Characterization of the Temporal Stability of ToM and Pain Functional Brain Networks Carry Distinct Developmental Signatures during Naturalistic Viewing

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Abstract A temporally stable functional brain network pattern among coordinated brain regions is fundamental to stimulus selectivity and functional specificity during the critical period of brain development. Brain networks that are recruited in time to process internal states of others’ bodies (like hunger and pain) versus internal mental states (like beliefs, desires, and emotions) of others’ minds allow us to ask whether a quantitative characterization of the stability of these networks carry meaning during early development and constrain cognition in a specific way. Previous research provides critical insight into the early development of the ToM network and its segregation from the Pain network throughout normal development using functional connectivity. However, a quantitative characterization of the temporal stability of ToM networks from early childhood to adulthood remains unexplored. In this work, using a large sample of children (n=122, 3–12 years) and adults (n=33), we addressed this question based on their fMRI data during a short and engaging naturalistic movie-watching task. The movie highlights the characters’ bodily sensations (often pain) and mental states (beliefs, desires, emotions), and is a feasible experiment for young children. Our results tracked the change in temporal stability using an unsupervised characterization of ToM and Pain networks dFC patterns using Angular and Mahalanobis distance between dominant dynamic functional connectivity subspaces. Our findings reveal that both ToM and Pain networks exhibit lower temporal stability as early as 3 years and gradually stabilize by 5 years, which continues till adolescence and late adulthood (often sharing similarity with adult dFC stability patterns). Further, we find that the temporal stability of ToM brain networks is predictive of participants’ task performance in the false-belief task to access mentalization at an early age. Interestingly, higher temporal stability is predictive of the pass group, and similarly, moderate and low temporal stability are predictive of the inconsistent group and the fail group. Our findings open an avenue for applying the temporal stability of dFC subspaces of large-scale functional brain networks during cortical development to act as a biomarker for multiple developmental disorders concerning impairment and discontinuity in the neural basis of social cognition.
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Characterization of the Temporal Stability of ToM and Pain Functional Brain Networks Carry Distinct Developmental Signatures during Naturalistic Viewing | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article Characterization of the Temporal Stability of ToM and Pain Functional Brain Networks Carry Distinct Developmental Signatures during Naturalistic Viewing Km Bhavna, Niniva Ghosh, Romi Banerjee, Dipanjan Roy This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3859295/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 28 Sep, 2024 Read the published version in Scientific Reports → Version 1 posted 11 You are reading this latest preprint version Abstract A temporally stable functional brain network pattern among coordinated brain regions is fundamental to stimulus selectivity and functional specificity during the critical period of brain development. Brain networks that are recruited in time to process internal states of others’ bodies (like hunger and pain) versus internal mental states (like beliefs, desires, and emotions) of others’ minds allow us to ask whether a quantitative characterization of the stability of these networks carry meaning during early development and constrain cognition in a specific way. Previous research provides critical insight into the early development of the ToM network and its segregation from the Pain network throughout normal development using functional connectivity. However, a quantitative characterization of the temporal stability of ToM networks from early childhood to adulthood remains unexplored. In this work, using a large sample of children (n=122, 3–12 years) and adults (n=33), we addressed this question based on their fMRI data during a short and engaging naturalistic movie-watching task. The movie highlights the characters’ bodily sensations (often pain) and mental states (beliefs, desires, emotions), and is a feasible experiment for young children. Our results tracked the change in temporal stability using an unsupervised characterization of ToM and Pain networks dFC patterns using Angular and Mahalanobis distance between dominant dynamic functional connectivity subspaces. Our findings reveal that both ToM and Pain networks exhibit lower temporal stability as early as 3 years and gradually stabilize by 5 years, which continues till adolescence and late adulthood (often sharing similarity with adult dFC stability patterns). Further, we find that the temporal stability of ToM brain networks is predictive of participants’ task performance in the false-belief task to access mentalization at an early age. Interestingly, higher temporal stability is predictive of the pass group, and similarly, moderate and low temporal stability are predictive of the inconsistent group and the fail group. Our findings open an avenue for applying the temporal stability of dFC subspaces of large-scale functional brain networks during cortical development to act as a biomarker for multiple developmental disorders concerning impairment and discontinuity in the neural basis of social cognition. Biological sciences/Neuroscience/Cognitive neuroscience Biological sciences/Neuroscience/Computational neuroscience Biological sciences/Neuroscience/Sensory processing Biological sciences/Neuroscience/Social behaviour Biological sciences/Neuroscience/Social neuroscience Theory of Mind (ToM) Pain networks Angular distance Mahalanobis distance Dynamic functional connectivity (dFC). Full Text Additional Declarations No competing interests reported. Supplementary Files SupplementaryMaterialupdated9JAN2024.pdf Cite Share Download PDF Status: Published Journal Publication published 28 Sep, 2024 Read the published version in Scientific Reports → Version 1 posted Editorial decision: Revision requested 16 May, 2024 Reviews received at journal 15 May, 2024 Reviewers agreed at journal 27 Apr, 2024 Reviews received at journal 25 Feb, 2024 Reviewers agreed at journal 18 Jan, 2024 Reviewers agreed at journal 18 Jan, 2024 Reviewers invited by journal 16 Jan, 2024 Editor assigned by journal 16 Jan, 2024 Editor invited by journal 14 Jan, 2024 Submission checks completed at journal 14 Jan, 2024 First submitted to journal 13 Jan, 2024 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. 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