Tract-based spatial statistics (TBSS) of diffusion tensor imaging data in alcohol dependence: Abnormalities of the motivational neurocircuitry

Previous diffusion tensor imaging (DTI) studies indicated microstructural disruption of white matter in alcohol dependence. To investigate the microstructure of primary neurocircuitry involved in alcohol use disorders, the present study used Tract-Based Spatial Statistics (TBSS) of DTI measures as well as probabilistic tractography. Eleven recovering alcoholics in their first week of abstinence from alcohol were compared with 10 light-drinking controls; diffusion measures were correlated with measures of neurocognition and drinking severity. Regions characterized by low fractional anisotropy and high mean diffusivity included cortico-striatal fibers and those in frontal white matter and limbic pathways. Greater diffusion abnormalities in sections of commissural fibers (inter-hemispheric connections) were associated with greater drinking severity, and lower fractional anisotropy measures in frontal and limbic fiber tracts correlated with lower visuospatial memory performance. These study findings provide direct evidence of compromised integrity of the motivational brain circuitry in alcohol use disorders. These abnormalities in fiber connections could be partially responsible for deficiencies in executive functions, behavioral regulation, and impulse control commonly described in alcohol dependence.

[1]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[2]  Karl Sjöstrand,et al.  Hierarchical linear modeling (HLM) of longitudinal brain structural and cognitive changes in alcohol-dependent individuals during sobriety. , 2007, Drug and alcohol dependence.

[3]  Rita Z. Goldstein,et al.  Role of Dopamine, the Frontal Cortex and Memory Circuits in Drug Addiction: Insight from Imaging Studies , 2002, Neurobiology of Learning and Memory.

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

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

[6]  Adolf Pfefferbaum,et al.  Diffusion tensor imaging with quantitative fibre tracking in HIV infection and alcoholism comorbidity: synergistic white matter damage. , 2006, Brain : a journal of neurology.

[7]  P. Lauterbur,et al.  Apparent diffusion tensor measurements in myelin‐deficient rat spinal cords , 2001, Magnetic resonance in medicine.

[8]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[9]  A. Pfefferbaum,et al.  Disruption of Brain White Matter Microstructure by Excessive Intracellular and Extracellular Fluid in Alcoholism: Evidence from Diffusion Tensor Imaging , 2005, Neuropsychopharmacology.

[10]  A. Snyder,et al.  Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. , 1998, Radiology.

[11]  A. Gass,et al.  Acute and chronic changes of the apparent diffusion coefficient in neurological disorders—biophysical mechanisms and possible underlying histopathology , 2001, Journal of the Neurological Sciences.

[12]  Linda C. Sobell,et al.  Timeline Follow-Back A Technique for Assessing Self-Reported Alcohol Consumption , 1992 .

[13]  P. Morell,et al.  Gene Expression in Brain during Cuprizone-Induced Demyelination and Remyelination , 1998, Molecular and Cellular Neuroscience.

[14]  Edith V. Sullivan,et al.  Supratentorial Profile of White Matter Microstructural Integrity in Recovering Alcoholic Men and Women , 2006, Biological Psychiatry.

[15]  Timothy Edward John Behrens,et al.  Characterization and propagation of uncertainty in diffusion‐weighted MR imaging , 2003, Magnetic resonance in medicine.

[16]  K O Lim,et al.  In vivo detection and functional correlates of white matter microstructural disruption in chronic alcoholism. , 2000, Alcoholism, clinical and experimental research.

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

[18]  JaneR . Taylor,et al.  Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli , 1999, Psychopharmacology.

[19]  M. Yücel,et al.  Neurocognitive and neuroimaging evidence of behavioural dysregulation in human drug addiction: implications for diagnosis, treatment and prevention. , 2007, Drug and alcohol review.

[20]  A. Wright,et al.  Magnetic resonance microimaging of intraaxonal water diffusion in live excised lamprey spinal cord , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[21]  C. Sotak Nuclear magnetic resonance (NMR) measurement of the apparent diffusion coefficient (ADC) of tissue water and its relationship to cell volume changes in pathological states , 2004, Neurochemistry International.

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

[23]  Daniel Rueckert,et al.  Nonrigid registration using free-form deformations: application to breast MR images , 1999, IEEE Transactions on Medical Imaging.

[24]  J. Mcnulty,et al.  Direct measurement of fast axonal organelle transport in chronic ethanol-fed rats. , 1992, Alcoholism, clinical and experimental research.

[25]  Edith V. Sullivan,et al.  Dysmorphology and microstructural degradation of the corpus callosum: Interaction of age and alcoholism , 2006, Neurobiology of Aging.

[26]  R. Schreiber,et al.  Long-term alcohol self-administration and alcohol withdrawal differentially modulate microtubule-associated protein 2 (MAP2) gene expression in the rat brain. , 1998, Brain research. Molecular brain research.

[27]  J. Kril,et al.  The cerebral cortex is damaged in chronic alcoholics , 1997, Neuroscience.

[28]  Adolf Pfefferbaum,et al.  Diffusion tensor imaging in normal aging and neuropsychiatric disorders. , 2003, European journal of radiology.

[29]  Terry E. Robinson,et al.  Incentive-sensitization As The Basis Of Drug Craving , 1993 .

[30]  N. Volkow,et al.  Drug addiction: the neurobiology of disrupted self-control. , 2006, Trends in molecular medicine.

[31]  M S Mega,et al.  Frontal-subcortical circuits and neuropsychiatric disorders. , 1994, The Journal of neuropsychiatry and clinical neurosciences.

[32]  A. Alexander,et al.  White matter tractography using diffusion tensor deflection , 2003, Human brain mapping.

[33]  S. McElroy,et al.  The relationship between substance use disorders, impulse control disorders, and pathological aggression. , 1998, The American journal on addictions.

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

[35]  C Studholme,et al.  Quantitative brain MRI in alcohol dependence: preliminary evidence for effects of concurrent chronic cigarette smoking on regional brain volumes. , 2005, Alcoholism, clinical and experimental research.

[36]  Jerry L. Prince,et al.  Effects of diffusion weighting schemes on the reproducibility of DTI-derived fractional anisotropy, mean diffusivity, and principal eigenvector measurements at 1.5T , 2007, NeuroImage.

[37]  K O Lim,et al.  Longitudinal changes in magnetic resonance imaging brain volumes in abstinent and relapsed alcoholics. , 1995, Alcoholism, clinical and experimental research.

[38]  P. Basser,et al.  Toward a quantitative assessment of diffusion anisotropy , 1996, Magnetic resonance in medicine.

[39]  Timothy Edward John Behrens,et al.  Probabilistic diffusion tractography: a potential tool to assess the rate of disease progression in amyotrophic lateral sclerosis. , 2006, Brain : a journal of neurology.

[40]  P. Poulet,et al.  Brain dysmyelination and recovery assessment by noninvasive in vivo diffusion tensor magnetic resonance imaging , 2006, Journal of neuroscience research.

[41]  Timothy Edward John Behrens,et al.  Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging , 2003, Nature Neuroscience.

[42]  M. Horsfield,et al.  Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging , 1999, Magnetic resonance in medicine.

[43]  Elizabeth L. Ogburn,et al.  Prevalence, correlates, disability, and comorbidity of DSM-IV alcohol abuse and dependence in the United States: results from the National Epidemiologic Survey on Alcohol and Related Conditions. , 2007, Archives of general psychiatry.

[44]  M. H. Parks,et al.  Disruption of frontocerebellar circuitry and function in alcoholism. , 2003, Alcoholism, clinical and experimental research.

[45]  Shu-Wei Sun,et al.  Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia , 2003, NeuroImage.

[46]  N. Conradi,et al.  Decreased axonal calibres without axonal loss in optic nerve following chronic alcohol feeding in adult rats: a morphometric study , 2004, Acta Neuropathologica.

[47]  M. Oscar-Berman,et al.  Alcoholism, aging, and functional cerebral asymmetries. , 1989, Psychological bulletin.

[48]  David H. Miller,et al.  Diffusion tensor imaging can detect and quantify corticospinal tract degeneration after stroke , 2000, Journal of neurology, neurosurgery, and psychiatry.

[49]  P. Basser,et al.  Water Diffusion Changes in Wallerian Degeneration and Their Dependence on White Matter Architecture , 2000 .

[50]  JaneR . Taylor,et al.  Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. , 2003, The American journal of psychiatry.

[51]  H A Skinner,et al.  Reliability of alcohol use indices. The Lifetime Drinking History and the MAST. , 1982, Journal of studies on alcohol.

[52]  Susumu Mori,et al.  Diffusion tensor brain imaging and tractography. , 2002, Neuroimaging clinics of North America.

[53]  Stefan Gazdzinski,et al.  Cigarette smoking exacerbates chronic alcohol-induced brain damage: a preliminary metabolite imaging study. , 2004, Alcoholism, clinical and experimental research.

[54]  Adolf Pfefferbaum,et al.  Microstructural but Not Macrostructural Disruption of White Matter in Women with Chronic Alcoholism , 2002, NeuroImage.

[55]  B. Grant,et al.  Comorbidity Between DSM–IV Alcohol and Specific Drug Use Disorders in the United States , 2005, Drug and alcohol dependence.

[56]  G. Gmel,et al.  Measuring Alcohol Consumption , 2004 .

[57]  H. Demaree,et al.  Brain lateralization of emotional processing: historical roots and a future incorporating "dominance". , 2005, Behavioral and cognitive neuroscience reviews.

[58]  N. Volkow,et al.  The neural basis of addiction: a pathology of motivation and choice. , 2005, The American journal of psychiatry.

[59]  Derek K. Jones,et al.  The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: A Monte Carlo study † , 2004, Magnetic resonance in medicine.

[60]  R. Benedict Effects of using same- versus alternate-form memory tests during short-interval repeated assessments in multiple sclerosis , 2005, Journal of the International Neuropsychological Society.

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

[62]  M. Oscar-Berman,et al.  Relationship between dopaminergic neurotransmission, alcoholism, and reward deficiency syndrome , 2005, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[63]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[64]  A. Pfefferbaum,et al.  Neurocircuitry in alcoholism: a substrate of disruption and repair , 2005, Psychopharmacology.

[65]  M. Yücel,et al.  Addiction, a condition of compulsive behaviour? Neuroimaging and neuropsychological evidence of inhibitory dysregulation. , 2004, Addiction.

[66]  Dieter J Meyerhoff,et al.  Neurobiological and neurocognitive effects of chronic cigarette smoking and alcoholism. , 2007, Frontiers in bioscience : a journal and virtual library.

[67]  P. Carlen,et al.  Partially Reversible Cerebral Atrophy and Functional Improvement in Recently Abstinent Alcoholics , 1984, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[68]  E. Sullivan Compromised pontocerebellar and cerebellothalamocortical systems: speculations on their contributions to cognitive and motor impairment in nonamnesic alcoholism. , 2003, Alcoholism, clinical and experimental research.

[69]  K. Fagerström,et al.  Towards better diagnoses and more individual treatment of tobacco dependence. , 1991, British journal of addiction.

[70]  Timothy Edward John Behrens,et al.  Discordant white matter N-acetylasparate and diffusion MRI measures suggest that chronic metabolic dysfunction contributes to axonal pathology in multiple sclerosis , 2007, NeuroImage.

[71]  V. Wedeen,et al.  Reduction of eddy‐current‐induced distortion in diffusion MRI using a twice‐refocused spin echo , 2003, Magnetic resonance in medicine.