Theory of mind mediates the prospective relationship between abnormal social brain network morphology and chronic behavior problems after pediatric traumatic brain injury.

Childhood and adolescence coincide with rapid maturation and synaptic reorganization of distributed neural networks that underlie complex cognitive-affective behaviors. These regions, referred to collectively as the 'social brain network' (SBN) are commonly vulnerable to disruption from pediatric traumatic brain injury (TBI); however, the mechanisms that link morphological changes in the SBN to behavior problems in this population remain unclear. In 98 children and adolescents with mild to severe TBI, we acquired 3D T1-weighted MRIs at 2-8 weeks post-injury. For comparison, 33 typically developing controls of similar age, sex and education were scanned. All participants were assessed on measures of Theory of Mind (ToM) at 6 months post-injury and parents provided ratings of behavior problems at 24-months post-injury. Severe TBI was associated with volumetric reductions in the overall SBN package, as well as regional gray matter structural change in multiple component regions of the SBN. When compared with TD controls and children with milder injuries, the severe TBI group had significantly poorer ToM, which was associated with more frequent behavior problems and abnormal SBN morphology. Mediation analysis indicated that impaired theory of mind mediated the prospective relationship between abnormal SBN morphology and more frequent chronic behavior problems. Our findings suggest that sub-acute alterations in SBN morphology indirectly contribute to long-term behavior problems via their influence on ToM. Volumetric change in the SBN and its putative hub regions may represent useful imaging biomarkers for prediction of post-acute social cognitive impairment, which may in turn elevate risk for chronic behavior problems.

[1]  T. Silk,et al.  The emergence of age‐dependent social cognitive deficits after generalized insult to the developing brain: A longitudinal prospective analysis using susceptibility‐weighted imaging , 2015, Human brain mapping.

[2]  Jae-Jin Kim,et al.  Involvement of the dorsolateral prefrontal cortex and superior temporal sulcus in impaired social perception in schizophrenia , 2015, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[3]  V. Anderson,et al.  Predictors of longitudinal outcome and recovery of pragmatic language and its relation to externalizing behaviour after pediatric traumatic brain injury , 2015, Brain and Language.

[4]  V. Anderson,et al.  Prevalence and Predictors of Externalizing Behavior in Young Adult Survivors of Pediatric Traumatic Brain Injury , 2015, The Journal of head trauma rehabilitation.

[5]  T. Silk,et al.  Relationships between acute imaging biomarkers and theory of mind impairment in post-acute pediatric traumatic brain injury: A prospective analysis using susceptibility weighted imaging (SWI) , 2015, Neuropsychologia.

[6]  Kenneth H. Rubin,et al.  Executive functions and theory of mind as predictors of social adjustment in childhood traumatic brain injury. , 2014, Journal of neurotrauma.

[7]  D. Fergusson,et al.  Substance Abuse and Criminal Activities Following Traumatic Brain Injury in Childhood, Adolescence, and Early Adulthood , 2014, The Journal of head trauma rehabilitation.

[8]  D. Indig,et al.  Traumatic Brain Injury, Mental Health, Substance Use, and Offending Among Incarcerated Young People , 2014, The Journal of head trauma rehabilitation.

[9]  V. Anderson,et al.  Predictors of very-long-term sociocognitive function after pediatric traumatic brain injury: evidence for the vulnerability of the immature "social brain". , 2014, Journal of neurotrauma.

[10]  V. Anderson,et al.  Social communication mediates the relationship between emotion perception and externalizing behaviors in young adult survivors of pediatric traumatic brain injury (TBI) , 2013, International Journal of Developmental Neuroscience.

[11]  Hugues Duffau,et al.  Is the right frontal cortex really crucial in the mentalizing network? A longitudinal study in patients with a slow-growing lesion , 2013, Cortex.

[12]  J. Ponsford,et al.  Regional cortical volume and cognitive functioning following traumatic brain injury , 2013, Brain and Cognition.

[13]  Keith Owen Yeates,et al.  Cognitive, affective, and conative theory of mind (ToM) in children with traumatic brain injury , 2013, Developmental Cognitive Neuroscience.

[14]  Kenneth H. Rubin,et al.  Heterogeneity of brain lesions in pediatric traumatic brain injury. , 2013, Neuropsychology.

[15]  Ezequiel Mikulan,et al.  The anterior cingulate cortex: an integrative hub for human socially-driven interactions , 2013, Front. Neurosci..

[16]  A. Hayes Introduction to Mediation, Moderation, and Conditional Process Analysis: A Regression-Based Approach , 2013 .

[17]  S. Hearps,et al.  Social Competence at 6 Months Following Childhood Traumatic Brain Injury , 2013, Journal of the International Neuropsychological Society.

[18]  Keith Owen Yeates,et al.  Irony and Empathy in Children with Traumatic Brain Injury , 2013, Journal of the International Neuropsychological Society.

[19]  Kenneth H. Rubin,et al.  Theory of Mind in Children with Traumatic Brain Injury – CORRIGENDUM , 2013, Journal of the International Neuropsychological Society.

[20]  Jianghong Liu,et al.  The effect of pediatric traumatic brain injury on behavioral outcomes: a systematic review , 2013, Developmental medicine and child neurology.

[21]  E. Bigler Traumatic brain injury, neuroimaging, and neurodegeneration , 2012, Front. Hum. Neurosci..

[22]  Kenneth H. Rubin,et al.  Emotional Expression and Socially Modulated Emotive Communication in Children with Traumatic Brain Injury , 2012, Journal of the International Neuropsychological Society.

[23]  Daniel P. Kennedy,et al.  The social brain in psychiatric and neurological disorders , 2012, Trends in Cognitive Sciences.

[24]  Tricia L. Merkley,et al.  Neuroimaging correlates of novel psychiatric disorders after pediatric traumatic brain injury. , 2012, Journal of the American Academy of Child and Adolescent Psychiatry.

[25]  Mikko Sams,et al.  Naturalistic fMRI Mapping Reveals Superior Temporal Sulcus as the Hub for the Distributed Brain Network for Social Perception , 2012, Front. Hum. Neurosci..

[26]  T. Singer,et al.  The neural basis of empathy. , 2012, Annual review of neuroscience.

[27]  W. H. Williams,et al.  Self-Reported Traumatic Brain Injury and Postconcussion Symptoms in Incarcerated Youth , 2012, The Journal of head trauma rehabilitation.

[28]  Patrick Dupont,et al.  Graph analysis of functional brain networks for cognitive control of action in traumatic brain injury. , 2012, Brain : a journal of neurology.

[29]  H. Levin,et al.  Diffusion tensor imaging in moderate-to-severe pediatric traumatic brain injury: changes within an 18 month post-injury interval , 2012, Brain Imaging and Behavior.

[30]  D C Good,et al.  Changes in resting connectivity during recovery from severe traumatic brain injury. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[31]  H. Taylor,et al.  Emotion Labeling and Socio-Emotional Outcomes 18 Months after Early Childhood Traumatic Brain Injury , 2011, Journal of the International Neuropsychological Society.

[32]  T. McAllister,et al.  Neurobiological consequences of traumatic brain injury , 2011, Dialogues in clinical neuroscience.

[33]  H. Abdi,et al.  Longitudinal changes of structural connectivity in traumatic axonal injury , 2011, Neurology.

[34]  M. Kean,et al.  Focal thinning of the posterior corpus callosum: Normal variant or post-traumatic? , 2011, Brain injury.

[35]  Kathrin Cohen Kadosh,et al.  The social brain in adolescence: Evidence from functional magnetic resonance imaging and behavioural studies , 2011, Neuroscience & Biobehavioral Reviews.

[36]  L. Murray,et al.  Neuropathological findings in disabled survivors of a head injury. , 2011, Journal of neurotrauma.

[37]  M. Kean,et al.  Hippocampus, amygdala and global brain changes 10 years after childhood traumatic brain injury , 2011, International Journal of Developmental Neuroscience.

[38]  Harvey S. Levin,et al.  Mental State Attributions and Diffusion Tensor Imaging After Traumatic Brain Injury in Children , 2011, Developmental neuropsychology.

[39]  B. Sodian Theory of Mind in Infancy , 2011 .

[40]  Jeffrey S. Spence,et al.  Assessing spatial relationships between axonal integrity, regional brain volumes, and neuropsychological outcomes after traumatic axonal injury. , 2010, Journal of neurotrauma.

[41]  Jason R. Tregellas,et al.  The role of the insula in schizophrenia , 2010, Schizophrenia Research.

[42]  Erin D. Bigler,et al.  Longitudinal Changes in the Corpus Callosum following Pediatric Traumatic Brain Injury , 2010, Developmental Neuroscience.

[43]  H. Taylor,et al.  Theory of mind skills 1 year after traumatic brain injury in 6- to 8-year-old children. , 2010, Journal of neuropsychology.

[44]  J. Tonks,et al.  Traumatic brain injury in a prison population: Prevalence and risk for re-offending , 2010, Brain injury.

[45]  Xiaoqi Li,et al.  Diffuse damage in pediatric traumatic brain injury: A comparison of automated versus operator-controlled quantification methods , 2010, NeuroImage.

[46]  D. McArthur,et al.  Early Nonischemic Oxidative Metabolic Dysfunction Leads to Chronic Brain Atrophy in Traumatic Brain Injury , 2010, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[47]  Iroise Dumontheil,et al.  Online usage of theory of mind continues to develop in late adolescence. , 2010, Developmental science.

[48]  Maya Troyanskaya,et al.  Evaluating the relationship between memory functioning and cingulum bundles in acute mild traumatic brain injury using diffusion tensor imaging. , 2010, Journal of neurotrauma.

[49]  A. Hayes Beyond Baron and Kenny: Statistical Mediation Analysis in the New Millennium , 2009 .

[50]  Lucina Q. Uddin,et al.  The anterior insula in autism: Under-connected and under-examined , 2009, Neuroscience & Biobehavioral Reviews.

[51]  H. Critchley,et al.  A common role of insula in feelings, empathy and uncertainty , 2009, Trends in Cognitive Sciences.

[52]  Adrian Beavis,et al.  The AUSEI06 , 2009 .

[53]  Erin D Bigler,et al.  Diffuse changes in cortical thickness in pediatric moderate-to-severe traumatic brain injury. , 2008, Journal of neurotrauma.

[54]  Erin D. Bigler,et al.  Morphometric MRI Findings in the Thalamus and Brainstem in Children After Moderate to Severe Traumatic Brain Injury , 2008, Journal of child neurology.

[55]  S. Blakemore The social brain in adolescence , 2008, Nature Reviews Neuroscience.

[56]  R. Grace,et al.  Prevalence of traumatic brain injury among children, adolescents and young adults: Prospective evidence from a birth cohort , 2008, Brain injury.

[57]  D. Sperber,et al.  PSYCHOLOGICAL SCIENCE Research Article Attribution of Beliefs by 13-Month-Old Infants , 2022 .

[58]  H S Levin,et al.  cerebellar atrophy after moderate-to-severe pediatric traumatic brain injury. , 2007, AJNR. American journal of neuroradiology.

[59]  Sarah-Jayne Blakemore,et al.  Social cognitive development during adolescence. , 2006, Social cognitive and affective neuroscience.

[60]  Erin D Bigler,et al.  Diffusion tensor imaging in the corpus callosum in children after moderate to severe traumatic brain injury. , 2006, Journal of neurotrauma.

[61]  Nathalie Boddaert,et al.  Autism, the superior temporal sulcus and social perception , 2006, Trends in Neurosciences.

[62]  C. Frith,et al.  The Neural Basis of Mentalizing , 2006, Neuron.

[63]  Anders M. Dale,et al.  Reliability in multi-site structural MRI studies: Effects of gradient non-linearity correction on phantom and human data , 2006, NeuroImage.

[64]  Mark H Johnson,et al.  The emergence of the social brain network: Evidence from typical and atypical development , 2005, Development and Psychopathology.

[65]  Claudia Pedroza,et al.  Frontal and temporal morphometric findings on MRI in children after moderate to severe traumatic brain injury. , 2005, Journal of neurotrauma.

[66]  Henrik Walter,et al.  Understanding Intentions in Social Interaction: The Role of the Anterior Paracingulate Cortex , 2004, Journal of Cognitive Neuroscience.

[67]  Richard S. Frackowiak,et al.  Superior temporal sulcus anatomical abnormalities in childhood autism: a voxel-based morphometry MRI study , 2004, NeuroImage.

[68]  D. Drotar,et al.  Short- and long-term social outcomes following pediatric traumatic brain injury , 2004, Journal of the International Neuropsychological Society.

[69]  Istvan Molnar-Szakacs,et al.  Watching social interactions produces dorsomedial prefrontal and medial parietal BOLD fMRI signal increases compared to a resting baseline , 2004, NeuroImage.

[70]  Richard E Thompson,et al.  Neuroimaging correlates of anxiety after pediatric traumatic brain injury , 2004, Biological Psychiatry.

[71]  J. Veijola,et al.  The association of preceding traumatic brain injury with mental disorders, alcoholism and criminality: the Northern Finland 1966 Birth Cohort Study , 2002, Psychiatry Research.

[72]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

[73]  H. Wellman,et al.  Meta-analysis of theory-of-mind development: the truth about false belief. , 2001, Child development.

[74]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[75]  B. Jennett,et al.  Assessment of coma and impaired consciousness. A practical scale. , 1974, Lancet.

[76]  S. Swinnen,et al.  Altered structural networks and executive deficits in traumatic brain injury patients , 2012, Brain Structure and Function.

[77]  V. Anderson,et al.  SOCIAL: an integrative framework for the development of social skills. , 2010, Psychological bulletin.

[78]  R. Adolphs,et al.  The social brain: neural basis of social knowledge. , 2009, Annual review of psychology.

[79]  D. Kenny,et al.  Relationship between Head Injury and Violent Offending in Juvenile Detainees, The , 2007 .

[80]  Nikos Makris,et al.  Automatically parcellating the human cerebral cortex. , 2004, Cerebral cortex.

[81]  E. Bigler,et al.  MR-based brain and cerebrospinal fluid measurement after traumatic brain injury: correlation with neuropsychological outcome. , 1997, AJNR. American journal of neuroradiology.

[82]  D. A. Kenny,et al.  The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. , 1986, Journal of personality and social psychology.