MEG spectral analysis in subtypes of mild cognitive impairment

Mild cognitive impairment (MCI) has been described as an intermediate stage between normal aging and dementia. Previous studies characterized the alterations of brain oscillatory activity at this stage, but little is known about the differences between single and multidomain amnestic MCI patients. In order to study the patterns of oscillatory magnetic activity in amnestic MCI subtypes, a total of 105 subjects underwent an eyes-closed resting-state magnetoencephalographic recording: 36 healthy controls, 33 amnestic single domain MCIs (a-sd-MCI), and 36 amnestic multidomain MCIs (a-md-MCI). Relative power values were calculated and compared among groups. Subsequently, relative power values were correlated with neuropsychological tests scores and hippocampal volumes. Both MCI groups showed an increase in relative power in lower frequency bands (delta and theta frequency ranges) and a decrease in power values in higher frequency bands (alpha and beta frequency ranges), as compared with the control group. More importantly, clear differences emerged from the comparison between the two amnestic MCI subtypes. The a-md-MCI group showed a significant power increase within delta and theta ranges and reduced relative power within alpha and beta ranges. Such pattern correlated with the neuropsychological performance, indicating that the a-md-MCI subtype is associated not only with a “slowing” of the spectrum but also with a poorer cognitive status. These results suggest that a-md-MCI patients are characterized by a brain activity profile that is closer to that observed in Alzheimer disease. Therefore, it might be hypothesized that the likelihood of conversion to dementia would be higher within this subtype.

[1]  F. Kruggel,et al.  Theta-power Differences in Patients with Mild Cognitive Impairment Under Rest Condition and During Haptic Tasks , 2002, Alzheimer disease and associated disorders.

[2]  Roberto Hornero,et al.  Quantitative Magnetoencephalography of Spontaneous Brain Activity in Alzheimer Disease: An Exhaustive Frequency Analysis , 2006, Alzheimer disease and associated disorders.

[3]  M. D. Ernst Permutation Methods: A Basis for Exact Inference , 2004 .

[4]  Sara Rosenblum,et al.  Neuropsychological prediction of conversion to Alzheimer disease in patients with mild cognitive impairment. , 2006, Archives of general psychiatry.

[5]  M. Lawton,et al.  Assessment of Older People: Self-Maintaining and Instrumental Activities of Daily Living , 1969 .

[6]  D. Amaral,et al.  Hippocampal‐neocortical interaction: A hierarchy of associativity , 2000, Hippocampus.

[7]  B. Reisberg,et al.  The Global Deterioration Scale for assessment of primary degenerative dementia. , 1982, The American journal of psychiatry.

[8]  W. Jagust,et al.  Degree of discrepancy between self and other‐reported everyday functioning by cognitive status: dementia, mild cognitive impairment, and healthy elders , 2005, International journal of geriatric psychiatry.

[9]  Alberto Fernández,et al.  Magnetoencephalographic parietal delta dipole density in mild cognitive impairment: preliminary results of a method to estimate the risk of developing Alzheimer disease. , 2006, Archives of neurology.

[10]  J. Peña-Casanova PROGRAMA INTEGRADO DE EXPLORACIÓN NEUROPSICOLÓGICA - TEST BARCELONA: BASES TEÓRICAS, OBJETIVOS Y CONTENIDOS , 1991 .

[11]  Claudio Babiloni,et al.  Apolipoprotein E and alpha brain rhythms in mild cognitive impairment: A multicentric Electroencephalogram study , 2006, Annals of neurology.

[12]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[13]  P. Campo,et al.  Increased biomagnetic activity in the ventral pathway in mild cognitive impairment , 2008, Clinical Neurophysiology.

[14]  D. Bennett,et al.  Entorhinal cortex beta-amyloid load in individuals with mild cognitive impairment. , 1999, Experimental neurology.

[15]  K. Herholz,et al.  Cholinergic system function and cognition in mild cognitive impairment , 2012, Neurobiology of Aging.

[16]  C. Jack,et al.  Patterns of atrophy differ among specific subtypes of mild cognitive impairment. , 2007, Archives of neurology.

[17]  P. Scheltens,et al.  Advances in the early detection of Alzheimer's disease , 2004, Nature Reviews Neuroscience.

[18]  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.

[19]  M. Yassuda,et al.  Diagnosis of Mild Cognitive Impairment Revisited after One Year , 2009, Dementia and Geriatric Cognitive Disorders.

[20]  P. Sachdev,et al.  Gray matter atrophy patterns of mild cognitive impairment subtypes , 2012, Journal of the Neurological Sciences.

[21]  R. Tate,et al.  The Behavioural Assessment of the Dysexecutive Syndrome (BADS): Ecological, Concurrent and Construct Validity , 2000 .

[22]  Jeffrey A. James,et al.  Amyloid imaging in mild cognitive impairment subtypes , 2009, Annals of neurology.

[23]  A. Lobo,et al.  [Cognocitive mini-test (a simple practical test to detect intellectual changes in medical patients)]. , 1979, Actas luso-espanolas de neurologia, psiquiatria y ciencias afines.

[24]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[25]  A. Nordberg,et al.  Quantitative electroencephalography in mild cognitive impairment: longitudinal changes and possible prediction of Alzheimer’s disease , 2000, Neurobiology of Aging.

[26]  C. Jack,et al.  Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment , 1999, Neurology.

[27]  J. Price,et al.  Mild cognitive impairment represents early-stage Alzheimer disease. , 2001, Archives of neurology.

[28]  Dong Young Lee,et al.  Predictive validity and diagnostic stability of mild cognitive impairment subtypes , 2012, Alzheimer's & Dementia.

[29]  J. Olmos,et al.  Programa integrado de exploración neuropsicológica — test barcelona: validez de contenidos , 1991 .

[30]  J. Morris,et al.  Current concepts in mild cognitive impairment. , 2001, Archives of neurology.

[31]  P. Rossini,et al.  Cortical sources of resting EEG rhythms in mild cognitive impairment and subjective memory complaint , 2010, Neurobiology of Aging.

[32]  E. R. John,et al.  Quantitative EEG correlates of cognitive deterioration in the elderly , 1994, Neurobiology of Aging.

[33]  C. Ghetti,et al.  Differential Patterns of Hypoperfusion in Subtypes of Mild Cognitive Impairment , 2008, The open neuroimaging journal.

[34]  Jyrki Ahveninen,et al.  Source estimation of spontaneous MEG oscillations in mild cognitive impairment , 2006, Neuroscience Letters.

[35]  L. Beckett,et al.  Entorhinal Cortex β-Amyloid Load in Individuals with Mild Cognitive Impairment , 1999, Experimental Neurology.

[36]  E G Tangalos,et al.  Mild cognitive impairment. When is it a precursor to Alzheimer's disease? , 2000, Geriatrics.

[37]  Claudio Del Percio,et al.  Frontal white matter volume and delta EEG sources negatively correlate in awake subjects with mild cognitive impairment and Alzheimer's disease , 2006, Clinical Neurophysiology.

[38]  C. Jack,et al.  Mild cognitive impairment – beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment , 2004, Journal of internal medicine.

[39]  H. Amièva,et al.  Incidence and outcome of mild cognitive impairment in a population-based prospective cohort , 2002, Neurology.

[40]  Osborne Rt,et al.  Variations in graduate record examination performance by age and sex. , 1954 .

[41]  E. R. John,et al.  Prediction of longitudinal cognitive decline in normal elderly with subjective complaints using electrophysiological imaging , 2006, Neurobiology of Aging.

[42]  R. Reitan Validity of the Trail Making Test as an Indicator of Organic Brain Damage , 1958 .

[43]  Nick C Fox,et al.  The Diagnosis of Mild Cognitive Impairment due to Alzheimer’s Disease: Recommendations from the National Institute on Aging-Alzheimer’s Association Workgroups on Diagnostic Guidelines for Alzheimer’s Disease , 2011 .

[44]  J. Morris,et al.  The diagnosis of dementia due to Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer's disease , 2011, Alzheimer's & Dementia.

[45]  R. Katzman.,et al.  Pathological verification of ischemic score in differentiation of dementias , 1980, Annals of neurology.

[46]  Roberto Hornero,et al.  MEG spectral profile in Alzheimer's disease and mild cognitive impairment , 2006, Clinical Neurophysiology.

[47]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[48]  Claudio Del Percio,et al.  Mapping distributed sources of cortical rhythms in mild Alzheimer's disease. A multicentric EEG study , 2004, NeuroImage.

[49]  Jing He,et al.  Differences in brain volume, hippocampal volume, cerebrovascular risk factors, and apolipoprotein E4 among mild cognitive impairment subtypes. , 2009, Archives of neurology.

[50]  V. Leirer,et al.  Development and validation of a geriatric depression screening scale: a preliminary report. , 1982, Journal of psychiatric research.

[51]  E. Kaplan,et al.  The Boston naming test , 2001 .

[52]  Claudio Del Percio,et al.  Sources of cortical rhythms change as a function of cognitive impairment in pathological aging: a multicenter study , 2006, Clinical Neurophysiology.

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

[54]  R. Petersen Mild cognitive impairment as a diagnostic entity , 2004, Journal of internal medicine.

[55]  J. Schneider,et al.  Mild cognitive impairment is related to Alzheimer disease pathology and cerebral infarctions , 2005, Neurology.

[56]  B. Agrell,et al.  Clock Drawing Test , 2013 .

[57]  E. Tangalos,et al.  Mild Cognitive Impairment Clinical Characterization and Outcome , 1999 .

[58]  R. Petersen Mild cognitive impairment: where are we? , 2005, Alzheimer disease and associated disorders.

[59]  Nick C Fox,et al.  Revising the definition of Alzheimer's disease: a new lexicon , 2010, The Lancet Neurology.

[60]  B. Reisberg,et al.  The GDS/FAST Staging System , 1997, International Psychogeriatrics.

[61]  Alberto Fernández,et al.  MEG delta mapping along the healthy aging-Alzheimer's disease continuum: diagnostic implications. , 2013, Journal of Alzheimer's disease : JAD.

[62]  P. Sachdev,et al.  Mild cognitive impairment in a community sample: The Sydney Memory and Ageing Study , 2013, Alzheimer's & Dementia.

[63]  Paolo Vitali,et al.  EEG spectral profile to stage Alzheimer's disease , 1999, Clinical Neurophysiology.

[64]  M. Folstein,et al.  Clinical diagnosis of Alzheimer's disease , 1984, Neurology.

[65]  J. G. van Dijk,et al.  EEG correlates in the spectrum of cognitive decline , 2007, Clinical Neurophysiology.

[66]  Andrzej Cichocki,et al.  Slowing and Loss of Complexity in Alzheimer's EEG: Two Sides of the Same Coin? , 2011, International journal of Alzheimer's disease.

[67]  Alberto Fernández,et al.  Correlations of hippocampal atrophy and focal low-frequency magnetic activity in Alzheimer disease: volumetric MR imaging-magnetoencephalographic study. , 2003, AJNR. American journal of neuroradiology.

[68]  Charles D. Smith,et al.  Evidence that volume of anterior medial temporal lobe is reduced in seniors destined for mild cognitive impairment , 2010, Neurobiology of Aging.

[69]  Fernando Maestú,et al.  Functional connectivity in mild cognitive impairment during a memory task: implications for the disconnection hypothesis. , 2010, Journal of Alzheimer's disease : JAD.

[70]  B. W van Dijk,et al.  Magnetoencephalographic analysis of cortical activity in Alzheimer's disease: a pilot study , 2000, Clinical Neurophysiology.

[71]  Ole Jensen,et al.  Altered generation of spontaneous oscillations in Alzheimer's disease , 2005, NeuroImage.

[72]  T. Kurosaki,et al.  Measurement of functional activities in older adults in the community. , 1982, Journal of gerontology.

[73]  M. Albert,et al.  Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD , 2005, Neurology.

[74]  Jaeseung Jeong EEG dynamics in patients with Alzheimer's disease , 2004, Clinical Neurophysiology.

[75]  Massimo Buscema,et al.  Is it possible to automatically distinguish resting EEG data of normal elderly vs. mild cognitive impairment subjects with high degree of accuracy? , 2008, Clinical Neurophysiology.

[76]  Claudio Babiloni,et al.  Hippocampal volume and cortical sources of EEG alpha rhythms in mild cognitive impairment and Alzheimer disease , 2009, NeuroImage.

[77]  T Dierks,et al.  Discrimination of Alzheimer's disease and mild cognitive impairment by equivalent EEG sources: a cross-sectional and longitudinal study , 2000, Clinical Neurophysiology.

[78]  E. Duchesnay,et al.  Longitudinal brain metabolic changes from amnestic Mild Cognitive Impairment to Alzheimer's disease , 2009, NeuroImage.

[79]  C. Jack,et al.  Mild cognitive impairment can be distinguished from Alzheimer disease and normal aging for clinical trials. , 2004, Archives of neurology.

[80]  A. Wallin,et al.  Two-year outcome of MCI subtypes and aetiologies in the Göteborg MCI study , 2009, Journal of Neurology, Neurosurgery & Psychiatry.

[81]  R. Petersen MILD COGNITIVE IMPAIRMENT , 2004, Lancet.

[82]  B. Winblad,et al.  Clinical trials in mild cognitive impairment: lessons for the future , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[83]  B. Rockstroh,et al.  Focal temporoparietal slow activity in Alzheimer’s disease revealed by magnetoencephalography , 2002, Biological Psychiatry.

[84]  W. J. Riedel,et al.  ALZHEIMER’S DISEASE AND RELATED DISORDERS- ORIGINAL ARTICLE Increased EEG gamma band activity in Alzheimer’s disease and mild cognitive impairment , 2022 .

[85]  S. Taulu,et al.  Presentation of electromagnetic multichannel data: The signal space separation method , 2005 .

[86]  O Almkvist,et al.  Quantitative electroencephalography power and coherence in Alzheimer's disease and mild cognitive impairment. , 1996, Dementia.