Error-related negativity is mediated by fractional anisotropy in the posterior cingulate gyrus--a study combining diffusion tensor imaging and electrophysiology in healthy adults.

White matter (WM) is critical to cognitive function and brain activity. The objective of the present study was to test whether diffusion tensor imaging (DTI) derived WM measures are related to the cognitive event-related potential error-related negativity (ERN). Eighty-seven healthy middle-aged adults underwent DTI scanning and electrophysiological recordings while doing a version of the Eriksen flanker task. ERN was elicited in error trials. Fractional anisotropy (FA) was calculated based on the DTI scans. FA indexes degree of anisotropic diffusion in every voxel, and is assumed related to the integrity of myelinated fiber bundles. The principal neuronal generator for ERN is located in the anterior cingulate cortex (ACC). Hence, the relationship between FA in the cingulum bundle and ERN amplitude was tested. It was found that FA in the left posterior cingulate correlated with ERN. Eigenvalue analyses revealed that radial diffusivity was responsible for the FA effect. ERN amplitude predicted response accuracy in the Flanker task, suggesting that electrophysiological measures are intermediate explanatory variables connecting DTI indices of WM organization, synchronization of large cell assemblies, and behavior.

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

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

[3]  J. Hohnsbein,et al.  ERP components on reaction errors and their functional significance: a tutorial , 2000, Biological Psychology.

[4]  Colin Studholme,et al.  Using automated morphometry to detect associations between ERP latency and structural brain MRI in normal adults , 2005, Human brain mapping.

[5]  Matthias J. Müller,et al.  Ultrastructural Hippocampal and White Matter Alterations in Mild Cognitive Impairment: A Diffusion Tensor Imaging Study , 2004, Dementia and Geriatric Cognitive Disorders.

[6]  A. Dale,et al.  Age‐Related Changes in Prefrontal White Matter Measured by Diffusion Tensor Imaging , 2005, Annals of the New York Academy of Sciences.

[7]  Scott A. Huettel,et al.  Diffusion tensor imaging of adult age differences in cerebral white matter: relation to response time , 2004, NeuroImage.

[8]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

[9]  K. Lim,et al.  Advances in white matter imaging: A review of in vivo magnetic resonance methodologies and their applicability to the study of development and aging , 2006, Neuroscience & Biobehavioral Reviews.

[10]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[11]  Matthias J. Müller,et al.  Predicting conversion to dementia in mild cognitive impairment by volumetric and diffusivity measurements of the hippocampus , 2006, Psychiatry Research: Neuroimaging.

[12]  D. Tuch.  Q‐ball imaging , 2004, Magnetic resonance in medicine.

[13]  G. Bartzokis,et al.  Heterogeneous age-related breakdown of white matter structural integrity: implications for cortical “disconnection” in aging and Alzheimer’s disease , 2004, Neurobiology of Aging.

[14]  Clay B. Holroyd,et al.  Errors in reward prediction are re£ected in the event-related brain potential , 2003 .

[15]  Scott T. Grafton,et al.  Wandering Minds: The Default Network and Stimulus-Independent Thought , 2007, Science.

[16]  R. Knight,et al.  Prefrontal–cingulate interactions in action monitoring , 2000, Nature Neuroscience.

[17]  C. A. Clark,et al.  A structural equation modeling investigation of age-related variance in executive function and DTI measured white matter damage , 2008, Neurobiology of Aging.

[18]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[19]  S. Luck.  An Introduction to the Event-Related Potential Technique , 2005 .

[20]  Keith J. Worsley,et al.  Statistical analysis of activation images , 2001 .

[21]  D. Head,et al.  Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: evidence from diffusion tensor imaging. , 2004, Cerebral cortex.

[22]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[23]  Clay B. Holroyd,et al.  Reinforcement-related brain potentials from medial frontal cortex: origins and functional significance , 2004, Neuroscience & Biobehavioral Reviews.

[24]  A. Dale,et al.  Age-related alterations in white matter microstructure measured by diffusion tensor imaging , 2005, Neurobiology of Aging.

[25]  C. Eriksen,et al.  Effects of noise letters upon the identification of a target letter in a nonsearch task , 1974 .

[26]  D. Yves von Cramon,et al.  The Role of Intact Frontostriatal Circuits in Error Processing , 2006, Journal of Cognitive Neuroscience.

[27]  D. Salat,et al.  Choice reaction time performance correlates with diffusion anisotropy in white matter pathways supporting visuospatial attention. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[28]  W. Gehring,et al.  Neural Systems for Error Monitoring , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

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

[30]  S. Wakana,et al.  Fiber tract-based atlas of human white matter anatomy. , 2004, Radiology.

[31]  C. Carter,et al.  Error Detection, Correction, and Prevention in the Brain: A Brief Review of Data and Theories , 2006, Clinical EEG and neuroscience.

[32]  J. Illes,et al.  Diffusion-tensor imaging of cognitive performance , 2002, Brain and Cognition.

[33]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[34]  J. Ford,et al.  Anatomy of an error: ERP and fMRI , 2003, Biological Psychology.

[35]  A. Engel,et al.  Trial-by-Trial Coupling of Concurrent Electroencephalogram and Functional Magnetic Resonance Imaging Identifies the Dynamics of Performance Monitoring , 2005, The Journal of Neuroscience.

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

[37]  M. O’Sullivan,et al.  Damage within a network of white matter regions underlies executive dysfunction in CADASIL , 2005, Neurology.

[38]  V. Wedeen,et al.  Diffusion MRI of Complex Neural Architecture , 2003, Neuron.

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

[40]  Jeff T. Larsen,et al.  The good, the bad and the neutral: Electrophysiological responses to feedback stimuli , 2006, Brain Research.

[41]  Denis Le Bihan,et al.  Looking into the functional architecture of the brain with diffusion MRI , 2003, Nature Reviews Neuroscience.

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

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

[44]  A. Dale,et al.  Effects of age on volumes of cortex, white matter and subcortical structures , 2005, Neurobiology of Aging.

[45]  E. Gordon,et al.  Cognitive aging, executive function, and fractional anisotropy: a diffusion tensor MR imaging study. , 2007, AJNR. American journal of neuroradiology.

[46]  M. Moseley.  Diffusion tensor imaging and aging – a review , 2002, NMR in biomedicine.

[47]  S. Segalowitz,et al.  Error detection in patients with lesions to the medial prefrontal cortex: an ERP study , 2004, Neuropsychologia.

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

[49]  T. Klingberg,et al.  Combined analysis of DTI and fMRI data reveals a joint maturation of white and grey matter in a fronto-parietal network. , 2003, Brain research. Cognitive brain research.

[50]  Steven Laureys,et al.  Cytology and functionally correlated circuits of human posterior cingulate areas , 2006, NeuroImage.

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

[52]  C. Carter,et al.  The anterior cingulate as a conflict monitor: fMRI and ERP studies , 2002, Physiology & Behavior.

[53]  S. Mori,et al.  Principles of Diffusion Tensor Imaging and Its Applications to Basic Neuroscience Research , 2006, Neuron.

[54]  A. Pfefferbaum,et al.  Diffusion tensor imaging and aging , 2006, Neuroscience & Biobehavioral Reviews.

[55]  E. Davelaar.  Conflict-monitoring and (meta)cognitive control , 2009 .

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

[57]  Myelination and Brain Electrophysiology in Healthy and Schizophrenic Individuals , 2003, Neuropsychopharmacology.

[58]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[59]  Torsten Baldeweg,et al.  Impact of frontal white matter lesions on performance monitoring: ERP evidence for cortical disconnection. , 2006, Brain : a journal of neurology.

[60]  Jonas Persson,et al.  Structure-function correlates of cognitive decline in aging. , 2006, Cerebral cortex.

[61]  H. Semlitsch,et al.  A solution for reliable and valid reduction of ocular artifacts, applied to the P300 ERP. , 1986, Psychophysiology.

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

[63]  P. Matthews,et al.  White matter abnormalities and brain activation in schizophrenia: A combined DTI and fMRI study , 2007, Schizophrenia Research.

[64]  Jonathan D. Cohen,et al.  The neural basis of error detection: conflict monitoring and the error-related negativity. , 2004, Psychological review.

[65]  H. Vankova.  Mini Mental State , 2010 .

[66]  Thomas E. Nichols,et al.  Acquisition and voxelwise analysis of multi-subject diffusion data with Tract-Based Spatial Statistics , 2007, Nature Protocols.

[67]  Petra S. Huppi,et al.  Combination of event-related fMRI and diffusion tensor imaging in an infant with perinatal stroke , 2004, NeuroImage.

[68]  Stephen M. Smith,et al.  Functional MRI : an introduction to methods , 2002 .

[69]  D. Pandya,et al.  Fiber Pathways of the Brain , 2006 .

[70]  R. Kraft,et al.  Relating imaging indices of white matter integrity and volume in healthy older adults. , 2008, Cerebral cortex.

[71]  Justin L. Vincent,et al.  Disruption of Large-Scale Brain Systems in Advanced Aging , 2007, Neuron.

[72]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[73]  D. Meyer,et al.  A Neural System for Error Detection and Compensation , 1993 .

[74]  M. Herrmann,et al.  Source localization (LORETA) of the error-related-negativity (ERN/Ne) and positivity (Pe). , 2004, Brain research. Cognitive brain research.

[75]  G. M. Halliday,et al.  White matter loss in healthy ageing: A postmortem analysis , 2009, Neurobiology of Aging.

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

[77]  Clay B. Holroyd,et al.  The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. , 2002, Psychological review.

[78]  M. O’Sullivan,et al.  White matter damage on diffusion tensor imaging correlates with age-related cognitive decline , 2006, Neurology.