Brain decoding of spontaneous thought: Predictive modeling of self-relevance and valence using personal narratives.

The contents and dynamics of spontaneous thought are important factors for personality traits and mental health. However, assessing spontaneous thoughts is challenging due to their unconstrained nature, and directing participants' attention to report their thoughts may fundamentally alter them. Here, we aimed to decode two key content dimensions of spontaneous thought-self-relevance and valence-directly from brain activity. To train functional MRI-based predictive models, we used individually generated personal stories as stimuli in a story-reading task to mimic narrative-like spontaneous thoughts (n = 49). We then tested these models on multiple test datasets (total n = 199). The default mode, ventral attention, and frontoparietal networks played key roles in the predictions, with the anterior insula and midcingulate cortex contributing to self-relevance prediction and the left temporoparietal junction and dorsomedial prefrontal cortex contributing to valence prediction. Overall, this study presents brain models of internal thoughts and emotions, highlighting the potential for the brain decoding of spontaneous thought.

Brain Functional Connectivity and Anatomical Features as Predictors of Cognitive Behavioral Therapy Outcome for Anxiety in Youths.

Background: Because pediatric anxiety disorders precede the onset of many other problems, successful prediction of response to the first-line treatment, cognitive-behavioral therapy (CBT), could have major impact. However, existing clinical models are weakly predictive. The current study evaluates whether structural and resting-state functional magnetic resonance imaging can predict post-CBT anxiety symptoms. Methods: Two datasets were studied: (A) one consisted of n=54 subjects with an anxiety diagnosis, who received 12 weeks of CBT, and (B) one consisted of n=15 subjects treated for 8 weeks. Connectome Predictive Modeling (CPM) was used to predict treatment response, as assessed with the PARS; additionally we investigated models using anatomical features, instead of functional connectivity. The main analysis included network edges positively correlated with treatment outcome, and age, sex, and baseline anxiety severity as predictors. Results from alternative models and analyses also are presented. Model assessments utilized 1000 bootstraps, resulting in a 95% CI for R2, r and mean absolute error (MAE). Outcomes: The main model showed a mean absolute error of approximately 3.5 (95%CI: [3.1-3.8]) points a R2 of 0.08 [-0.14 - 0.26] and r of 0.38 [0.24 - 0.511]. When testing this model in the left-out sample (B) the results were similar, with a MAE of 3.4 [2.8 - 4.7], R2-0.65 [-2.29 - 0.16] and r of 0.4 [0.24 - 0.54]. The anatomical metrics showed a similar pattern, where models rendered overall low R2. Interpretation: The analysis showed that models based on earlier promising results failed to predict clinical outcomes. Despite the small sample size, the current study does not support extensive use of CPM to predict outcome in pediatric anxiety.

Individuals who see the good in the bad engage distinctive default network coordination during post-encoding rest.

Focusing on the upside of negative events often promotes resilience. Yet, the underlying mechanisms that allow some people to spontaneously see the good in the bad remain unclear. The broaden-and-build theory of positive emotion has long suggested that positive affect, including positivity in the face of negative events, is linked to idiosyncratic thought patterns (i.e., atypical cognitive responses). Yet, evidence in support of this view has been limited, in part, due to difficulty in measuring idiosyncratic cognitive processes as they unfold. To overcome this barrier, we applied Inter-Subject Representational Similarity Analysis to test whether and how idiosyncratic neural responding supports positive reactions to negative experience. We found that idiosyncratic functional connectivity patterns in the brain's default network while resting after a negative experience predicts more positive descriptions of the event. This effect persisted when controlling for connectivity 1) before and during the negative experience, 2) before, during, and after a neutral experience, and 3) between other relevant brain regions (i.e., the limbic system). The relationship between idiosyncratic default network responding and positive affect was largely driven by functional connectivity patterns between the ventromedial prefrontal cortex and the rest of the default network and occurred relatively quickly during rest. We identified post-encoding rest as a key moment and the default network as a key brain system in which idiosyncratic responses correspond with seeing the good in the bad.

Will you read how I will read? Naturalistic fMRI predictors of emergent reading.

Despite reading being an essential and almost universal skill in the developed world, reading proficiency varies substantially from person to person. To study why, the fMRI field is beginning to turn from single-word or nonword reading tasks to naturalistic stimuli like connected text and listening to stories. To study reading development in children just beginning to read, listening to stories is an appropriate paradigm because speech perception and phonological processing are important for, and are predictors of, reading proficiency. Our study examined the relationship between behavioral reading-related skills and the neural response to listening to stories in the fMRI environment. Functional MRI were gathered in a 3T TIM-Trio scanner. During the fMRI scan, children aged approximately 7 years listened to professionally narrated common short stories and answered comprehension questions following the narration. Analyses of the data used inter-subject correlation (ISC), and representational similarity analysis (RSA). Our primary finding is that ISC reveals areas of increased synchrony in both high- and low-performing emergent readers previously implicated in reading ability/disability. Of particular interest are that several previously identified brain regions (medial temporal gyrus (MTG), inferior frontal gyrus (IFG), inferior temporal gyrus (ITG)) were found to "synchronize" across higher reading ability participants, while lower reading ability participants had idiosyncratic activation patterns in these regions. Additionally, two regions (superior frontal gyrus (SFG) and another portion of ITG) were recruited by all participants, but their specific timecourse of activation depended on reading performance. These analyses support the idea that different brain regions involved in reading follow different developmental trajectories that correlate with reading proficiency on a spectrum rather than the usual dichotomy of poor readers versus strong readers.

Functional neuroimaging as a catalyst for integrated neuroscience.

Functional magnetic resonance imaging (fMRI) enables non-invasive access to the awake, behaving human brain. By tracking whole-brain signals across a diverse range of cognitive and behavioural states or mapping differences associated with specific traits or clinical conditions, fMRI has advanced our understanding of brain function and its links to both normal and atypical behaviour. Despite this headway, progress in human cognitive neuroscience that uses fMRI has been relatively isolated from rapid advances in other subdomains of neuroscience, which themselves are also somewhat siloed from one another. In this Perspective, we argue that fMRI is well-placed to integrate the diverse subfields of systems, cognitive, computational and clinical neuroscience. We first summarize the strengths and weaknesses of fMRI as an imaging tool, then highlight examples of studies that have successfully used fMRI in each subdomain of neuroscience. We then provide a roadmap for the future advances that will be needed to realize this integrative vision. In this way, we hope to demonstrate how fMRI can help usher in a new era of interdisciplinary coherence in neuroscience.

Inter-subject correlation during long narratives reveals widespread neural correlates of reading ability.

Recent work using fMRI inter-subject correlation analysis has provided new information about the brain's response to video and audio narratives, particularly in frontal regions not typically activated by single words. This approach is very well suited to the study of reading, where narrative is central to natural experience. But since past reading paradigms have primarily presented single words or phrases, the influence of narrative on semantic processing in the brain - and how that influence might change with reading ability - remains largely unexplored. In this study, we presented coherent stories to adolescents and young adults with a wide range of reading abilities. The stories were presented in alternating visual and auditory blocks. We used a dimensional inter-subject correlation analysis to identify regions in which better and worse readers had varying levels of consistency with other readers. This analysis identified a widespread set of brain regions in which activity timecourses were more similar among better readers than among worse readers. These differences were not detected with standard block activation analyses. Worse readers had higher correlation with better readers than with other worse readers, suggesting that the worse readers had "idiosyncratic" responses rather than using a single compensatory mechanism. Close inspection confirmed that these differences were not explained by differences in IQ or motion. These results suggest an expansion of the current view of where and how reading ability is reflected in the brain, and in doing so, they establish inter-subject correlation as a sensitive tool for future studies of reading disorders.

The default network dominates neural responses to evolving movie stories.

Neuroscientific studies exploring real-world dynamic perception often overlook the influence of continuous changes in narrative content. In our research, we utilize machine learning tools for natural language processing to examine the relationship between movie narratives and neural responses. By analyzing over 50,000 brain images of participants watching Forrest Gump from the studyforrest dataset, we find distinct brain states that capture unique semantic aspects of the unfolding story. The default network, associated with semantic information integration, is the most engaged during movie watching. Furthermore, we identify two mechanisms that underlie how the default network liaises with the amygdala and hippocampus. Our findings demonstrate effective approaches to understanding neural processes in everyday situations and their relation to conscious awareness.

Negative affect homogenizes and positive affect diversifies social memory consolidation across people.

We are often surprised when an interaction we remember positively is recalled by a peer negatively. What colors social memories with positive versus negative hues? We show that when resting after a social experience, individuals showing similar default network responding subsequently remember more negative information, while individuals showing idiosyncratic default network responding remember more positive information. Results were specific to rest after the social experience (as opposed to before or during the social experience, or rest after a nonsocial experience). The results provide novel neural evidence in support of the "broaden and build" theory of positive emotion, which posits that while negative affect confines, positive affect broadens idiosyncrasy in cognitive processing. For the first time, we identified post-encoding rest as a key moment and the default network as a key brain system in which negative affect homogenizes, whereas positive affect diversifies social memories.

Individual differences in neural event segmentation of continuous experiences.

Event segmentation is a spontaneous part of perception, important for processing continuous information and organizing it into memory. Although neural and behavioral event segmentation show a degree of inter-subject consistency, meaningful individual variability exists atop these shared patterns. Here we characterized individual differences in the location of neural event boundaries across four short movies that evoked variable interpretations. Event boundary alignment across subjects followed a posterior-to-anterior gradient that was tightly correlated with the rate of segmentation: slower-segmenting regions that integrate information over longer time periods showed more individual variability in boundary locations. This relationship held irrespective of the stimulus, but the degree to which boundaries in particular regions were shared versus idiosyncratic depended on certain aspects of movie content. Furthermore, this variability was behaviorally significant in that similarity of neural boundary locations during movie-watching predicted similarity in how the movie was ultimately remembered and appraised. In particular, we identified a subset of regions in which neural boundary locations are both aligned with behavioral boundaries during encoding and predictive of stimulus interpretation, suggesting that event segmentation may be a mechanism by which narratives generate variable memories and appraisals of stimuli.

Neural unscrambling of temporal information during a nonlinear narrative.

Although we must experience our lives chronologically, storytellers often manipulate the order in which they relay events. How the brain processes temporal information while encoding a nonlinear narrative remains unclear. Here, we use functional magnetic resonance imaging during movie watching to investigate which brain regions are sensitive to information about time in a narrative and test whether the representation of temporal context across a narrative is more influenced by the order in which events are presented or their underlying chronological sequence. Results indicate that medial parietal regions are sensitive to cued jumps through time over and above other changes in context (i.e., location). Moreover, when processing non-chronological narrative information, the precuneus and posterior cingulate engage in on-the-fly temporal unscrambling to represent information chronologically. Specifically, days that are closer together in chronological time are represented more similarly regardless of when they are presented in the movie, and this representation is consistent across participants. Additional analyses reveal a strong spatial signature associated with higher magnitude jumps through time. These findings are consistent with prior theorizing on medial parietal regions as central to maintaining and updating narrative situation models, and suggest the priority of chronological information when encoding narrative events.

Seeing Social: A Neural Signature for Conscious Perception of Social Interactions.

Social information is some of the most ambiguous content we encounter in our daily lives, yet in experimental contexts, percepts of social interactions-that is, whether an interaction is present and if so, the nature of that interaction-are often dichotomized as correct or incorrect based on experimenter-assigned labels. Here, we investigated the behavioral and neural correlates of subjective (or conscious) social perception using data from the Human Connectome Project in which participants (n = 1049; 486 men, 562 women) viewed animations of geometric shapes during fMRI and indicated whether they perceived a social interaction or random motion. Critically, rather than experimenter-assigned labels, we used observers' own reports of "Social" or "Non-social" to classify percepts and characterize brain activity, including leveraging a particularly ambiguous animation perceived as "Social" by some but "Non-social" by others to control for visual input. Behaviorally, observers were biased toward perceiving information as social (vs non-social); and neurally, observer reports (compared with experimenter labels) explained more variance in activity across much of the brain. Using "Unsure" reports, we identified several regions that responded parametrically to perceived socialness. Neural responses to social versus non-social content diverged early in time and in the cortical hierarchy. Finally, individuals with higher internalizing trait scores showed both a higher response bias toward "Social" and an inverse relationship with activity in default mode and visual association areas while scanning for social information. Findings underscore the subjective nature of social perception and the importance of using observer reports to study percepts of social interactions.SIGNIFICANCE STATEMENT Simple animations involving two or more geometric shapes have been used as a gold standard to understand social cognition and impairments therein. Yet, experimenter-assigned labels of what is social versus non-social are frequently used as a ground truth, despite the fact that percepts of such ambiguous social stimuli are highly subjective. Here, we used behavioral and fMRI data from a large sample of neurotypical individuals to show that participants' responses reveal subtle behavioral biases, help us study neural responses to social content more precisely, and covary with internalizing trait scores. Our findings underscore the subjective nature of social perception and the importance of considering observer reports in studying behavioral and neural dynamics of social perception.

Leveraging the power of media to drive cognition: a media-informed approach to naturalistic neuroscience.

So-called 'naturalistic' stimuli have risen in popularity in cognitive, social and affective neuroscience over the last 15 years. However, a critical property of these stimuli is frequently overlooked: Media-like film, television, books and podcasts-are 'fundamentally not natural'. They are deliberately crafted products meant to elicit particular human thought, emotion and behavior. Here, we argue for a more informed approach to adopting media stimuli in experimental paradigms. We discuss the pitfalls of combining stimuli that are designed for research with those that are designed for other purposes (e.g. entertainment) under the umbrella term of 'naturalistic' and present strategies to improve rigor in the stimulus selection process. We assert that experiencing media should be considered a task akin to any other experimental task(s) and explain how this shift in perspective will compel more nuanced and generalizable research using these stimuli. Throughout, we offer theoretical and practical knowledge from multidisciplinary media research to raise the standard for the treatment of media stimuli in neuroscience research.

In-degree centrality in a social network is linked to coordinated neural activity.

Convergent processing of the world may be a factor that contributes to social connectedness. We use neuroimaging and network analysis to investigate the association between the social-network position (as measured by in-degree centrality) of first-year university students and their neural similarity while watching naturalistic audio-visual stimuli (specifically, videos). There were 119 students in the social-network study; 63 of them participated in the neuroimaging study. We show that more central individuals had similar neural responses to their peers and to each other in brain regions that are associated with high-level interpretations and social cognition (e.g., in the default mode network), whereas less-central individuals exhibited more variable responses. Self-reported enjoyment of and interest in stimuli followed a similar pattern, but accounting for these data did not change our main results. These findings show that neural processing of external stimuli is similar in highly-central individuals but is idiosyncratic in less-central individuals.

The positive-negative mode link between brain connectivity, demographics and behaviour: a pre-registered replication of Smith et al. (2015).

In mental health research, it has proven difficult to find measures of brain function that provide reliable indicators of mental health and well-being, including susceptibility to mental health disorders. Recently, a family of data-driven analyses have provided such reliable measures when applied to large, population-level datasets. In the current pre-registered replication study, we show that the canonical correlation analysis (CCA) methods previously developed using resting-state magnetic resonance imaging functional connectivity and subject measures (SMs) of cognition and behaviour from healthy adults are also effective in measuring well-being (a 'positive-negative axis') in an independent developmental dataset. Our replication was successful in two out of three of our pre-registered criteria, such that a primary CCA mode's weights displayed a significant positive relationship and explained a significant amount of variance in both functional connectivity and SMs. The only criterion that was not successful was that compared to other modes the magnitude of variance explained by the primary CCA mode was smaller than predicted, a result that could indicate a developmental trajectory of a primary mode. This replication establishes a signature neurotypical relationship between connectivity and phenotype, opening new avenues of research in neuroscience with clear clinical applications.

Is it time to put rest to rest?

The so-called resting state, in which participants lie quietly with no particular inputs or outputs, represented a paradigm shift from conventional task-based studies in human neuroimaging. Our foray into rest was fruitful from both a scientific and methodological perspective, but at this point, how much more can we learn from rest on its own? While rest still dominates in many subfields, data from tasks have empirically demonstrated benefits, as well as the potential to provide insights about the mind in addition to the brain. I argue that we can accelerate progress in human neuroscience by de-emphasizing rest in favor of more grounded experiments, including promising integrated designs that respect the prominence of self-generated activity while offering enhanced control and interpretability.

Neural signatures of attentional engagement during narratives and its consequences for event memory.

As we comprehend narratives, our attentional engagement fluctuates over time. Despite theoretical conceptions of narrative engagement as emotion-laden attention, little empirical work has characterized the cognitive and neural processes that comprise subjective engagement in naturalistic contexts or its consequences for memory. Here, we relate fluctuations in narrative engagement to patterns of brain coactivation and test whether neural signatures of engagement predict subsequent memory. In behavioral studies, participants continuously rated how engaged they were as they watched a television episode or listened to a story. Self-reported engagement was synchronized across individuals and driven by the emotional content of the narratives. In functional MRI datasets collected as different individuals watched the same show or listened to the same story, engagement drove neural synchrony, such that default mode network activity was more synchronized across individuals during more engaging moments of the narratives. Furthermore, models based on time-varying functional brain connectivity predicted evolving states of engagement across participants and independent datasets. The functional connections that predicted engagement overlapped with a validated neuromarker of sustained attention and predicted recall of narrative events. Together, our findings characterize the neural signatures of attentional engagement in naturalistic contexts and elucidate relationships among narrative engagement, sustained attention, and event memory.