Relationship between Cortical Thickness and EEG Alterations during Sleep in the Alzheimer’s Disease

Recent evidence showed that EEG activity alterations that occur during sleep are associated with structural, age-related, changes in healthy aging brains, and predict age-related decline in memory performance. Alzheimer’s disease (AD) patients show specific EEG alterations during sleep associated with cognitive decline, including reduced sleep spindles during NREM sleep and EEG slowing during REM sleep. We investigated the relationship between these EEG sleep alterations and brain structure changes in a study of 23 AD patients who underwent polysomnographic recording of their undisturbed sleep and 1.5T MRI scans. Cortical thickness measures were correlated with EEG power in the sigma band during NREM sleep and with delta- and beta-power during REM sleep. Thinning in the right precuneus correlated with all the EEG indexes considered in this study. Frontal–central NREM sigma power showed an inverse correlation with thinning of the left entorhinal cortex. Increased delta activity at the frontopolar and temporal regions was significantly associated with atrophy in some temporal, parietal, and frontal cortices, and with mean thickness of the right hemisphere. Our findings revealed an association between sleep EEG alterations and the changes to AD patients’ brain structures. Findings also highlight possible compensatory processes involving the sources of frontal–central sleep spindles.

[1]  P. Rossini,et al.  EEG alterations during wake and sleep in mild cognitive impairment and Alzheimer's disease , 2021, iScience.

[2]  M. Gorgoni,et al.  Sleep-Based Interventions in Alzheimer’s Disease: Promising Approaches from Prevention to Treatment along the Disease Trajectory , 2021, Pharmaceuticals.

[3]  O. Gosseries,et al.  Local sleep-like cortical reactivity in the awake brain after focal injury , 2019, bioRxiv.

[4]  Jens G. Klinzing,et al.  Mechanisms of systems memory consolidation during sleep , 2019, Nature Neuroscience.

[5]  M. Ferrara,et al.  Spatiotemporal Dynamics of Sleep Spindle Sources Across NREM Sleep Cycles , 2019, Front. Neurosci..

[6]  Feng Shi,et al.  Study of brain morphology change in Alzheimer’s disease and amnestic mild cognitive impairment compared with normal controls , 2019, General Psychiatry.

[7]  J. Lina,et al.  Age-related cortical signatures of human sleep electroencephalography , 2019, Neurobiology of Aging.

[8]  G. Tononi,et al.  Regional Delta Waves In Human Rapid Eye Movement Sleep , 2019, The Journal of Neuroscience.

[9]  J. Morris,et al.  Effect of sleep on overnight cerebrospinal fluid amyloid β kinetics , 2018, Annals of neurology.

[10]  Emmanuel Mignot,et al.  Slow wave sleep disruption increases cerebrospinal fluid amyloid-&bgr; levels , 2017, Brain : a journal of neurology.

[11]  M. Walker,et al.  Sleep and Human Aging , 2017, Neuron.

[12]  P. Bosco,et al.  Brain atrophy in Alzheimer’s Disease and aging , 2016, Ageing Research Reviews.

[13]  C. Babiloni,et al.  Brain neural synchronization and functional coupling in Alzheimer's disease as revealed by resting state EEG rhythms. , 2016, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[14]  N. Gosselin,et al.  Quantitative EEG of Rapid-Eye-Movement Sleep , 2016, Clinical EEG and neuroscience.

[15]  P. Rossini,et al.  Parietal Fast Sleep Spindle Density Decrease in Alzheimer's Disease and Amnesic Mild Cognitive Impairment , 2016, Journal of Neural Transplantation and Plasticity.

[16]  Alan C. Evans,et al.  Cortical Thinning Explains Changes in Sleep Slow Waves during Adulthood , 2015, The Journal of Neuroscience.

[17]  M. Walker,et al.  β-amyloid disrupts human NREM slow waves and related hippocampus-dependent memory consolidation , 2015, Nature Neuroscience.

[18]  Sonia Ancoli-Israel,et al.  Impaired prefrontal sleep spindle regulation of hippocampal-dependent learning in older adults. , 2014, Cerebral cortex.

[19]  Miranda M Lim,et al.  The sleep-wake cycle and Alzheimer's disease: what do we know? , 2014, Neurodegenerative disease management.

[20]  Sebastiaan Overeem,et al.  Effect of 1 night of total sleep deprivation on cerebrospinal fluid β-amyloid 42 in healthy middle-aged men: a randomized clinical trial. , 2014, JAMA neurology.

[21]  Daniel J. R. Christensen,et al.  Sleep Drives Metabolite Clearance from the Adult Brain , 2013, Science.

[22]  M. Walker,et al.  Prefrontal atrophy, disrupted NREM slow waves, and impaired hippocampal-dependent memory in aging , 2013, Nature Neuroscience.

[23]  Ken A Paller,et al.  Concurrent Impairments in Sleep and Memory in Amnestic Mild Cognitive Impairment , 2012, Journal of the International Neuropsychological Society.

[24]  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.

[25]  Guillén Fernández,et al.  Autobiographical memory retrieval in patients with Alzheimer's disease , 2010, NeuroImage.

[26]  Cheryl L. Grady,et al.  Altered connectivity among emotion-related brain regions during short-term memory in Alzheimer's disease , 2010, Neurobiology of Aging.

[27]  J. Whitwell Progression of Atrophy in Alzheimer’s Disease and Related Disorders , 2010, Neurotoxicity Research.

[28]  C. Jack,et al.  Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade , 2010, The Lancet Neurology.

[29]  Seiji Nishino,et al.  Amyloid-β Dynamics Are Regulated by Orexin and the Sleep-Wake Cycle , 2009, Science.

[30]  Alan C. Evans,et al.  Cortical Thickness Analysis to Detect Progressive Mild Cognitive Impairment: A Reference to Alzheimer’s Disease , 2009, Dementia and Geriatric Cognitive Disorders.

[31]  Akram Bakkour,et al.  The cortical signature of prodromal AD , 2009, Neurology.

[32]  B T Hyman,et al.  Temporoparietal MR Imaging Measures of Atrophy in Subjects with Mild Cognitive Impairment That Predict Subsequent Diagnosis of Alzheimer Disease , 2009, American Journal of Neuroradiology.

[33]  M. Albert,et al.  MRI measures of temporoparietal regions show differential rates of atrophy during prodromal AD , 2008, Neurology.

[34]  Francis Eustache,et al.  Is there a link between sleep changes and memory in Alzheimer's disease? , 2008, Neuroreport.

[35]  Nick C Fox,et al.  Amnestic Mild Cognitive Impairment: Structural MR Imaging Findings Predictive of Conversion to Alzheimer Disease , 2008, American Journal of Neuroradiology.

[36]  C. Jack,et al.  MRI patterns of atrophy associated with progression to AD in amnestic mild cognitive impairment , 2008, Neurology.

[37]  Eini Niskanen,et al.  Voxel-based morphometry to detect brain atrophy in progressive mild cognitive impairment , 2007, NeuroImage.

[38]  M. Filippi,et al.  The contribution of voxel-based morphometry in staging patients with mild cognitive impairment , 2006, Neurology.

[39]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[40]  M. Steriade,et al.  Waking-sleep modulation of paroxysmal activities induced by partial cortical deafferentation. , 2006, Cerebral cortex.

[41]  Brigitte Landeau,et al.  Using voxel-based morphometry to map the structural changes associated with rapid conversion in MCI: A longitudinal MRI study , 2005, NeuroImage.

[42]  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.

[43]  J. Gabrieli,et al.  Memory encoding in Alzheimer's disease: an fMRI study of explicit and implicit memory. , 2005, Brain : a journal of neurology.

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

[45]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[46]  M. Ferrara,et al.  Sleep spindles: an overview. , 2003, Sleep medicine reviews.

[47]  G Klösch,et al.  Low-resolution brain electromagnetic tomography revealed simultaneously active frontal and parietal sleep spindle sources in the human cortex , 2001, Neuroscience.

[48]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[49]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[50]  I Kanno,et al.  Regional correlations between the EEG and oxygen metabolism in dementia of Alzheimer's type. , 1997, Electroencephalography and clinical neurophysiology.

[51]  P. Prinz,et al.  Sleep/wake patterns In Alzheimer's disease: relationships with cognition and function , 1995, Journal of sleep research.

[52]  P N Prinz,et al.  Sleep disturbances in patients with mild-stage Alzheimer's disease. , 1990, Journal of gerontology.

[53]  M R Nuwer,et al.  Evaluation of stroke using EEG frequency analysis and topographic mapping , 1987, Neurology.

[54]  K. Nagata,et al.  Topographic electroencephalographic study with power ratio index mapping in patients with malignant brain tumors. , 1985, Neurosurgery.

[55]  M. Vitiello,et al.  Sleep, EEG and mental function changes in senile dementia of the Alzheimer's type , 1982, Neurobiology of Aging.

[56]  P. Selnes,et al.  Executive dysfunction in mild cognitive impairment is associated with changes in frontal and cingulate white matter tracts. , 2011, Journal of Alzheimer's disease : JAD.

[57]  A. Chesson,et al.  The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology, and Techinical Specifications , 2007 .

[58]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[59]  T. Nielsen,et al.  Quantitative EEG and statistical mapping of wakefulness and REM sleep in the evaluation of mild to moderate Alzheimer's disease. , 1997, European neurology.

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

[61]  B T Hyman,et al.  Entorhinal cortex pathology in Alzheimer's disease , 1991, Hippocampus.