentalizing, it is not a direct test of how similarly the brain responds to these two contexts. The current study used representational similarity analysis on data from 8- to 14-year-olds who made mental and nonmental judgments about an abstract character and a live interaction partner during fMRI. A within-subject, 2 (Mental/Nonmental) × 2 (Peer/Character) design enabled us to examine response pattern similarity between conditions, and estimate fit to three conceptual models of how the two contexts relate: (1) social interaction and mentalizing about an abstract character are represented similarly; (2) interactive peers and abstract characters are represented differently regardless of the evaluation type; and (3) mental and nonmental states are represented dissimilarly regardless of target. We found that the temporal poles represent mentalizing and peer interactions similarly (Model 1), suggesting a neurocognitive link between the two in these regions. Much of the rest of the social brain exhibits different representations of interactive peers and abstract characters (Model 2). Our findings highlight the importance of studying social-cognitive processes using interactive approaches, and the utility of pattern-based analyses for understanding how social-cognitive processes relate to each other.

Developmental differences in brain functional connectivity during social interaction in middle childhood.

The transition from childhood to adolescence is marked by significant changes in peer interactions. However, limited research has examined the brain systems (e.g., mentalizing and reward networks) involved in direct peer interaction, particularly during childhood and early adolescence. Here, we analyzed fMRI data from 50 children aged 8-12 years while they participated in a task in which they chatted with a peer (Peer) or answered questions about a story character (Character). Using a beta-series correlation analysis, we investigated how social interaction modulates functional connectivity within and between mentalizing and reward networks and whether this modulation changes with age. We observed effects of social interaction on functional connectivity were modulated by age within the mentalizing and reward networks. Further, greater connectivity within and between these networks during social interaction was related to faster reaction time to the Peer versus Character condition. Similar effects were found in the salience and mirror neuron networks. These findings provide insights into age-related differences in how the brain supports social interaction, and thus have the potential to advance our understanding of core social difficulties in social-communicative disorders, such as autism spectrum disorder.

Examining Associations Between Amygdala Volumes and Anxiety Symptoms in Autism Spectrum Disorder.

BACKGROUND: Anxiety is one of the most common co-occurring conditions in people with autism spectrum disorder. The amygdala has been identified as being associated with anxiety in populations with and without autism, yet associations in autism were based on relatively small or developmentally constrained samples, leaving questions as to whether these results hold at different developmental ages and in a larger, more robust sample. METHODS: Structural neuroimaging and parent report of anxiety symptoms of children ages 5-13 years with (n = 123) and without (n = 171) a diagnosis of autism were collected from the University of Maryland and three sites from the Autism Brain Imaging Data Exchange. Standardized residuals for bilateral amygdala volumes were computed adjusting for site, hemispheric volumes, and covariates (age, sex, Full Scale IQ). RESULTS: Clinically significant anxiety symptoms did not differentiate amygdala volumes between groups (i.e., autism and anxiety, autism without anxiety, without autism or anxiety). No significant association between left or right amygdala volumes and anxiety scores was observed among the sample of individuals with autism. Meta-analytic and Bayes factor estimations provided additional support for the null hypothesis. Age, sex, and autism severity did not moderate associations between anxiety and amygdala volumes. CONCLUSIONS: No relation between amygdala volumes and anxiety symptoms in children with autism was observed in the largest sample to investigate this question. We discuss directions for future research to determine whether additional factors including age or method of assessment may contribute to this lack of association.

Effects of social and emotional context on neural activation and synchrony during movie viewing.

Sharing emotional experiences impacts how we perceive and interact with the world, but the neural mechanisms that support this sharing are not well characterized. In this study, participants (N = 52) watched videos in an MRI scanner in the presence of an unfamiliar peer. Videos varied in valence and social context (i.e., participants believed their partner was viewing the same (joint condition) or a different (solo condition) video). Reported togetherness increased during positive videos regardless of social condition, indicating that positive contexts may lessen the experience of being alone. Two analysis approaches were used to examine both sustained neural activity averaged over time and dynamic synchrony throughout the videos. Both approaches revealed clusters in the medial prefrontal cortex that were more responsive to the joint condition. We observed a time-averaged social-emotion interaction in the ventromedial prefrontal cortex, although this region did not demonstrate synchrony effects. Alternatively, social-emotion interactions in the amygdala and superior temporal sulcus showed greater neural synchrony in the joint compared to solo conditions during positive videos, but the opposite pattern for negative videos. These findings suggest that positive stimuli may be more salient when experienced together, suggesting a mechanism for forming social bonds.

Read my lips! Perception of speech in noise by preschool children with autism and the impact of watching the speaker's face.

BACKGROUND: Adults and adolescents with autism spectrum disorders show greater difficulties comprehending speech in the presence of noise. Moreover, while neurotypical adults use visual cues on the mouth to help them understand speech in background noise, differences in attention to human faces in autism may affect use of these visual cues. No work has yet examined these skills in toddlers with ASD, despite the fact that they are frequently faced with noisy, multitalker environments. METHODS: Children aged 2-5 years, both with and without autism spectrum disorder (ASD), saw pairs of images in a preferential looking study and were instructed to look at one of the two objects. Sentences were presented in the presence of quiet or another background talker (noise). On half of the trials, the face of the target person speaking was presented, while half had no face present. Growth-curve modeling was used to examine the time course of children's looking to the appropriate vs. opposite image. RESULTS: Noise impaired performance for both children with ASD and their age- and language-matched peers. When there was no face present on the screen, the effect of noise was generally similar across groups with and without ASD. But when the face was present, the noise had a more detrimental effect on children with ASD than their language-matched peers, suggesting neurotypical children were better able to use visual cues on the speaker's face to aid performance. Moreover, those children with ASD who attended more to the speaker's face showed better listening performance in the presence of noise. CONCLUSIONS: Young children both with and without ASD show poorer performance comprehending speech in the presence of another talker than in quiet. However, results suggest that neurotypical children may be better able to make use of face cues to partially counteract the effects of noise. Children with ASD varied in their use of face cues, but those children who spent more time attending to the face of the target speaker appeared less disadvantaged by the presence of background noise, indicating a potential path for future interventions.

Explaining Variance in Social Symptoms of Children with Autism Spectrum Disorder.

The social symptoms of autism spectrum disorder are likely influenced by multiple psychological processes, yet most previous studies have focused on a single social domain. In school-aged autistic children (n = 49), we compared the amount of variance in social symptoms uniquely explained by theory of mind (ToM), biological motion perception, empathy, social reward, and social anxiety. Parent-reported emotional contagion-the aspect of empathy in which one shares another's emotion-emerged as the most important predictor, explaining 11-14% of the variance in social symptoms, with higher levels of emotional contagion predicting lower social symptom severity. Our findings highlight the role of mutual emotional experiences in social-interactive success, as well as the limitations of standard measures of ToM and social processing in general.

A conceptual model of risk and protective factors associated with internalizing symptoms in autism spectrum disorder: A scoping review, synthesis, and call for more research.

This paper reviews and synthesizes key areas of research related to the etiology, development, and maintenance of internalizing symptoms in children, adolescents, and adults with autism spectrum disorder (ASD). In developing an integrated conceptual model, we draw from current conceptual models of internalizing symptoms in ASD and extend the model to include factors related to internalizing within other populations (e.g., children that have experienced early life stress, children with other neurodevelopmental conditions, typically developing children) that have not been systematically examined in ASD. Our review highlights the need for more research to understand the developmental course of internalizing symptoms, potential moderators, and the interplay between early risk and protective factors. Longitudinal studies incorporating multiple methods and both environmental and biological factors will be important in order to elucidate these mechanisms.

Functional near-infrared spectroscopy in toddlers: Neural differentiation of communicative cues and relation to future language abilities.

The toddler and preschool years are a time of significant development in both expressive and receptive communication abilities. However, little is known about the neurobiological underpinnings of language development during this period, likely due to difficulties acquiring functional neuroimaging data. Functional near-infrared spectroscopy (fNIRS) is a motion-tolerant neuroimaging technique that assesses cortical brain activity and can be used in very young children. Here, we use fNIRS during perception of communicative and noncommunicative speech and gestures in typically developing 2- and 3-year-olds (Study 1, n = 15, n = 12 respectively) and in a sample of 2-year-olds with both fNIRS data collected at age 2 and language outcome data at age 3 (Study 2, n = 18). In Study 1, 2- and 3-year-olds differentiated between communicative and noncommunicative stimuli as well as between speech and gestures in the left lateral frontal region. However, 2-year-olds showed different patterns of activation from 3-year-olds in right medial frontal regions. In Study 2, which included two toddlers identified with early language delays along with 16 typically developing toddlers, neural differentiation of communicative stimuli in the right medial frontal region at age 2 predicted receptive language at age 3. Specifically, after accounting for variance related to verbal ability at age 2, increased neural activation for communicative gestures (vs. both communicative speech and noncommunicative gestures) at age 2 predicted higher receptive language scores at age 3. These results are discussed in the context of the underlying mechanisms of toddler language development and use of fNIRS in prediction of language outcomes.