Demyelination of superficial white matter in early Alzheimer's disease: a magnetization transfer imaging study

Assuming selective vulnerability of short association U-fibers in early Alzheimer's disease (AD), we quantified demyelination of the surface white matter (dSWM) with magnetization transfer ratio (MTR) in 15 patients (Clinical Dementia Rating Scale [CDR] 0.5-1; Functional Assessment Staging [FAST]: 3-4) compared with 15 controls. MTRs were computed for 39 areas in each hemisphere. We found a bilateral MTR decrease in the temporal, cingulate, parietal, and prefrontal areas. With linear discriminant analysis, we successfully classified all the participants with 3 variates including the cuneus, parahippocampal, and superior temporal regions of the left hemisphere. The pattern of dSWM changed with the age of AD onset. In early onset patients, we found bilateral posterior demyelination spreading to the temporal areas in the left hemisphere. The late onset patients showed a distributed bilateral pattern with the temporal and cingulate areas strongly affected. A correlation with Mini Mental State Examination (MMSE), Lexis, and memory tests revealed the dSWM impact on cognition. A specific landscape of dSWM in early AD shows the potential of MTR imaging as an in vivo biomarker superior to currently used techniques.

[1]  W. Le,et al.  Hypoxia increases Aβ generation by altering β- and γ-cleavage of APP , 2009, Neurobiology of Aging.

[2]  R I Grossman,et al.  Quantitative volumetric magnetization transfer analysis in multiple sclerosis: Estimation of macroscopic and microscopic disease burden , 1996, Magnetic resonance in medicine.

[3]  M. O’Sullivan,et al.  Activate your online subscription , 2001, Neurology.

[4]  M. Bronskill,et al.  Characterizing white matter with magnetization transfer and T2 , 1999, Magnetic resonance in medicine.

[5]  C D Frith,et al.  The functional roles of prefrontal cortex in episodic memory. II. Retrieval. , 1998, Brain : a journal of neurology.

[6]  M Cercignani,et al.  Reproducibility of magnetization transfer ratio histogram-derived measures of the brain in healthy volunteers. , 2000, AJNR. American journal of neuroradiology.

[7]  A. Auchus,et al.  Diffusion Tensor Imaging of Normal Appearing White Matter and Its Correlation with Cognitive Functioning in Mild Cognitive Impairment and Alzheimer's Disease , 2007, Annals of the New York Academy of Sciences.

[8]  G. Frisoni,et al.  In vivo mapping of amyloid toxicity in Alzheimer disease , 2009, Neurology.

[9]  A. Schüz.  Cortical areas : unity and diversity , 2002 .

[10]  R. Cabeza,et al.  Neural bases of learning and memory: functional neuroimaging evidence , 2000, Current opinion in neurology.

[11]  Alan C. Evans,et al.  Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. , 1996, Cerebral cortex.

[12]  M Cercignani,et al.  Magnetisation transfer ratio and mean diffusivity of normal appearing white and grey matter from patients with multiple sclerosis , 2001, Journal of neurology, neurosurgery, and psychiatry.

[13]  H. Olofsen,et al.  Lobar Distribution of Changes in Gray Matter and White Matter in Memory Clinic Patients: Detected Using Magnetization Transfer Imaging , 2007, American Journal of Neuroradiology.

[14]  P. Lachenbruch.  Statistical Power Analysis for the Behavioral Sciences (2nd ed.) , 1989 .

[15]  F. Barkhof,et al.  Patterns of lesion development in multiple sclerosis: longitudinal observations with T1-weighted spin-echo and magnetization transfer MR. , 1998, AJNR. American journal of neuroradiology.

[16]  A. Wunderlich,et al.  Subjective memory complaints: Objective neural markers in patients with Alzheimer's disease and major depressive disorder , 2002, Annals of neurology.

[17]  J L Andersson,et al.  Brain regions associated with episodic retrieval in normal aging and Alzheimer’s disease , 1999, Neurology.

[18]  Udo Rüb,et al.  Vulnerability of cortical neurons to Alzheimer's and Parkinson's diseases. , 2006, Journal of Alzheimer's disease : JAD.

[19]  P. Yakovlev,et al.  The myelogenetic cycles of regional maturation of the brain , 1967 .

[20]  B. Reisberg,et al.  Functional Assessment Staging (FAST) in Alzheimer's Disease: Reliability, Validity, and Ordinality , 1992, International Psychogeriatrics.

[21]  H. Kinney,et al.  Sequence of Central Nervous System Myelination in Human Infancy. II. Patterns of Myelination in Autopsied Infants , 1988, Journal of neuropathology and experimental neurology.

[22]  Marie-Claude Potier,et al.  Classification and basic pathology of Alzheimer disease , 2009, Acta Neuropathologica.

[23]  Fumitaka Kimura,et al.  Myelination and Isochronicity in Neural Networks , 2009, Front. Neuroanat..

[24]  R. Fields,et al.  Myelination: An Overlooked Mechanism of Synaptic Plasticity? , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[25]  J. Morrison,et al.  Stereologic analysis of neurofibrillary tangle formation in prefrontal cortex area 9 in aging and Alzheimer’s disease , 2003, Neuroscience.

[26]  R. Benedict,et al.  Regional Specificity of Magnetization Transfer Imaging in Multiple Sclerosis , 2008, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[27]  Faith M. Gunning-Dixon,et al.  Aging of cerebral white matter: a review of MRI findings , 2009, International journal of geriatric psychiatry.

[28]  T. J. Crow,et al.  Minicolumnar structure in Heschl’s gyrus and planum temporale: Asymmetries in relation to sex and callosal fiber number , 2006, Neuroscience.

[29]  Benjamin J. Shannon,et al.  Molecular, Structural, and Functional Characterization of Alzheimer's Disease: Evidence for a Relationship between Default Activity, Amyloid, and Memory , 2005, The Journal of Neuroscience.

[30]  Osamu Abe,et al.  Diffusion abnormality in the posterior cingulum and hippocampal volume: correlation with disease progression in Alzheimer's disease. , 2009, Magnetic resonance imaging.

[31]  H. Braak,et al.  Development of Alzheimer-related neurofibrillary changes in the neocortex inversely recapitulates cortical myelogenesis , 1996, Acta Neuropathologica.

[32]  Hongkeun Kim,et al.  Common and specific brain regions in high- versus low-confidence recognition memory , 2009, Brain Research.

[33]  Jim Mintz,et al.  Human brain myelination and amyloid beta deposition in Alzheimer’s disease , 2007, Alzheimer's & Dementia.

[34]  B. Reisberg.  Functional assessment staging (FAST). , 1988, Psychopharmacology bulletin.

[35]  M. Folstein,et al.  Clinical diagnosis of Alzheimer's disease: Report of the NINCDS—ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease , 2011, Neurology.

[36]  G. Stebbins,et al.  Diffusion Tensor Imaging in Alzheimer’s Disease and Mild Cognitive Impairment , 2009, Behavioural neurology.

[37]  S. Schoenberg,et al.  White matter damage in Alzheimer disease and mild cognitive impairment: assessment with diffusion-tensor MR imaging and parallel imaging techniques. , 2007, Radiology.

[38]  Jacob Cohen.  Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[39]  Reto Meuli,et al.  Topography of EEG multivariate phase synchronization in early Alzheimer's disease , 2010, Neurobiology of Aging.

[40]  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.

[41]  Arthur W. Toga,et al.  Atlas-based whole brain white matter analysis using large deformation diffeomorphic metric mapping: Application to normal elderly and Alzheimer's disease participants , 2009, NeuroImage.

[42]  G. Bartzokis.  Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer’s disease , 2004, Neurobiology of Aging.

[43]  M. van Buchem,et al.  Detection of cerebral involvement in patients with active neuropsychiatric systemic lupus erythematosus by the use of volumetric magnetization transfer imaging. , 2000, Arthritis and rheumatism.

[44]  Nina Kraus,et al.  Relating Structure to Function: Heschl's Gyrus and Acoustic Processing , 2009, The Journal of Neuroscience.

[45]  H. Buschke,et al.  Genuine memory deficits in dementia , 1987 .

[46]  Michael Hull,et al.  Patterns of Regional Brain Hypometabolism Associated with Knowledge of Semantic Features and Categories in Alzheimer's Disease , 2006, Journal of Cognitive Neuroscience.

[47]  Patrick R Hof,et al.  Life and death of neurons in the aging cerebral cortex. , 2007, International review of neurobiology.

[48]  Cecilia Parazzini,et al.  Terminal zones of myelination: MR evaluation of children aged 20-40 months. , 2002, AJNR. American journal of neuroradiology.

[49]  S. Rose,et al.  Gray and white matter changes in Alzheimer's disease: A diffusion tensor imaging study , 2008, Journal of magnetic resonance imaging : JMRI.

[50]  G. Scotti,et al.  Quantification of tissue damage in AD using diffusion tensor and magnetization transfer MRI , 2001, Neurology.

[51]  H. Damasio,et al.  Humans and great apes share a large frontal cortex , 2002, Nature Neuroscience.

[52]  H. Braak,et al.  Neuropathology and Cognitive Impairment in Alzheimer Disease: A Complex but Coherent Relationship , 2009, Journal of neuropathology and experimental neurology.

[53]  J. Baron,et al.  The neural substrates of memory systems impairment in Alzheimer's disease. A PET study of resting brain glucose utilization. , 1998, Brain : a journal of neurology.

[54]  K. Ishii,et al.  Voxel-based morphometric comparison between early- and late-onset mild Alzheimer's disease and assessment of diagnostic performance of z score images. , 2005, AJNR. American journal of neuroradiology.

[55]  Charles D. Smith,et al.  Alzheimer's-type neuropathology in the precuneus is not increased relative to other areas of neocortex across a range of cognitive impairment , 2009, Neuroscience Letters.

[56]  F. Craik,et al.  Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[57]  K. Ishii,et al.  Neuronal Substrates for Semantic Memory: A Positron Emission Tomography Study in Alzheimer’s Disease , 2000, Dementia and Geriatric Cognitive Disorders.

[58]  A. Song,et al.  Cerebral White Matter Integrity and Cognitive Aging: Contributions from Diffusion Tensor Imaging , 2009, Neuropsychology Review.

[59]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[60]  D. Bennett,et al.  White matter changes in mild cognitive impairment and AD: A diffusion tensor imaging study , 2006, Neurobiology of Aging.

[61]  Francis Eustache,et al.  The Functional Neuroanatomy of Episodic Memory: The Role of the Frontal Lobes, the Hippocampal Formation, and Other Areas , 1998, NeuroImage.

[62]  Seong Jin Cho,et al.  Multitracer PET imaging of amyloid plaques and neurofibrillary tangles in Alzheimer's disease , 2008, NeuroImage.

[63]  L. Hugonot-Diener,et al.  [Presentation by the GRECO group of the French adaptation of a cognitive assessment scale used in Alzheimer type dementia]. , 1996, Presse medicale.

[64]  A. Toga,et al.  Tracking Alzheimer's Disease , 2007, Annals of the New York Academy of Sciences.

[65]  Brent A. Vogt,et al.  Multivariate Analysis of Laminar Patterns of Neurodegeneration in Posterior Cingulate Cortex in Alzheimer's Disease , 1998, Experimental Neurology.

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

[67]  Matthias J. Müller,et al.  Functional relevant loss of long association fibre tracts integrity in early Alzheimer's disease , 2008, Neuropsychologia.

[68]  C. Duffy,et al.  White matter integrity linked to functional impairments in aging and early Alzheimer's disease , 2008, Alzheimer's & Dementia.

[69]  Braitenberg,et al.  The Human Cortical White Matter: Quantitative Aspects of Cortico-Cortical Long-Range Connectivity , 2002 .

[70]  Marco Rovaris,et al.  Conventional and magnetization transfer MRI predictors of clinical multiple sclerosis evolution: a medium-term follow-up study. , 2003, Brain : a journal of neurology.

[71]  John G. Sled,et al.  Magnetization Transfer Ratio in Mild Cognitive Impairment and Dementia of Alzheimer's Type , 2002, NeuroImage.

[72]  A. Minkowski,et al.  Regional Development of the Brain in Early Life , 1968 .

[73]  Takashi Yoshiura,et al.  Diffusion tensor in posterior cingulate gyrus: correlation with cognitive decline in Alzheimer's disease , 2002, Neuroreport.

[74]  Seth Love,et al.  Long-term effects of Aβ42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial , 2008, The Lancet.

[75]  Malou M-Louise Haine,et al.  De Wilde V. , 1986 .

[76]  Kiralee M. Hayashi,et al.  The topography of grey matter involvement in early and late onset Alzheimer's disease. , 2007, Brain : a journal of neurology.

[77]  Lawrence R. Frank,et al.  Decreased white matter integrity in late-myelinating fiber pathways in Alzheimer's disease supports retrogenesis , 2009, NeuroImage.

[78]  Florence Rémy,et al.  Verbal episodic memory impairment in Alzheimer's disease: a combined structural and functional MRI study , 2005, NeuroImage.

[79]  H. Seldon.  Structure of human auditory cortex. I. Cytoarchitectonics and dendritic distributions , 1981, Brain Research.

[80]  M. Moscovitch,et al.  The parietal cortex and episodic memory: an attentional account , 2008, Nature Reviews Neuroscience.

[81]  W. M. van der Flier,et al.  Magnetization transfer imaging in normal aging, mild cognitive impairment, and Alzheimer's disease , 2002, Annals of neurology.

[82]  Wei Wen,et al.  The topography of white matter hyperintensities on brain MRI in healthy 60- to 64-year-old individuals , 2004, NeuroImage.

[83]  Shigeo Abe DrEng.  Pattern Classification , 2001, Springer London.

[84]  David G. Stork,et al.  Pattern Classification , 1973 .

[85]  Marie-Pierre de Partz de Courtray,et al.  Lexis. Tests pour le diagnostic des troubles lexicaux chez le patient aphasique , 2001 .

[86]  Hilkka Soininen,et al.  Diffusion tensor imaging and Tract-Based Spatial Statistics in Alzheimer's disease and mild cognitive impairment , 2011, Neurobiology of Aging.

[87]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.