Altered White Matter Microstructure in Adolescents and Adults with Bulimia Nervosa

Previous data suggest structural and functional deficits in frontal control circuits in adolescents and adults with bulimia nervosa (BN), but less is known about the microstructure of white matter in these circuits early in the course of the disorder. Diffusion tensor imaging (DTI) data were acquired from 28 female adolescents and adults with BN and 28 age- and BMI-matched healthy female participants. Tract-based spatial statistics (TBSS) was used to detect group differences in white matter microstructure and explore the differential effects of age on white matter microstructure across groups. Significant reductions in fractional anisotropy (FA) were detected in the BN compared with healthy control group in multiple tracts including forceps minor and major, superior longitudinal, inferior fronto-occipital, and uncinate fasciculi, anterior thalamic radiation, cingulum, and corticospinal tract. FA reductions in forceps and frontotemporal tracts correlated inversely with symptom severity and Stroop interference in the BN group. These findings suggest that white matter microstructure is abnormal in BN in tracts extending through frontal and temporoparietal cortices, especially in those with the most severe symptoms. Age-related differences in both FA and RD in these tracts in BN compared with healthy individuals may represent an abnormal trajectory of white matter development that contributes to the persistence of functional impairments in self-regulation in BN.

[1]  A. Zalesky,et al.  Disruption of brain white matter microstructure in women with anorexia nervosa. , 2014, Journal of psychiatry & neuroscience : JPN.

[2]  M. Catani,et al.  A diffusion tensor imaging tractography atlas for virtual in vivo dissections , 2008, Cortex.

[3]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[4]  Heidi Johansen-Berg,et al.  Changes in white matter microstructure during adolescence , 2008, NeuroImage.

[5]  Gabriele Polonara,et al.  Functional Topography of Human Corpus Callosum: An fMRI Mapping Study , 2013, Neural plasticity.

[6]  Wei Liu,et al.  Automated assessment of the quality of diffusion tensor imaging data using color cast of color-encoded fractional anisotropy images. , 2014, Magnetic resonance imaging.

[7]  R. Bronen,et al.  MR imaging of the temporal stem: anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer's loop of the optic radiation. , 2004, AJNR. American journal of neuroradiology.

[8]  Hugues Duffau,et al.  Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data , 2010, Cortex.

[9]  Joanna Jacobus,et al.  Altered white matter integrity in adolescent binge drinkers. , 2009, Alcoholism, clinical and experimental research.

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

[11]  B. Peterson,et al.  Deficient activity in the neural systems that mediate self-regulatory control in bulimia nervosa. , 2009, Archives of general psychiatry.

[12]  J. Hagman,et al.  Alterations in brain structures related to taste reward circuitry in ill and recovered anorexia nervosa and in bulimia nervosa. , 2013, The American journal of psychiatry.

[13]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[14]  Stephen M. Smith,et al.  Crossing fibres in tract-based spatial statistics , 2010, NeuroImage.

[15]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[16]  J. Reichenbach,et al.  Association between white matter fiber structure and reward‐related reactivity of the ventral striatum , 2014, Human brain mapping.

[17]  D. Pandya,et al.  Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. , 2005, Cerebral cortex.

[18]  Daniel Romer,et al.  Adolescent risk taking, impulsivity, and brain development: implications for prevention. , 2010, Developmental psychobiology.

[19]  S. Wakana,et al.  MRI Atlas of Human White Matter , 2005 .

[20]  W. Orrison,et al.  Atlas of Brain Function , 1995 .

[21]  Hongtu Zhu,et al.  A developmental fMRI study of self‐regulatory control , 2006, Human brain mapping.

[22]  B. Peterson,et al.  Anatomical Characteristics of the Cerebral Surface in Bulimia Nervosa , 2015, Biological Psychiatry.

[23]  Yasuyuki Taki,et al.  Brain structures associated with executive functions during everyday events in a non-clinical sample , 2012, Brain Structure and Function.

[24]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[25]  B. Peterson,et al.  An FMRI study of self-regulatory control and conflict resolution in adolescents with bulimia nervosa. , 2011, The American journal of psychiatry.

[26]  P. Szeszko,et al.  MRI atlas of human white matter , 2006 .

[27]  J. Ridley Studies of Interference in Serial Verbal Reactions , 2001 .

[28]  B. Sonies,et al.  Dysphagia in bulimia nervosa , 1989, Dysphagia.

[29]  P. DeRosse,et al.  Age-Related Differences in White Matter Tract Microstructure Are Associated with Cognitive Performance from Childhood to Adulthood , 2014, Biological Psychiatry.

[30]  K. Davis,et al.  Myelination, oligodendrocytes, and serious mental illness , 2014, Glia.

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

[32]  Atsushi Iriki,et al.  Self-images in the video monitor coded by monkey intraparietal neurons , 2001, Neuroscience Research.

[33]  J. Fleiss,et al.  Medication and psychotherapy in the treatment of bulimia nervosa. , 1997, The American journal of psychiatry.

[34]  Volker A Coenen,et al.  Human medial forebrain bundle (MFB) and anterior thalamic radiation (ATR): imaging of two major subcortical pathways and the dynamic balance of opposite affects in understanding depression. , 2012, The Journal of neuropsychiatry and clinical neurosciences.

[35]  B. Luna,et al.  White matter development in adolescence: a DTI study. , 2010, Cerebral cortex.

[36]  Thomas F. Münte,et al.  Microstructural Brain Differences Predict Functional Hemodynamic Responses in a Reward Processing Task , 2010, The Journal of Neuroscience.

[37]  Samantha J. Brooks,et al.  Nonvisual Multisensory Impairment of Body Perception in Anorexia Nervosa: A Systematic Review of Neuropsychological Studies , 2014, PloS one.

[38]  H. Ge,et al.  Fiber Pathways of Attention Subnetworks Revealed with Tract-Based Spatial Statistics (TBSS) and Probabilistic Tractography , 2013, PloS one.

[39]  Alexander Leemans,et al.  Microstructural maturation of the human brain from childhood to adulthood , 2008, NeuroImage.

[40]  C. Lebel,et al.  Longitudinal Development of Human Brain Wiring Continues from Childhood into Adulthood , 2011, The Journal of Neuroscience.

[41]  V. Glauche,et al.  Voxel-based morphometry in eating disorders: Correlation of psychopathology with grey matter volume , 2010, Psychiatry Research: Neuroimaging.

[42]  Daniella J. Furman,et al.  Menstrual cycle phase modulates reward-related neural function in women , 2007, Proceedings of the National Academy of Sciences.

[43]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[44]  J. Maller,et al.  Brain connectivity in body dysmorphic disorder compared with controls: a diffusion tensor imaging study , 2013, Psychological Medicine.

[45]  J. Hagman,et al.  Altered fimbria-fornix white matter integrity in anorexia nervosa predicts harm avoidance , 2011, Psychiatry Research: Neuroimaging.

[46]  G. Frank,et al.  White matter integrity is reduced in bulimia nervosa. , 2013, The International journal of eating disorders.

[47]  J. Rapoport,et al.  Structural MRI of Pediatric Brain Development: What Have We Learned and Where Are We Going? , 2010, Neuron.

[48]  P. Shaw,et al.  White Matter Microstructure and the Variable Adult Outcome of Childhood Attention Deficit Hyperactivity Disorder , 2015, Neuropsychopharmacology.

[49]  Khader M Hasan,et al.  Reduced Anterior Corpus Callosum White Matter Integrity is Related to Increased Impulsivity and Reduced Discriminability in Cocaine-Dependent Subjects: Diffusion Tensor Imaging , 2005, Neuropsychopharmacology.

[50]  John Russell,et al.  Dysmyelination Revealed through MRI as Increased Radial (but Unchanged Axial) Diffusion of Water , 2002, NeuroImage.