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

The Neural Bases of Directed and Spontaneous Mental State Attributions to Group Agents

In daily life, perceivers often need to predict and interpret the behavior of group agents, such as corporations and governments. Although research has investigated how perceivers reason about individual members of particular groups, less is known about how perceivers reason about group agents themselves. The present studies investigate how perceivers understand group agents by investigating the extent to which understanding the ‘mind’ of the group as a whole shares important properties and processes with understanding the minds of individuals. Experiment 1 demonstrates that perceivers are sometimes willing to attribute a mental state to a group as a whole even when they are not willing to attribute that mental state to any of the individual members of the group, suggesting that perceivers can reason about the beliefs and desires of group agents over and above those of their individual members. Experiment 2 demonstrates that the degree of activation in brain regions associated with attributing mental states to individuals—i.e., brain regions associated with mentalizing or theory-of-mind, including the medial prefrontal cortex (MPFC), temporo-parietal junction (TPJ), and precuneus—does not distinguish individual from group targets, either when reading statements about those targets' mental states (directed) or when attributing mental states implicitly in order to predict their behavior (spontaneous). Together, these results help to illuminate the processes that support understanding group agents themselves

Using Fiction to Assess Mental State Understanding: A New Task for Assessing Theory of Mind in Adults

Social functioning depends on the ability to attribute and reason about the mental states of others – an ability known as theory of mind (ToM). Research in this field is limited by the use of tasks in which ceiling effects are ubiquitous, rendering them insensitive to individual differences in ToM ability and instances of subtle ToM impairment. Here, we present data from a new ToM task – the Short Story Task (SST) - intended to improve upon many aspects of existing ToM measures. More specifically, the SST was designed to: (a) assess the full range of individual differences in ToM ability without suffering from ceiling effects; (b) incorporate a range of mental states of differing complexity, including epistemic states, affective states, and intentions to be inferred from a first- and second-order level; (c) use ToM stimuli representative of real-world social interactions; (d) require participants to utilize social context when making mental state inferences; (e) exhibit adequate psychometric properties; and (f) be quick and easy to administer and score. In the task, participants read a short story and were asked questions that assessed explicit mental state reasoning, spontaneous mental state inference, and comprehension of the non-mental aspects of the story. Responses were scored according to a rubric that assigned greater points for accurate mental state attributions that included multiple characters’ mental states. Results demonstrate that the SST is sensitive to variation in ToM ability, can be accurately scored by multiple raters, and exhibits concurrent validity with other social cognitive tasks. The results support the effectiveness of this new measure of ToM in the study of social cognition. The findings are also consistent with studies demonstrating significant relationships among narrative transportation, ToM, and the reading of fiction. Together, the data indicate that reading fiction may be an avenue for improving ToM ability

The neural basis of theory of mind and its relationship to social functioning and social anhedonia in individuals with schizophrenia☆

Theory of mind (ToM), the ability to attribute and reason about the mental states of others, is a strong determinant of social functioning among individuals with schizophrenia. Identifying the neural bases of ToM and their relationship to social functioning may elucidate functionally relevant neurobiological targets for intervention. ToM ability may additionally account for other social phenomena that affect social functioning, such as social anhedonia (SocAnh). Given recent research in schizophrenia demonstrating improved neural functioning in response to increased use of cognitive skills, it is possible that SocAnh, which decreases one's opportunity to engage in ToM, could compromise social functioning through its deleterious effect on ToM-related neural circuitry. Here, twenty individuals with schizophrenia and 18 healthy controls underwent fMRI while performing the False-Belief Task. Aspects of social functioning were assessed using multiple methods including self-report (Interpersonal Reactivity Index, Social Adjustment Scale), clinician-ratings (Global Functioning Social Scale), and performance-based tasks (MSCEIT—Managing Emotions). SocAnh was measured with the Revised Social Anhedonia Scale. Region-of-interest and whole-brain analyses revealed reduced recruitment of medial prefrontal cortex (MPFC) for ToM in individuals with schizophrenia. Across all participants, activity in this region correlated with most social variables. Mediation analysis revealed that neural activity for ToM in MPFC accounted for the relationship between SocAnh and social functioning. These findings demonstrate that reduced recruitment of MPFC for ToM is an important neurobiological determinant of social functioning. Furthermore, SocAhn may affect social functioning through its impact on ToM-related neural circuitry. Together, these findings suggest ToM ability as an important locus for intervention

Reading fiction and reading minds : the role of simulation in the default network

Research in psychology has suggested that reading fiction can improve individuals’ social-cognitive abilities. Findings from neuroscience show that reading and social cognition both recruit the default network, a network which is known to support our capacity to simulate hypothetical scenes, spaces and mental states. The current research tests the hypothesis that fiction reading enhances social cognition because it serves to exercise the default subnetwork involved in theory of mind. While undergoing functional neuroimaging, participants read literary passages that differed along two dimensions: (i) vivid vs abstract and (ii) social vs non-social. Analyses revealed distinct subnetworks of the default network respond to the two dimensions of interest: the medial temporal lobe subnetwork responded preferentially to vivid passages, with or without social content; the dorsomedial prefrontal cortex (dmPFC) subnetwork responded preferentially to passages with social and abstract content. Analyses also demonstrated that participants who read fiction most often also showed the strongest social cognition performance. Finally, mediation analysis showed that activity in the dmPFC subnetwork in response to the social content mediated this relation, suggesting that the simulation of social content in fiction plays a role in fiction’s ability to enhance readers’ social cognition

The Neural Basis of Social Cognition in Typically Developing Children and Its Relationship to Social Functioning

Theory of mind (ToM), the ability to think about the perspectives, beliefs, and feelings of another, develops throughout childhood and adolescence and is an important skill for social interactions. This study examines neural activity in typically developing children during a novel ToM task – the Movie Mentalizing Task– and tests its relations to ToM behavioral performance and social functioning. In this fMRI task, children ages 8–13years (N=25) watched a brief movie clip and were asked to predict a character’s mental state after a social interaction. Engaging in the Movie Mentalizing Task activated the ToM neural network. Moreover, greater neural activity in the ToM network, including the superior temporal gyrus and inferior frontal gyrus, was associated with better behavioral performance on independent ToM tasks and was related to better social functioning, though these results do not survive correction for multiple comparisons. Results offer a new affective theory of mind task for children in the scanner that robustly recruits activity in theory of mind regions

Response patterns in the developing social brain are organized by social and emotion features and disrupted in children diagnosed with autism spectrum disorder

© 2019 Elsevier Ltd Adults and children recruit a specific network of brain regions when engaged in “Theory of Mind” (ToM) reasoning. Recently, fMRI studies of adults have used multivariate analyses to provide a deeper characterization of responses in these regions. These analyses characterize representational distinctions within the social domain, rather than comparing responses across preferred (social) and non-preferred stimuli. Here, we conducted opportunistic multivariate analyses in two previously collected datasets (Experiment 1: n = 20 5–11 year old children and n = 37 adults; Experiment 2: n = 76 neurotypical and n = 29 5–12 year old children diagnosed with Autism Spectrum Disorder (ASD)) in order to characterize the structure of representations in the developing social brain, and in order to discover if this structure is disrupted in ASD. Children listened to stories that described characters' mental states (Mental), non-mentalistic social information (Social), and causal events in the environment (Physical), while undergoing fMRI. We measured the extent to which neural responses in ToM brain regions were organized according to two ToM-relevant models: 1) a condition model, which reflected the experimenter-generated condition labels, and 2) a data-driven emotion model, which organized stimuli according to their emotion content. We additionally constructed two control models based on linguistic and narrative features of the stories. In both experiments, the two ToM-relevant models outperformed the control models. The fit of the condition model increased with age in neurotypical children. Moreover, the fit of the condition model to neural response patterns was reduced in the RTPJ in children diagnosed with ASD. These results provide a first glimpse into the conceptual structure of information in ToM brain regions in childhood, and suggest that there are real, stable features that predict responses in these regions in children. Multivariate analyses are a promising approach for sensitively measuring conceptual and neural developmental change and individual differences in ToM.NSF (Award 1122374

Measuring mindreading : a review of behavioral approaches to testing cognitive and affective mental state attribution in neurologically typical adults

Mindreading refers to the ability to attribute mental states, including thoughts, intentions and emotions, to oneself and others, and is essential for navigating the social world. Empirical mindreading research has predominantly featured children, groups with autism spectrum disorder and clinical samples, and many standard tasks suffer ceiling effects with neurologically typical (NT) adults. We first outline a case for studying mindreading in NT adults and proceed to review tests of emotion perception, cognitive and affective mentalizing, and multidimensional tasks combining these facets. We focus on selected examples of core experimental paradigms including emotion recognition tests, social vignettes, narrative fiction (prose and film) and participative interaction (in real and virtual worlds), highlighting challenges for studies with NT adult cohorts. We conclude that naturalistic, multidimensional approaches may be productively applied alongside traditional tasks to facilitate a more nuanced picture of mindreading in adulthood, and to ensure construct validity whilst remaining sensitive to variation at the upper echelons of the ability

Live face-to-face interaction during fMRI: A new tool for social cognitive neuroscience

Cooperative social interaction is critical for human social development and learning. Despite the importance of social interaction, previous neuroimaging studies lack two fundamental components of everyday face-to-face interactions: contingent responding and joint attention. In the current studies, functional MRI data were collected while participants interacted with a human experimenter face-to-face via live video feed as they engaged in simple cooperative games. In Experiment 1, participants engaged in a live interaction with the experimenter (“Live”) or watched a video of the same interaction (“Recorded”). During the “Live” interaction, as compared to the Recorded conditions, greater activation was seen in brain regions involved in social cognition and reward, including the right temporoparietal junction (rTPJ), anterior cingulate cortex (ACC), right superior temporal sulcus (rSTS), ventral striatum, and amygdala. Experiment 2 isolated joint attention, a critical component of social interaction. Participants either followed the gaze of the live experimenter to a shared target of attention (“Joint Attention”) or found the target of attention alone while the experimenter was visible but not sharing attention (“Solo Attention”). The right temporoparietal junction and right posterior STS were differentially recruited during Joint, as compared to Solo, attention. These findings suggest the rpSTS and rTPJ are key regions for both social interaction and joint attention. This method of allowing online, contingent social interactions in the scanner could open up new avenues of research in social cognitive neuroscience, both in typical and atypical populations.Simons FoundationNational Institutes of Health (Postdoctoral National Research Service Award

How We Know It Hurts: Item Analysis of Written Narratives Reveals Distinct Neural Responses to Others' Physical Pain and Emotional Suffering

People are often called upon to witness, and to empathize with, the pain and suffering of others. In the current study, we directly compared neural responses to others' physical pain and emotional suffering by presenting participants (n = 41) with 96 verbal stories, each describing a protagonist's physical and/or emotional experience, ranging from neutral to extremely negative. A separate group of participants rated “how much physical pain”, and “how much emotional suffering” the protagonist experienced in each story, as well as how “vivid and movie-like” the story was. Although ratings of Pain, Suffering and Vividness were positively correlated with each other across stories, item-analyses revealed that each scale was correlated with activity in distinct brain regions. Even within regions of the “Shared Pain network” identified using a separate data set, responses to others' physical pain and emotional suffering were distinct. More broadly, item analyses with continuous predictors provided a high-powered method for identifying brain regions associated with specific aspects of complex stimuli – like verbal descriptions of physical and emotional events.United States. Air Force Office of Scientific Research (Office of Naval Research, grant number N000140910845