Young Alzheimer patients show distinct regional changes of oscillatory brain dynamics

The objective of this study was to examine the differences in oscillatory brain dynamics in Alzheimer's disease (AD) according to age at onset using quantitative electroencephalography (EEG). We examined resting state electroencephalograms of 320 probable AD patients and 246 controls, both categorized into a young (≤ 65 years) and old (> 65 years) group. Relative power in 4 different frequency bands was calculated. The effect of age on global and regional relative power was examined. Globally, young AD patients showed lower alpha- and higher delta-power than old AD patients. Regional analysis showed that these differences were most pronounced in the parieto-occipital region. Young AD patients had lower beta- and higher theta-power than old patients in all but the temporal regions. In controls, there was no age effect on global relative power in any frequency band. Young AD patients present with more severe slowing of spontaneous oscillatory activity than old AD patients, which is most pronounced in the posterior brain areas. This finding supports the hypothesis that early onset AD presents with a distinct endophenotype.

[1]  R. Palmer,et al.  Modeling regional vulnerability to Alzheimer pathology , 2012, Neurobiology of Aging.

[2]  J. Lindesay,et al.  Neuropsychological performance in early and late onset Alzheimer's disease: comparisons in a memory clinic population , 2004, International journal of geriatric psychiatry.

[3]  C. Holmes,et al.  Alzheimer’s disease: differences in technetium-99m HMPAO SPECT scan findings between early onset and late onset dementia , 2003, Journal of neurology, neurosurgery, and psychiatry.

[4]  Prashanthi Vemuri,et al.  Effect of APOE ε4 status on intrinsic network connectivity in cognitively normal elderly subjects. , 2011, Archives of neurology.

[5]  L. Prichep,et al.  Quantitative EEG and Electromagnetic Brain Imaging in Aging and in the Evolution of Dementia , 2007, Annals of the New York Academy of Sciences.

[6]  Tetsuya Mori,et al.  Differences in cerebral metabolic impairment between early and late onset types of Alzheimer's disease , 2002, Journal of the Neurological Sciences.

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

[8]  K Kosaka,et al.  Quantitative EEG in patients with presenile and senile dementia of the Alzheimer type , 1994, Acta neurologica Scandinavica.

[9]  A. Cichocki,et al.  Diagnosis of Alzheimer's disease from EEG signals: where are we standing? , 2010 .

[10]  G. Rondouin,et al.  Diagnostic value of quantitative EEG in Alzheimer’s disease , 2001, Neurophysiologie Clinique/Clinical Neurophysiology.

[11]  Nick C Fox,et al.  Early-onset versus late-onset Alzheimer's disease: the case of the missing APOE ɛ4 allele , 2011, The Lancet Neurology.

[12]  Kenneth J. Pope,et al.  Thinking activates EMG in scalp electrical recordings , 2008, Clinical Neurophysiology.

[13]  Nick C Fox,et al.  The effect of APOE genotype on clinical phenotype in Alzheimer disease , 2006, Neurology.

[14]  E. I. Rogaev,et al.  EEG alterations in non-demented individuals related to apolipoprotein E genotype and to risk of Alzheimer disease , 2008, Neurobiology of Aging.

[15]  Julie S. Snowden,et al.  Cognitive Phenotypes in Alzheimer's Disease and Genetic Risk , 2007, Cortex.

[16]  V. Narayanaswami,et al.  Apolipoprotein E: from lipid transport to neurobiology. , 2011, Progress in lipid research.

[17]  P. Vitali,et al.  Quantitative EEG Changes in Alzheimer Patients during Long-Term Donepezil Therapy , 2002, Neuropsychobiology.

[18]  W. M. van der Flier,et al.  Associations between Patterns of EEG Abnormalities and Diagnosis in a Large Memory Clinic Cohort , 2008, Dementia and Geriatric Cognitive Disorders.

[19]  C. Buchpiguel,et al.  SPECT in Alzheimer's disease:features associated with bilateral parietotemporal hypoperfusion , 2000, Acta neurologica Scandinavica.

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

[21]  Clare E. Mackay,et al.  The effects of APOE on the functional architecture of the resting brain , 2012, NeuroImage.

[22]  W. Singer,et al.  Neural Synchrony in Brain Disorders: Relevance for Cognitive Dysfunctions and Pathophysiology , 2006, Neuron.

[23]  T Gasser,et al.  Quantitative EEG analysis in early onset Alzheimer's disease: correlations with severity, clinical characteristics, visual EEG and CCT. , 1994, Electroencephalography and clinical neurophysiology.

[24]  T. Gasser,et al.  Transformations towards the normal distribution of broad band spectral parameters of the EEG. , 1982, Electroencephalography and clinical neurophysiology.

[25]  Cornelis J Stam,et al.  EEG abnormalities in early and late onset Alzheimer's disease: understanding heterogeneity , 2010, Journal of Neurology, Neurosurgery & Psychiatry.

[26]  W. M. van der Flier,et al.  Differential effect of APOE genotype on amyloid load and glucose metabolism in AD dementia , 2013, Neurology.

[27]  Xiaochuan Sun,et al.  Different quantitative EEG alterations induced by TBI among patients with different APOE genotypes , 2011, Neuroscience Letters.

[28]  Alan C. Evans,et al.  Neuronal Networks in Alzheimer's Disease , 2009, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[29]  Claudio Babiloni,et al.  Individual analysis of EEG frequency and band power in mild Alzheimer's disease , 2004, Clinical Neurophysiology.

[30]  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.

[31]  P Julin,et al.  Apolipoprotein E ε4 allele decreases functional connectivity in Alzheimer’s disease as measured by EEG coherence , 1997, Journal of neurology, neurosurgery, and psychiatry.

[32]  E. Mori,et al.  Apolipoprotein E epsilon 4 and the pattern of regional brain atrophy in Alzheimer's disease. , 2001, Neurology.

[33]  G. Frisoni,et al.  Structural correlates of early and late onset Alzheimer’s disease: voxel based morphometric study , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[34]  W. M. van der Flier,et al.  CSF biomarkers in relationship to cognitive profiles in Alzheimer disease , 2009, Neurology.

[35]  Jesse A. Brown,et al.  Brain network local interconnectivity loss in aging APOE-4 allele carriers , 2011, Proceedings of the National Academy of Sciences.

[36]  M. Matousek,et al.  EEG abnormalities in dementia reflect the parietal lobe syndrome , 2001, Clinical Neurophysiology.

[37]  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.

[38]  Cornelis J. Stam,et al.  EEG functional connectivity and ApoE genotype in Alzheimer’s disease and controls , 2008, Clinical Neurophysiology.

[39]  Dietrich Lehmann,et al.  Rivastigmine effects on EEG spectra and three-dimensional LORETA functional imaging in Alzheimer’s disease , 2008, Psychopharmacology.

[40]  Martin Klein,et al.  Cognitive Impairment in Alzheimer’s Disease Is Modified by APOE Genotype , 2007, Dementia and Geriatric Cognitive Disorders.

[41]  H. Berendse,et al.  Cognitive decline in Parkinson's disease is associated with slowing of resting-state brain activity: a longitudinal study , 2013, Neurobiology of Aging.

[42]  E. Whitham,et al.  Scalp electrical recording during paralysis: Quantitative evidence that EEG frequencies above 20Hz are contaminated by EMG , 2007, Clinical Neurophysiology.

[43]  Masayuki Matsuda,et al.  Four subgroups of Alzheimer's disease based on patterns of atrophy using VBM and a unique pattern for early onset disease , 2006, NeuroImage.

[44]  Cornelis J Stam,et al.  Resting-State Oscillatory Brain Dynamics in Alzheimer Disease , 2008, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[45]  F H Duffy,et al.  Brain electrical activity in patients with presenile and senile dementia of the Alzheimer type , 1984, Annals of neurology.

[46]  M. Mendez,et al.  Positron Emission Tomography Facilitates Diagnosis of Early-Onset Alzheimer’s Disease , 2007, European Neurology.

[47]  M. Greicius,et al.  Presenile dementia syndromes: an update on taxonomy and diagnosis , 2002, Journal of neurology, neurosurgery, and psychiatry.

[48]  Juhani Partanen,et al.  Spectral analysis of EEG in Alzheimer's disease: Relation to apolipoprotein E polymorphism , 1996, Neurobiology of Aging.

[49]  G. Baal,et al.  Twin and family studies of the human electroencephalogram: a review and a meta-analysis , 2002, Biological Psychology.

[50]  M. Mendez,et al.  Cognitive Differences between Early- and Late-Onset Alzheimer's Disease , 2007, American journal of Alzheimer's disease and other dementias.

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

[52]  P. Rossini,et al.  Reactivity of cortical alpha rhythms to eye opening in mild cognitive impairment and Alzheimer's disease: an EEG study. , 2011, Journal of Alzheimer's disease : JAD.

[53]  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.

[54]  K. Bales.  Brain lipid metabolism, apolipoprotein E and the pathophysiology of Alzheimer's disease , 2010, Neuropharmacology.

[55]  Sue J. Kang,et al.  Glucose metabolism in early onset versus late onset Alzheimer's disease: an SPM analysis of 120 patients. , 2005, Brain : a journal of neurology.

[56]  Vladimir V. Frolkis,et al.  Neurobiology of Aging , 2019, Psychobiology of Behaviour.

[57]  Martin Klein,et al.  Precuneus atrophy in early-onset Alzheimer’s disease: a morphometric structural MRI study , 2007, Neuroradiology.

[58]  Hiroaki Kazui,et al.  Apolipoprotein E ε4 and the pattern of regional brain atrophy in Alzheimer’s disease , 2001, Neurology.

[59]  A. Hofman,et al.  Risk estimates of dementia by apolipoprotein E genotypes from a population-based incidence study: the Rotterdam Study. , 1998, Archives of neurology.

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

[61]  A D Roses,et al.  Apolipoprotein E and Alzheimer disease. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[62]  F. Angeleri,et al.  EEG power spectrum differences in early and late onset forms of Alzheimer's disease , 1999, Clinical Neurophysiology.

[63]  B. Seltzer,et al.  A comparison of clinical features in early- and late-onset primary degenerative dementia. One entity or two? , 1983, Archives of neurology.

[64]  M. Weiner,et al.  Increased metabolic vulnerability in early-onset Alzheimer's disease is not related to amyloid burden. , 2010, Brain : a journal of neurology.

[65]  F. Collette,et al.  Alzheimer' Disease as a Disconnection Syndrome? , 2003, Neuropsychology Review.

[66]  Wiesje M van der Flier,et al.  Early-versus late-onset Alzheimer's disease: more than age alone. , 2010, Journal of Alzheimer's disease : JAD.

[67]  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.