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Associations between Cortical Thickness and Metamemory in Alzheimer’s Disease

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Abstract

Metacognitive deficits affect Alzheimer’s disease (AD) patient safety and increase caregiver burden. The brain areas that support metacognition are not well understood. 112 participants from the Imaging and Genetic Biomarkers for AD (ImaGene) study underwent comprehensive cognitive testing and brain magnetic resonance imaging. A performance-prediction paradigm was used to evaluate metacognitive abilities for California Verbal Learning Test–II learning (CVLT-II 1–5) and delayed recall (CVLT-II DR); Visual Reproduction-I immediate recall (VR-I Copy) and Visual Reproduction-II delayed recall (VR-II DR); Rey-Osterrieth Complex Figure Copy (Rey-O Copy) and delayed recall (Rey-O DR). Vertex-wise multivariable regression of cortical thickness was performed using metacognitive scores as predictors while controlling for age, sex, education, and intracranial volume. Subjects who overestimated CVLT-II DR in prediction showed cortical atrophy, most pronounced in the bilateral temporal and left greater than right (L > R) frontal cortices. Overestimation of CVLT-II 1–5 prediction and DR performance in postdiction showed L > R associations with medial, inferior and lateral temporal and left posterior cingulate cortical atrophy. Overconfident prediction of VR-I Copy performance was associated with right greater than left medial, inferior and lateral temporal, lateral parietal, anterior and posterior cingulate and lateral frontal cortical atrophy. Underestimation of Rey-O Copy performance in prediction was associated with atrophy localizing to the temporal and cingulate areas, and in postdiction, with diffuse cortical atrophy. Impaired metacognition was associated to cortical atrophy. Our results indicate that poor insight into one’s cognitive abilities is a pervasive neurodegenerative feature associated with AD across the cognitive spectrum.

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Data availability

MRI data is available through LONI Image Data Archive (IDA) (https://ida.loni.usc.edu).

Code availability

No software was used for data collection. We used publicly available packages and functions described in methods for data analysis.

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Funding

The analyses reported in this manuscript were funded by the NIA R01 AG040770, NIA K02 AG048240, NIA P50 AG16570, NIA P30 AG010133, NIA U01 AG02490, NLM R01 LM012535, NIA R03 AG054936, the Alzheimer’s Association, the Easton Consortium for Alzheimer’s Drug Discovery and Biomarker Development, and the Indiana Clinical and Translational Science Institute.

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Authors and Affiliations

  1. Department of Internal Medicine-Section of Gerontology and Geriatric Medicine, Wake Forest University School of Medicine, 525 Vine Street, Suite 150, Winston-Salem, NC, 27101, USA

    Tugce Duran

  2. Department of Psychology, California State University, Fresno, Fresno, CA, USA

    Ellen Woo

  3. Department of Psychiatry, University of California, San Francisco, San Francisco, CA, USA

    Ellen Woo

  4. Department of Neurology, Indiana University School of Medicine, Indianapolis, IN, USA

    Diana Otero, Eddie Stage, Apoorva B. Sanjay & Liana G. Apostolova

  5. Department of Radiology, Indiana University School of Medicine, Indianapolis, IN, USA

    Shannon L. Risacher, Kwangsik Nho, John D. West & Liana G. Apostolova

  6. Department of Epidemiology and Biostatistics, Indiana University School of Public Health, Bloomington, IN, USA

    Meredith L. Phillips

  7. Larner College of Medicine, University of Vermont, Burlington, VT, USA

    Naira Goukasian

  8. Department of Neurology, Emory University School of Medicine, Atlanta, GA, USA

    Kristy S. Hwang

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  1. Tugce Duran
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Contributions

Ms. Tugce Duran performed analysis and interpretation of the data and was responsible for drafting and revision of the manuscript. Dr. Diana Otero, Dr. Shannon Risacher, Dr. Kwangsik Nho, Dr. Eddie Stage, Mrs. Meredith Phillips and Ms. Apoorva Sanjay were involved in the analysis of the data contained in this study and revision of the manuscript. Mr. John West was involved in the data processing and analysis. Dr. Kristy Hwang and Ms. Naira Goukasian were involved in subject recruitment, collection and analysis of the study data, and revision of the manuscript. Dr. Ellen Woo was involved in the design, conceptualization, data collection and execution of the cognitive component of study, interpretation of the data, and revision of the manuscript. Dr. Liana Apostolova, the primary investigator of the study, was involved with the design, conceptualization, data collection and execution of the clinical and neuroimaging components of the study, interpretation of the data, and revision of the manuscript.

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Correspondence to Tugce Duran.

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Conflicts of Interest

Tugce Duran, MS, Ellen Woo, PhD, Diana Otero, PhD, Shannon L. Risacher, PhD, Eddie Stage, PhD, Apoorva B. Sanjay, BS, Kwangsik Nho, PhD, John D. West, MS, Meredith L. Phillips, MS, Naira Goukasian, BS, and Kristy S. Hwang, MD have no relevant conflicts of interest to report. Liana G. Apostolova, MD, MS has served on Advisory Boards for Eli Lilly, Biogen and Two Labs, and has received research support from GE Healthcare, AVID Radiopharmaceuticals Inc., Life Molecular Imaging and Roche Diagnostics. Dr. Apostolova serves on a DSMB for IQVIA.

The UCLA Institutional Review Boards approved the study. All ImaGene participants or their legally authorized representatives provided informed consent for data collection and publication according to the Declaration of Helsinki, U.S. federal regulations, local state laws and regulations, and policies of the UCLA IRB.

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Duran, T., Woo, E., Otero, D. et al. Associations between Cortical Thickness and Metamemory in Alzheimer’s Disease. Brain Imaging and Behavior 16, 1495–1503 (2022). https://doi.org/10.1007/s11682-021-00627-0

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