White matter microstructure in trauma-exposed children: Associations with pubertal stage.

Puberty represents a critical period in maturation during which major changes in neural architecture emerge; these changes are shaped, in part, by environmental experiences, including exposure to psychological trauma. However, little is known about how trauma exposure affects white matter microstructure across pubertal stages. This was the goal of the present cross-sectional study. Forty-one male and female African-American children between ages 8-13 were recruited as part of a study of developmental trauma and received assessments of trauma exposure, including violence, and pubertal development as well as diffusion tensor imaging (DTI). Significant interactions of pubertal stage and violent trauma exposure were observed in association with a marker of white matter integrity (mean diffusivity, MD) in the corpus callosum, cingulum bundle and uncinate fasciculus. Greater violent trauma exposure was associated with lower MD in the hippocampal cingulum and uncinate fasciculus in girls, but not boys. These data from a sample of trauma-exposed children may reflect a pattern of accelerated maturation in pathways that are critical for emotion regulation as well as attention and memory processes. It appears that fronto-limbic and callosal connections are particularly sensitive to the effects of violent trauma, revealing a potential pathway through which trauma creates vulnerability for later psychiatric and neurological disorders.

[1]  C. Lebel,et al.  Different brain profiles in children with prenatal alcohol exposure with or without early adverse exposures , 2020, Human brain mapping.

[2]  T. Jovanović,et al.  Puberty drives fear learning during adolescence. , 2020, Developmental Science.

[3]  N. Pedersen,et al.  Association of Stress-Related Disorders With Subsequent Neurodegenerative Diseases. , 2020, JAMA neurology.

[4]  N. Tottenham,et al.  Increased activation of the fear neurocircuitry in children exposed to violence , 2020, Depression and anxiety.

[5]  K. Ressler,et al.  Structural connectivity and risk for anhedonia after trauma: A prospective study and replication. , 2019, Journal of psychiatric research.

[6]  Adon F. G. Rosen,et al.  Burden of Environmental Adversity Associated With Psychopathology, Maturation, and Brain Behavior Parameters in Youths. , 2019, JAMA psychiatry.

[7]  E. Crone,et al.  Understanding the Role of Puberty in Structural and Functional Development of the Adolescent Brain. , 2019, Journal of research on adolescence : the official journal of the Society for Research on Adolescence.

[8]  Katie A. McLaughlin,et al.  Early Experiences of Threat, but Not Deprivation, Are Associated With Accelerated Biological Aging in Children and Adolescents , 2019, Biological Psychiatry.

[9]  S. Rombouts,et al.  General psychopathology factor and unresolved-disorganized attachment uniquely correlated to white matter integrity using diffusion tensor imaging , 2019, Behavioural Brain Research.

[10]  M. Del Giudice,et al.  Developmental Adaptation to Stress: An Evolutionary Perspective. , 2019, Annual review of psychology.

[11]  D. Lyons,et al.  Myelin Dynamics Throughout Life: An Ever-Changing Landscape? , 2018, Front. Cell. Neurosci..

[12]  Jennifer H. Pfeifer,et al.  Puberty and the human brain: Insights into adolescent development , 2018, Neuroscience & Biobehavioral Reviews.

[13]  M. Kubicki,et al.  Childhood adversity associated with white matter alteration in the corpus callosum, corona radiata, and uncinate fasciculus of psychiatrically healthy adults , 2018, Brain Imaging and Behavior.

[14]  T. Jovanović,et al.  Exposure to Violence Accelerates Epigenetic Aging in Children , 2017, Scientific Reports.

[15]  E. Sowell,et al.  Puberty and structural brain development in humans , 2017, Frontiers in Neuroendocrinology.

[16]  Elizabeth M Davenport,et al.  Abnormalities in Diffusional Kurtosis Metrics Related to Head Impact Exposure in a Season of High School Varsity Football. , 2016, Journal of neurotrauma.

[17]  Kirsten M P McKone,et al.  Early Childhood Maltreatment and Pubertal Development: Replication in a Population-Based Sample. , 2016, Journal of research on adolescence : the official journal of the Society for Research on Adolescence.

[18]  R. Marioni,et al.  Corrigendum: The epigenetic clock and telomere length are independently associated with chronological age and mortality [Int J Epidemiol., 45, 2, (424-432)(2016)] DOI: 10.1093/ije/dyw041 , 2016 .

[19]  Tricia Z. King,et al.  STRUCTURAL AND FUNCTIONAL CONNECTIVITY IN POSTTRAUMATIC STRESS DISORDER: ASSOCIATIONS WITH FKBP5 , 2016, Depression and anxiety.

[20]  N. Tottenham,et al.  The Stress Acceleration Hypothesis: effects of early-life adversity on emotion circuits and behavior , 2016, Current Opinion in Behavioral Sciences.

[21]  Bung-Nyun Kim,et al.  Increased white matter connectivity in traumatized children with attention deficit hyperactivity disorder , 2016, Psychiatry Research: Neuroimaging.

[22]  Alan C. Evans,et al.  Trajectories of cortical thickness maturation in normal brain development — The importance of quality control procedures , 2016, NeuroImage.

[23]  A. Dale,et al.  Through Thick and Thin: a Need to Reconcile Contradictory Results on Trajectories in Human Cortical Development , 2016, Cerebral cortex.

[24]  S. Rombouts,et al.  Abnormalities of white matter integrity in the corpus callosum of adolescents with PTSD after childhood sexual abuse: a DTI study , 2015, European Child & Adolescent Psychiatry.

[25]  Naomi R. Wray,et al.  Lifetime stress accelerates epigenetic aging in an urban, African American cohort: relevance of glucocorticoid signaling , 2015, Genome Biology.

[26]  M. Matsui,et al.  Normal Development of Human Brain White Matter from Infancy to Early Adulthood: A Diffusion Tensor Imaging Study , 2015, Developmental Neuroscience.

[27]  Tricia Z. King,et al.  Fear-potentiated startle during extinction is associated with white matter microstructure and functional connectivity , 2015, Cortex.

[28]  Sarah-Jayne Blakemore,et al.  Is adolescence a sensitive period for sociocultural processing? , 2014, Annual review of psychology.

[29]  W. Frankenhuis,et al.  Does Early-Life Exposure to Stress Shape or Impair Cognition? , 2013 .

[30]  E. Crone,et al.  Sex differences and structural brain maturation from childhood to early adulthood , 2013, Developmental Cognitive Neuroscience.

[31]  Thomas R. Knösche,et al.  White matter integrity, fiber count, and other fallacies: The do's and don'ts of diffusion MRI , 2013, NeuroImage.

[32]  N. Wee,et al.  Neuroimaging in children, adolescents and young adults with psychological trauma , 2013, European Child & Adolescent Psychiatry.

[33]  H. Walter,et al.  WHITE MATTER INTEGRITY AND ITS RELATIONSHIP TO PTSD AND CHILDHOOD TRAUMA—A SYSTEMATIC REVIEW AND META‐ANALYSIS , 2013, Depression and anxiety.

[34]  Ernestine C. Briggs,et al.  Psychometric properties of the UCLA PTSD reaction index: part I. , 2013, Journal of traumatic stress.

[35]  Tricia Z. King,et al.  White Matter Integrity in Highly Traumatized Adults With and Without Post-Traumatic Stress Disorder , 2012, Neuropsychopharmacology.

[36]  Hao Huang,et al.  White Matter Disruptions in Adolescents Exposed to Childhood Maltreatment and Vulnerability to Psychopathology , 2012, Neuropsychopharmacology.

[37]  Bonnie J Nagel,et al.  The impact of sex, puberty, and hormones on white matter microstructure in adolescents. , 2012, Cerebral cortex.

[38]  C. Lebel,et al.  Diffusion tensor imaging of white matter tract evolution over the lifespan , 2012, NeuroImage.

[39]  Terry L. Jernigan,et al.  Longitudinal characterization of white matter maturation during adolescence , 2010, Brain Research.

[40]  R. Romeo Pubertal maturation and programming of hypothalamic–pituitary–adrenal reactivity , 2010, Frontiers in Neuroendocrinology.

[41]  V. Schmithorst,et al.  White matter development during adolescence as shown by diffusion MRI , 2010, Brain and Cognition.

[42]  Ronald E. Dahl,et al.  Pubertal development and behavior: Hormonal activation of social and motivational tendencies , 2010, Brain and Cognition.

[43]  B. Bradley,et al.  Childhood abuse is associated with increased startle reactivity in adulthood , 2009, Depression and anxiety.

[44]  B. Bradley,et al.  Trauma exposure and stress-related disorders in inner city primary care patients. , 2009, General hospital psychiatry.

[45]  Paul M. Thompson,et al.  Extending Genetic Linkage Analysis to Diffusion Tensor Images to Map Single Gene Effects on Brain Fiber Architecture , 2009, MICCAI.

[46]  Stephan Eliez,et al.  Converging evidence for abnormalities of the prefrontal cortex and evaluation of midsagittal structures in pediatric posttraumatic stress disorder: An MRI study , 2009, Psychiatry Research: Neuroimaging.

[47]  T. Paus,et al.  Sex differences in the growth of white matter during adolescence , 2009, NeuroImage.

[48]  R. Dahl,et al.  Pubertal development: correspondence between hormonal and physical development. , 2009, Child development.

[49]  Bumseok Jeong,et al.  Preliminary Evidence for White Matter Tract Abnormalities in Young Adults Exposed to Parental Verbal Abuse , 2009, Biological Psychiatry.

[50]  B. Mädler,et al.  Is diffusion anisotropy an accurate monitor of myelination? Correlation of multicomponent T2 relaxation and diffusion tensor anisotropy in human brain. , 2008, Magnetic resonance imaging.

[51]  Richard F. Thompson,et al.  Progesterone receptors: Form and function in brain , 2008, Frontiers in Neuroendocrinology.

[52]  Robert T. Schultz,et al.  Corpus callosum in maltreated children with posttraumatic stress disorder: A diffusion tensor imaging study , 2008, Psychiatry Research: Neuroimaging.

[53]  Peter A. Calabresi,et al.  Tract probability maps in stereotaxic spaces: Analyses of white matter anatomy and tract-specific quantification , 2008, NeuroImage.

[54]  Paul M. Thompson,et al.  Sexual dimorphism of brain developmental trajectories during childhood and adolescence , 2007, NeuroImage.

[55]  Cheuk Y. Tang,et al.  Diffusion Tensor Anisotropy in Adolescents and Adults , 2007, Neuropsychobiology.

[56]  Larry A. Kramer,et al.  Diffusion tensor imaging-based tissue segmentation: Validation and application to the developing child and adolescent brain , 2007, NeuroImage.

[57]  Larry A. Tupler,et al.  Segmented Hippocampal Volume in Children and Adolescents with Posttraumatic Stress Disorder , 2006, Biological Psychiatry.

[58]  D. Coall,et al.  Early stress predicts age at menarche and first birth, adult attachment, and expected lifespan , 2005, Human nature.

[59]  Talma Hendler,et al.  Normal white matter development from infancy to adulthood: Comparing diffusion tensor and high b value diffusion weighted MR images , 2005, Journal of magnetic resonance imaging : JMRI.

[60]  Kenneth L. Jones,et al.  A Validation Study of Early Adolescents’ Pubertal Self-Assessments , 2004 .

[61]  C. Sisk,et al.  The neural basis of puberty and adolescence , 2004, Nature Neuroscience.

[62]  Suzanne E. Welcome,et al.  Mapping cortical change across the human life span , 2003, Nature Neuroscience.

[63]  C. Beaulieu,et al.  The basis of anisotropic water diffusion in the nervous system – a technical review , 2002, NMR in biomedicine.

[64]  T. Jernigan,et al.  Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study , 2002, Developmental medicine and child neurology.

[65]  B. McEwen Invited review: Estrogens effects on the brain: multiple sites and molecular mechanisms. , 2001, Journal of applied physiology.

[66]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[67]  J. Gabrieli,et al.  Myelination and organization of the frontal white matter in children: a diffusion tensor MRI study. , 1999, Neuroreport.

[68]  Alan C. Evans,et al.  Structural maturation of neural pathways in children and adolescents: in vivo study. , 1999, Science.

[69]  F. Benes,et al.  Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. , 1994, Archives of general psychiatry.

[70]  C. Nelson,et al.  Early Adverse Experiences and the Developing Brain , 2016, Neuropsychopharmacology.

[71]  Adriana Galvan,et al.  The adolescent brain. , 2008, Developmental review : DR.

[72]  A. Reiss,et al.  Regional differences of the prefrontal cortex in pediatric PTSD: an MRI study , 2006, Depression and anxiety.

[73]  F. Benes,et al.  Myelination of cortical-hippocampal relays during late adolescence. , 1989, Schizophrenia bulletin.