Resting-state posterior alpha rhythms are abnormal in subjective memory complaint seniors with preclinical Alzheimer's neuropathology and high education level: the INSIGHT-preAD study

Claudio Babiloni; Susanna Lopez; Claudio Del Percio; Giuseppe Noce; Maria Teresa Pascarelli; Roberta Lizio; Stefan J Teipel; Gabriel González-Escamilla; Hovagim Bakardjian; Nathalie George; Enrica Cavedo; Simone Lista; Patrizia Andrea Chiesa; Andrea Vergallo; Pablo Lemercier; Giuseppe Spinelli; Michel J Grothe; Marie-Claude Potier; Fabrizio Stocchi; Raffaele Ferri; Marie-Odile Habert; Francisco J Fraga; Bruno Dubois; Harald Hampel; INSIGHT-preAD Study Group

doi:10.1016/j.neurobiolaging.2020.01.012

Resting-state posterior alpha rhythms are abnormal in subjective memory complaint seniors with preclinical Alzheimer's neuropathology and high education level: the INSIGHT-preAD study

Neurobiol Aging. 2020 Jun:90:43-59. doi: 10.1016/j.neurobiolaging.2020.01.012. Epub 2020 Feb 1.

Authors

Claudio Babiloni¹, Susanna Lopez², Claudio Del Percio³, Giuseppe Noce⁴, Maria Teresa Pascarelli⁵, Roberta Lizio⁴, Stefan J Teipel⁶, Gabriel González-Escamilla⁷, Hovagim Bakardjian⁸, Nathalie George⁹, Enrica Cavedo¹⁰, Simone Lista¹⁰, Patrizia Andrea Chiesa¹⁰, Andrea Vergallo¹¹, Pablo Lemercier¹⁰, Giuseppe Spinelli⁸, Michel J Grothe¹², Marie-Claude Potier¹³, Fabrizio Stocchi¹⁴, Raffaele Ferri⁵, Marie-Odile Habert¹⁵, Francisco J Fraga¹⁶, Bruno Dubois⁸, Harald Hampel¹¹; INSIGHT-preAD Study Group

Affiliations

¹ Department of Physiology and Pharmacology "Erspamer", Sapienza University of Rome, Rome, Italy; Hospital San Raffaele Cassino, Cassino, FR, Italy. Electronic address: claudio.babiloni@uniroma1.it.
² Department of Physiology and Pharmacology "Erspamer", Sapienza University of Rome, Rome, Italy; Department of Emergency and Organ Transplantation - Nephrology, Dialysis and Transplantation Unit, Aldo Moro University of Bari, Bari, Italy.
³ Department of Physiology and Pharmacology "Erspamer", Sapienza University of Rome, Rome, Italy.
⁴ IRCCS SDN, Naples, Italy.
⁵ Oasi Research Institute - IRCCS, Troina, Italy.
⁶ Department of Psychosomatic Medicine, University of Rostock, Rostock, Germany; German Center for Neurodegenerative Diseases (DZNE) - Rostock/Greifswald, Rostock, Germany.
⁷ Department of Neurology, Focus Program Translational Neuroscience (FTN), Rhine-Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.
⁸ Department of Neurology, Institute of Memory and Alzheimer's Disease (IM2A), Pitié-Salpêtrière Hospital, Paris, France; Institut du Cerveau et de la Moelle épinière, ICM, INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France.
⁹ Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Centre de NeuroImagerie de Recherche, CENIR, Centre MEG-EEG, Paris, France.
¹⁰ Department of Neurology, Institute of Memory and Alzheimer's Disease (IM2A), Pitié-Salpêtrière Hospital, Paris, France; Institut du Cerveau et de la Moelle épinière, ICM, INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; GRC n° 21, Alzheimer Precision Medicine (APM), AP-HP, Pitié-Salpêtrière Hospital, Sorbonne University, Paris, France.
¹¹ GRC n° 21, Alzheimer Precision Medicine (APM), AP-HP, Pitié-Salpêtrière Hospital, Sorbonne University, Paris, France.
¹² German Center for Neurodegenerative Diseases (DZNE) - Rostock/Greifswald, Rostock, Germany.
¹³ Institut du Cerveau et de la Moelle épinière, ICM, INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France.
¹⁴ IRCCS San Raffaele Pisana, Rome, Italy.
¹⁵ Centre pour l'Acquisition et le Traitement des Images, (CATI platform), Paris, France; Laboratoire d'Imagerie Biomédicale, CNRS, INSERM, Sorbonne University, Paris, France; Department of Nuclear Medicine, AP-HP, Pitié-Salpêtrière Hospital, Paris, France.
¹⁶ CECS - Engineering, Modelling and Applied Social Sciences Center, Federal University of ABC (UFABC), Santo Andre, SP, Brazil.

PMID: 32111391
DOI: 10.1016/j.neurobiolaging.2020.01.012

Abstract

Cognitive reserve is present in Alzheimer's disease (AD) seniors with high education attainment making them clinically resilient to extended brain neuropathology and neurodegeneration. Here, we tested whether subjective memory complaint (SMC) seniors with AD neuropathology and high education attainment of the prospective INSIGHT-preAD cohort (Paris) may present abnormal eyes-closed resting state posterior electroencephalographic rhythms around individual alpha frequency peak, typically altered in AD patients. The SMC participants negative to amyloid PET AD markers (SMCneg) with high (over low-moderate) education level showed higher posterior alpha 2 power density (possibly "neuroprotective"). Furthermore, amyloid PET-positive SMC (SMCpos) participants with high (over low-moderate) education level showed higher temporal alpha 3 power density (possibly "neuroprotective") and lower posterior alpha 2 power density (possibly "compensatory"). This effect may reflect cognitive reserve as no differences in brain gray-white matter, and cognitive functions were observed between these SMCpos/SMCneg subgroups. Preclinical Alzheimer's neuropathology may interact with education attainment and neurophysiological mechanisms generating cortical alpha rhythms around individual alpha frequency peak (i.e., alpha 2 and 3) in quiet wakefulness.

Keywords: Alpha rhythms; INSIGHT-preAD study; Preclinical Alzheimer's disease (AD); Preclinical Alzheimer's neuropathology; Resting state EEG rhythms; Subjective memory complaint (SMC).

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Aged
Aged, 80 and over
Alpha Rhythm*
Alzheimer Disease / diagnosis*
Alzheimer Disease / physiopathology*
Alzheimer Disease / psychology*
Brain / physiopathology*
Cognitive Reserve*
Cohort Studies
Educational Status*
Electroencephalography*
Female
Humans
Magnetic Resonance Imaging
Male
Memory*
Positron-Emission Tomography
Prospective Studies
Rest / physiology*