Neuroimaging of the Injured Pediatric Brain: Methods and New Lessons

Traumatic brain injury (TBI) is a significant public health problem in the United States, especially for children and adolescents. Current epidemiological data estimate over 600,000 patients younger than 20 years are treated for TBI in emergency rooms annually. While many patients experience a full recovery, for others there can be long-lasting cognitive, neurological, psychological, and behavioral disruptions. TBI in youth can disrupt ongoing brain development and create added family stress during a formative period. The neuroimaging methods used to assess brain injury improve each year, providing researchers a more detailed characterization of the injury and recovery process. In this review, we cover current imaging methods used to quantify brain disruption post-injury, including structural magnetic resonance imaging (MRI), diffusion MRI, functional MRI, resting state fMRI, and magnetic resonance spectroscopy (MRS), with brief coverage of other methods, including electroencephalography (EEG), single-photon emission computed tomography (SPECT), and positron emission tomography (PET). We include studies focusing on pediatric moderate-severe TBI from 2 months post-injury and beyond. While the morbidity of pediatric TBI is considerable, continuing advances in imaging methods have the potential to identify new treatment targets that can lead to significant improvements in outcome.

[1]  P. Expert,et al.  Traumatic brain injury impairs small-world topology , 2013, Neurology.

[2]  Hiroshi Otsubo,et al.  Fluctuations in cortical synchronization in pediatric traumatic brain injury. , 2008, Journal of neurotrauma.

[3]  Toru Nakamura,et al.  Resting Network Plasticity Following Brain Injury , 2009, PloS one.

[4]  J. Rosenfeld,et al.  Intellectual Outcome from Preschool Traumatic Brain Injury: A 5-Year Prospective, Longitudinal Study , 2009, Pediatrics.

[5]  Scott K Holland,et al.  Neural substrate differences in language networks and associated language-related behavioral impairments in children with TBI: a preliminary fMRI investigation. , 2007, NeuroRehabilitation.

[6]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[7]  J. Rosenfeld,et al.  Children's attentional skills 5 years post-TBI. , 2006, Journal of pediatric psychology.

[8]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[9]  K. Yeates,et al.  Arithmetic skills and their cognitive correlates in children with acquired and congenital brain disorder , 2005, Journal of the International Neuropsychological Society.

[10]  M. Hulkower,et al.  A Decade of DTI in Traumatic Brain Injury: 10 Years and 100 Articles Later , 2013, American Journal of Neuroradiology.

[11]  S. Swinnen,et al.  Brain‐behavior relationships in young traumatic brain injury patients: DTI metrics are highly correlated with postural control , 2009, Human brain mapping.

[12]  Paul M. Thompson,et al.  White matter disruption in moderate/severe pediatric traumatic brain injury: Advanced tract-based analyses , 2015, NeuroImage: Clinical.

[13]  M. Waugh,et al.  An Investigation of Neuronal Integrity in Severe Paediatric Traumatic Brain Injury , 2004, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[14]  Mark D'Esposito,et al.  Focal Brain Lesions to Critical Locations Cause Widespread Disruption of the Modular Organization of the Brain , 2012, Journal of Cognitive Neuroscience.

[15]  S. Ashwal,et al.  Proton Spectroscopy Detected Myoinositol in Children with Traumatic Brain Injury , 2004, Pediatric Research.

[16]  Mary R. Newsome,et al.  Working Memory Brain Activation Following Severe Traumatic Brain Injury , 2007, Cortex.

[17]  K. Nordengen,et al.  Localisation of N-acetylaspartate in oligodendrocytes/myelin , 2015, Brain Structure and Function.

[18]  R. Asarnow,et al.  Pivotal Role of Anterior Cingulate Cortex in Working Memory after Traumatic Brain Injury in Youth , 2010, Front. Neur..

[19]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[20]  Larry A Kramer,et al.  Predicting Behavioral Deficits in Pediatric Traumatic Brain Injury Through Uncinate Fasciculus Integrity , 2011, Journal of the International Neuropsychological Society.

[21]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[22]  Joseph A. Kufera,et al.  Frontal lobe changes after severe diffuse closed head injury in children: a volumetric study of magnetic resonance imaging. , 1995, Neurosurgery.

[23]  S. Rose,et al.  Endocrine changes after pediatric traumatic brain injury , 2012, Pituitary.

[24]  V. Anderson,et al.  Quality of life in children and adolescents post-TBI: a systematic review and meta-analysis. , 2012, Journal of neurotrauma.

[25]  V. Anderson,et al.  Memory outcome at 5 years post-childhood traumatic brain injury , 2007, Brain injury.

[26]  Stephen Ashwal,et al.  Use of Advanced Neuroimaging Techniques in the Evaluation of Pediatric Traumatic Brain Injury , 2006, Developmental Neuroscience.

[27]  Stephen Ashwal,et al.  Susceptibility-weighted imaging and proton magnetic resonance spectroscopy in assessment of outcome after pediatric traumatic brain injury. , 2006, Archives of physical medicine and rehabilitation.

[28]  Christopher Babbitt,et al.  Diverging white matter trajectories in children after traumatic brain injury , 2017, Neurology.

[29]  Harvey S. Levin,et al.  Diffusion Tensor Imaging in Relation to Cognitive and Functional Outcome of Traumatic Brain Injury in Children , 2008, The Journal of head trauma rehabilitation.

[30]  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.

[31]  S. Ashwal,et al.  Application of Advanced Neuroimaging Modalities in Pediatric Traumatic Brain Injury , 2014, Journal of child neurology.

[32]  M. Ernst,et al.  The Role of Functional Neuroimaging in Pediatric Brain Injury , 2006, Pediatrics.

[33]  Bryon A Mueller,et al.  Neurocognitive and neuroimaging correlates of pediatric traumatic brain injury: a diffusion tensor imaging (DTI) study. , 2007, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[34]  Mary R. Newsome,et al.  Brain imaging correlates of verbal working memory in children following traumatic brain injury. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[35]  S. Ashwal,et al.  Predictive value of proton magnetic resonance spectroscopy in pediatric closed head injury. , 2000, Pediatric neurology.

[36]  V. Anderson,et al.  Educational, Vocational, Psychosocial, and Quality‐of‐Life Outcomes for Adult Survivors of Childhood Traumatic Brain Injury , 2009, The Journal of head trauma rehabilitation.

[37]  Linda Ewing-Cobbs,et al.  Longitudinal diffusion tensor imaging after pediatric traumatic brain injury: Impact of age at injury and time since injury on pathway integrity , 2016, Human brain mapping.

[38]  M. Verfaellie,et al.  Traumatic Brain Injury as a Disorder of Brain Connectivity , 2016, Journal of the International Neuropsychological Society.

[39]  D. Hovda,et al.  The molecular pathophysiology of concussive brain injury. , 2011, Clinics in sports medicine.

[40]  D B Hinshaw,et al.  Proton MR spectroscopy after acute central nervous system injury: outcome prediction in neonates, infants, and children. , 1997, Radiology.

[41]  A. Blamire,et al.  Magnetic Resonance Spectroscopy for Traumatic Brain Injury , 2015, Topics in magnetic resonance imaging : TMRI.

[42]  S. Ashwal,et al.  Proton MR spectroscopic imaging depicts diffuse axonal injury in children with traumatic brain injury. , 2005, AJNR. American journal of neuroradiology.

[43]  D. Robin,et al.  Personality change disorder in children and adolescents following traumatic brain injury , 2000, Journal of the International Neuropsychological Society.

[44]  Daniel Rueckert,et al.  Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data , 2006, NeuroImage.

[45]  Amanda Wood,et al.  Do children really recover better? Neurobehavioural plasticity after early brain insult. , 2011, Brain : a journal of neurology.

[46]  William B. Gallentine Utility of Continuous EEG in Children With Acute Traumatic Brain Injury , 2013, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[47]  F. Babl,et al.  Timing of traumatic brain injury in childhood and intellectual outcome. , 2012, Journal of pediatric psychology.

[48]  Christopher Babbitt,et al.  The UCLA study of Predictors of Cognitive Functioning Following Moderate/Severe Pediatric Traumatic Brain Injury , 2016, Journal of the International Neuropsychological Society.

[49]  Erin D. Bigler,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.

[50]  B. Sahakian,et al.  Head Circumference and Brain and Hippocampal Volume after Severe Traumatic Brain Injury in Childhood , 2005, Pediatric Research.

[51]  L. G. Cook,et al.  A SPECT study of language and brain reorganization three years after pediatric brain injury. , 2006, Progress in brain research.

[52]  S. Holland,et al.  Neural Correlates of Interference Control in Adolescents with Traumatic Brain Injury: Functional Magnetic Resonance Imaging Study of the Counting Stroop Task , 2010, Journal of the International Neuropsychological Society.

[53]  L. Kramer,et al.  Executive Functions Following Traumatic Brain Injury in Young Children: A Preliminary Analysis , 2004, Developmental neuropsychology.

[54]  M. Barnes,et al.  Linguistic outcomes following traumatic brain injury in children. , 2002, Seminars in pediatric neurology.

[55]  N. Walz,et al.  Late proton magnetic resonance spectroscopy following traumatic brain injury during early childhood: relationship with neurobehavioral outcomes. , 2008, Journal of neurotrauma.

[56]  B. Wandell,et al.  Tract Profiles of White Matter Properties: Automating Fiber-Tract Quantification , 2012, PloS one.

[57]  M. Filippi,et al.  Altered Recruitment of the Attention Network Is Associated with Disability and Cognitive Impairment in Pediatric Patients with Acquired Brain Injury , 2015, Neural plasticity.

[58]  Tricia L. Merkley,et al.  Longitudinal changes in cortical thickness in children after traumatic brain injury and their relation to behavioral regulation and emotional control , 2012, International Journal of Developmental Neuroscience.

[59]  I. Shelef,et al.  Blood-Brain Barrier Breakdown Following Traumatic Brain Injury: A Possible Role in Posttraumatic Epilepsy , 2011, Cardiovascular psychiatry and neurology.

[60]  R. Kikinis,et al.  A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury , 2012, Brain Imaging and Behavior.

[61]  J. Rosenfeld,et al.  Educational skills: Long-term outcome and predictors following paediatric traumatic brain injury , 2009, Neuropsychological rehabilitation.

[62]  Peter Herscovitch,et al.  A Review of the Effectiveness of Neuroimaging Modalities for the Detection of Traumatic Brain Injury. , 2015, Journal of neurotrauma.

[63]  H. Taylor,et al.  The Family Environment Predicts Long-Term Academic Achievement and Classroom Behavior Following Traumatic Brain Injury in Early Childhood , 2017, Neuropsychology.

[64]  C. Acerini,et al.  Traumatic brain injury induced hypothalamic-pituitary dysfunction: a paediatric perspective , 2007, Pituitary.

[65]  J. Stephens,et al.  Preliminary findings of altered functional connectivity of the default mode network linked to functional outcomes one year after pediatric traumatic brain injury , 2018, Developmental neurorehabilitation.

[66]  N. Walz,et al.  Neural substrates of inhibitory and emotional processing in adolescents with traumatic brain injury. , 2015, Journal of pediatric rehabilitation medicine.

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

[68]  Ana C. Vasquez,et al.  Diffusion Tensor Imaging of the Cingulum Bundle in Children After Traumatic Brain Injury , 2010, Developmental neuropsychology.

[69]  K. Chapman,et al.  Incidence of seizures on continuous EEG monitoring following traumatic brain injury in children. , 2015, Journal of neurosurgery. Pediatrics.

[70]  Jeffry R Alger,et al.  Metabolic levels in the corpus callosum and their structural and behavioral correlates after moderate to severe pediatric TBI. , 2010, Journal of neurotrauma.

[71]  Bradley S. Peterson,et al.  Loss of mTOR-Dependent Macroautophagy Causes Autistic-like Synaptic Pruning Deficits , 2014, Neuron.

[72]  Larry A. Kramer,et al.  Arrested development and disrupted callosal microstructure following pediatric traumatic brain injury: relation to neurobehavioral outcomes , 2008, NeuroImage.

[73]  S. Mostofsky,et al.  Altered functional connectivity in children with mild to moderate TBI relates to motor control. , 2015, Journal of pediatric rehabilitation medicine.

[74]  S. Ashwal,et al.  MR spectroscopy: Predicting long‐term neuropsychological outcome following pediatric TBI , 2006, Journal of magnetic resonance imaging : JMRI.

[75]  Yul-Wan Sung,et al.  Functional magnetic resonance imaging , 2004, Scholarpedia.

[76]  W. Walker,et al.  Motor impairment after severe traumatic brain injury: A longitudinal multicenter study. , 2007, Journal of rehabilitation research and development.

[77]  Early diffuse slowing on electroencephalogram in pediatric traumatic brain injury: Impact on management and prognosis. , 2015, Journal of pediatric surgery.

[78]  H S Levin,et al.  Reduction of corpus callosum growth after severe traumatic brain injury in children , 2000, Neurology.

[79]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[80]  H. Levin,et al.  Ten-year outcome of early childhood traumatic brain injury: Diffusion tensor imaging of the ventral striatum in relation to executive functioning , 2016, Brain injury.

[81]  H. Levin,et al.  Executive functions after traumatic brain injury in children. , 2005, Pediatric neurology.

[82]  H. Duffau,et al.  Frontal terminations for the inferior fronto-occipital fascicle: anatomical dissection, DTI study and functional considerations on a multi-component bundle , 2011, Brain Structure and Function.

[83]  C. Dixon,et al.  9 Neurotransmitters and Electrophysiology in Traumatic Brain Injury , 2009 .

[84]  Jocelyne Bachevalier,et al.  Hippocampus, amygdala, and basal ganglia morphometrics in children after moderate‐to‐severe traumatic brain injury , 2007, Developmental medicine and child neurology.

[85]  Paul M. Thompson,et al.  Tract-based spectroscopy to investigate pediatric brain trauma , 2017, Symposium on Medical Information Processing and Analysis.

[86]  S. Hearps,et al.  Uncovering the neuroanatomical correlates of cognitive, affective and conative theory of mind in paediatric traumatic brain injury: a neural systems perspective , 2017, Social cognitive and affective neuroscience.

[87]  Takayuki Kato,et al.  Statistical image analysis of cerebral glucose metabolism in patients with cognitive impairment following diffuse traumatic brain injury. , 2007, Journal of neurotrauma.

[88]  A. Karantanas,et al.  Outcome of patients with diffuse axonal injury: the significance and prognostic value of MRI in the acute phase. , 2000, The Journal of trauma.

[89]  L. Shah,et al.  Functional magnetic resonance imaging. , 2010, Seminars in roentgenology.

[90]  C. Giza,et al.  Is Being Plastic Fantastic? Mechanisms of Altered Plasticity after Developmental Traumatic Brain Injury , 2006, Developmental Neuroscience.

[91]  R. Mink,et al.  Pediatric traumatic brain injury: not just little adults , 2007, Current opinion in critical care.

[92]  Emily L. Dennis,et al.  Tensor-Based Morphometry Reveals Volumetric Deficits in Moderate=Severe Pediatric Traumatic Brain Injury , 2016, Journal of neurotrauma.

[93]  Cesar C. Santos,et al.  18‐FLUORODEOXYGLUCOSE POSITRON EMISSION TOMOGRAPHY IN CHILDREN AND ADOLESCENTS WITH TRAUMATIC BRAIN INJURY , 1995 .

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

[95]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[97]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[98]  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.

[99]  M. Phelps,et al.  Correlation of regional metabolic rates of glucose with glasgow coma scale after traumatic brain injury. , 2003, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[100]  G. Manley,et al.  Classification of traumatic brain injury for targeted therapies. , 2008, Journal of neurotrauma.

[101]  M. B. Nebel,et al.  Response Inhibition Deficits and Altered Motor Network Connectivity in the Chronic Phase of Pediatric Traumatic Brain Injury. , 2017, Journal of neurotrauma.

[102]  N. Jahanshad,et al.  Diverging volumetric trajectories following pediatric traumatic brain injury , 2017, NeuroImage: Clinical.

[103]  S. Swinnen,et al.  Bimanual coordination and corpus callosum microstructure in young adults with traumatic brain injury: a diffusion tensor imaging study. , 2010, Journal of neurotrauma.

[104]  J. Rosenfeld,et al.  Attentional skills 10 years post-paediatric traumatic brain injury (TBI) , 2011, Brain injury.

[105]  J. Langlois,et al.  Traumatic brain injury in the United States; emergency department visits, hospitalizations, and deaths , 2006 .

[106]  M. McKenna,et al.  Metabolic Alterations in Developing Brain After Injury: Knowns and Unknowns , 2015, Neurochemical Research.

[107]  Mary R. Newsome,et al.  Effects of traumatic brain injury on working memory-related brain activation in adolescents. , 2008, Neuropsychology.

[108]  Paul M. Thompson,et al.  Automatic clustering of white matter fibers in brain diffusion MRI with an application to genetics , 2014, NeuroImage.

[109]  W. Brooks,et al.  Magnetic resonance spectroscopy detects brain injury and predicts cognitive functioning in children with brain injuries. , 2006, Journal of neurotrauma.

[110]  D. Holtzman,et al.  Diffusion Tensor Imaging Reliably Detects Experimental Traumatic Axonal Injury and Indicates Approximate Time of Injury , 2007, The Journal of Neuroscience.

[111]  L. Mechtler,et al.  Advanced neuroimaging of mild traumatic brain injury. , 2014, Neurologic clinics.

[112]  Ana C. Vasquez,et al.  Diffusion tensor imaging of incentive effects in prospective memory after pediatric traumatic brain injury. , 2011, Journal of neurotrauma.

[113]  L. Kramer,et al.  White matter and reading deficits after pediatric traumatic brain injury: A diffusion tensor imaging study , 2015, NeuroImage: Clinical.

[114]  Tricia L. Merkley,et al.  How Functional Connectivity between Emotion Regulation Structures Can Be Disrupted: Preliminary Evidence from Adolescents with Moderate to Severe Traumatic Brain Injury , 2013, Journal of the International Neuropsychological Society.

[115]  Christopher Babbitt,et al.  Callosal Function in Pediatric Traumatic Brain Injury Linked to Disrupted White Matter Integrity , 2015, The Journal of Neuroscience.

[116]  Carl-Fredrik Westin,et al.  Automatic Tractography Segmentation Using a High-Dimensional White Matter Atlas , 2007, IEEE Transactions on Medical Imaging.

[117]  S. Wade,et al.  Neural correlates of verbal associative memory and mnemonic strategy use following childhood traumatic brain injury. , 2009, Journal of pediatric rehabilitation medicine.

[118]  M. Farneti,et al.  Occurrence of pituitary dysfunction following traumatic brain injury. , 2004, Journal of neurotrauma.

[119]  J. Fletcher,et al.  Lifetime and novel psychiatric disorders after pediatric traumatic brain injury. , 2001, Journal of the American Academy of Child and Adolescent Psychiatry.

[120]  Suzanne T. Witt,et al.  Multiple resting state network functional connectivity abnormalities in mild traumatic brain injury , 2012, Brain Imaging and Behavior.

[121]  Ruben G. L. Real,et al.  Traumatic brain injury: integrated approaches to improve prevention, clinical care, and research , 2017, The Lancet Neurology.

[122]  Brian A. Taylor,et al.  Advanced neuroimaging applied to veterans and service personnel with traumatic brain injury: state of the art and potential benefits , 2015, Brain Imaging and Behavior.

[123]  M. Ashtari Anatomy and functional role of the inferior longitudinal fasciculus: a search that has just begun , 2012, Developmental medicine and child neurology.

[124]  P. Karunanayaka,et al.  Diffusion Tensor MR Imaging Reveals Persistent White Matter Alteration after Traumatic Brain Injury Experienced during Early Childhood , 2007, American Journal of Neuroradiology.

[125]  H. Levin,et al.  Diffusion Tensor Imaging Analysis of Frontal Lobes in Pediatric Traumatic Brain Injury , 2010, Journal of child neurology.

[126]  Keith Owen Yeates,et al.  Social outcomes in childhood brain disorder: a heuristic integration of social neuroscience and developmental psychology. , 2007, Psychological bulletin.

[127]  Steven D Chen,et al.  The Superior Longitudinal Fasciculus in Typically Developing Children and Adolescents , 2015, Journal of child neurology.

[128]  Alan C. Evans,et al.  Growth patterns in the developing brain detected by using continuum mechanical tensor maps , 2000, Nature.

[129]  J. Hunter,et al.  Emerging imaging tools for use with traumatic brain injury research. , 2012, Journal of neurotrauma.

[130]  Talin Babikian,et al.  Neurocognitive outcomes and recovery after pediatric TBI: meta-analytic review of the literature. , 2009, Neuropsychology.

[131]  Brian B. Avants,et al.  Structural consequences of diffuse traumatic brain injury: A large deformation tensor-based morphometry study , 2008, NeuroImage.

[132]  Linda Ewing-Cobbs,et al.  Late intellectual and academic outcomes following traumatic brain injury sustained during early childhood. , 2006, Journal of neurosurgery.

[133]  S. Swinnen,et al.  Brain-behavior relationships in young traumatic brain injury patients: Fractional anisotropy measures are highly correlated with dynamic visuomotor tracking performance , 2010, Neuropsychologia.

[134]  P. Karunanayaka,et al.  Long-term neural processing of attention following early childhood traumatic brain injury: fMRI and neurobehavioral outcomes , 2008, Journal of the International Neuropsychological Society.

[135]  S. Ashwal,et al.  Predicting neuropsychologic outcome after traumatic brain injury in children. , 2003, Pediatric neurology.

[136]  E. Melhem,et al.  Neuroimaging: applications in disorders of early brain development. , 2000, Journal of developmental and behavioral pediatrics : JDBP.

[137]  Daniele Marinazzo,et al.  Enhanced prefrontal functional–structural networks to support postural control deficits after traumatic brain injury in a pediatric population , 2017, Network Neuroscience.

[138]  Weihong Yuan,et al.  Changes in Structural Connectivity Following a Cognitive Intervention in Children With Traumatic Brain Injury , 2017, Neurorehabilitation and neural repair.

[139]  Erin D Bigler,et al.  Patterns of Cortical Thinning in Relation to Event-Based Prospective Memory Performance Three Months after Moderate to Severe Traumatic Brain Injury in Children , 2010, Developmental neuropsychology.

[140]  R. Huber,et al.  High-Density Electroencephalographic Recordings During Sleep in Children and Adolescents With Acquired Brain Injury , 2017, Neurorehabilitation and Neural Repair.

[141]  S. Holland,et al.  Diffusion tensor imaging detects white matter abnormalities and associated cognitive deficits in chronic adolescent TBI , 2013, Brain injury.

[142]  D. Thurman,et al.  The Epidemiology of Traumatic Brain Injury in Children and Youths , 2016, Journal of child neurology.

[143]  David L McArthur,et al.  The UCLA Study of Children with Moderate-to-Severe Traumatic Brain Injury: Event-Related Potential Measure of Interhemispheric Transfer Time. , 2016, Journal of neurotrauma.