Frontotemporal structure preservation underlies the protective effect of lifetime intellectual cognitive reserve on cognition in the elderly

Abstract Background Cognitive decline with age has heterogeneous, which might be related to the accumulation of protective factors called cognitive reserve, especially intellectual engagement factors over the life course. However, how lifetime intellectual cognitive reserve (LICR) protects cognitive...

Full description

Saved in:
Bibliographic Details
Main Authors: Dandan Wang, Xin Li, Mingxi Dang, Shaokun Zhao, Feng Sang, Zhanjun Zhang
Format: Article
Language:English
Published: BMC 2024-11-01
Series:Alzheimer’s Research & Therapy
Subjects:
Online Access:https://doi.org/10.1186/s13195-024-01613-6
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850129463561420800
author Dandan Wang
Xin Li
Mingxi Dang
Shaokun Zhao
Feng Sang
Zhanjun Zhang
author_facet Dandan Wang
Xin Li
Mingxi Dang
Shaokun Zhao
Feng Sang
Zhanjun Zhang
author_sort Dandan Wang
collection DOAJ
description Abstract Background Cognitive decline with age has heterogeneous, which might be related to the accumulation of protective factors called cognitive reserve, especially intellectual engagement factors over the life course. However, how lifetime intellectual cognitive reserve (LICR) protects cognitive function in the elderly remains unclear. We aimed to examine the relationship between LICR and cognition and the mild cognitive impairment (MCI) risk, as well as the neural mechanism of LICR on cognition. Methods A total of 5126 participants completed extensive neuropsychological tests, with LICR indicator encompassing early education, midlife occupational complexity, and mental leisure activities after retirement. Confirmatory factor analysis was performed to derive LICR score and cognitive function scores, then the hierarchical regression analysis was used to explore the relationship between LICR and cognitive functions and the risk of MCI. We further explored the macro- and micro-structural preservation underly LICR in 1117 participants. Multiple regressions and tract-based spatial statistics were used to explore the relationship between LICR and gray matter volume and white matter microstructure (FA value). Finally, using the mediation model to explore the relationship of “LICR-brain-cognition”. Result The new LICR index, which was more protective than its single indexes, could protect widespread cognitive functions and was associated with a reduction in MCI risk (Odds Ratio, 0.52; 95% CI, 0.47–0.57). For the structure basis of LICR, the higher LICR score was associated with the greater gray matter volume in right fusiform gyrus (t = 4.62, FDR corrected, p < 0.05) and left orbital superior frontal gyrus (t = 4.56, FDR corrected, p < 0.05), and the higher FA values in the frontotemporal related white matter fiber tracts. Furthermore, the right fusiform gyrus partially mediated the relationship between LICR and executive processing ability (β = 0.01, p = 0.02) and general cognitive ability (β = 0.01, p = 0.03). Conclusions The new comprehensive cognitive reserve index could promote the temporal macro-structural preservation and thus contribute to maintain better cognitive function. These findings highlight the importance of intellectual CR accumulation over the life course in successful cognitive aging and MCI prevention, thereby contributing to improve the quality of life in the elderly.
format Article
id doaj-art-7b8a77fcce91481dbd5342dc34433a8b
institution OA Journals
issn 1758-9193
language English
publishDate 2024-11-01
publisher BMC
record_format Article
series Alzheimer’s Research & Therapy
spelling doaj-art-7b8a77fcce91481dbd5342dc34433a8b2025-08-20T02:32:57ZengBMCAlzheimer’s Research & Therapy1758-91932024-11-0116111410.1186/s13195-024-01613-6Frontotemporal structure preservation underlies the protective effect of lifetime intellectual cognitive reserve on cognition in the elderlyDandan Wang0Xin Li1Mingxi Dang2Shaokun Zhao3Feng Sang4Zhanjun Zhang5State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal UniversityState Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal UniversityState Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal UniversityState Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal UniversityState Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal UniversityState Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal UniversityAbstract Background Cognitive decline with age has heterogeneous, which might be related to the accumulation of protective factors called cognitive reserve, especially intellectual engagement factors over the life course. However, how lifetime intellectual cognitive reserve (LICR) protects cognitive function in the elderly remains unclear. We aimed to examine the relationship between LICR and cognition and the mild cognitive impairment (MCI) risk, as well as the neural mechanism of LICR on cognition. Methods A total of 5126 participants completed extensive neuropsychological tests, with LICR indicator encompassing early education, midlife occupational complexity, and mental leisure activities after retirement. Confirmatory factor analysis was performed to derive LICR score and cognitive function scores, then the hierarchical regression analysis was used to explore the relationship between LICR and cognitive functions and the risk of MCI. We further explored the macro- and micro-structural preservation underly LICR in 1117 participants. Multiple regressions and tract-based spatial statistics were used to explore the relationship between LICR and gray matter volume and white matter microstructure (FA value). Finally, using the mediation model to explore the relationship of “LICR-brain-cognition”. Result The new LICR index, which was more protective than its single indexes, could protect widespread cognitive functions and was associated with a reduction in MCI risk (Odds Ratio, 0.52; 95% CI, 0.47–0.57). For the structure basis of LICR, the higher LICR score was associated with the greater gray matter volume in right fusiform gyrus (t = 4.62, FDR corrected, p < 0.05) and left orbital superior frontal gyrus (t = 4.56, FDR corrected, p < 0.05), and the higher FA values in the frontotemporal related white matter fiber tracts. Furthermore, the right fusiform gyrus partially mediated the relationship between LICR and executive processing ability (β = 0.01, p = 0.02) and general cognitive ability (β = 0.01, p = 0.03). Conclusions The new comprehensive cognitive reserve index could promote the temporal macro-structural preservation and thus contribute to maintain better cognitive function. These findings highlight the importance of intellectual CR accumulation over the life course in successful cognitive aging and MCI prevention, thereby contributing to improve the quality of life in the elderly.https://doi.org/10.1186/s13195-024-01613-6Lifetime intellectual cognitive reserve (LICR)Cognitive functionMacro- and micro-structural preservationNeural mechanismSuccessful cognitive agingMCI
spellingShingle Dandan Wang
Xin Li
Mingxi Dang
Shaokun Zhao
Feng Sang
Zhanjun Zhang
Frontotemporal structure preservation underlies the protective effect of lifetime intellectual cognitive reserve on cognition in the elderly
Alzheimer’s Research & Therapy
Lifetime intellectual cognitive reserve (LICR)
Cognitive function
Macro- and micro-structural preservation
Neural mechanism
Successful cognitive aging
MCI
title Frontotemporal structure preservation underlies the protective effect of lifetime intellectual cognitive reserve on cognition in the elderly
title_full Frontotemporal structure preservation underlies the protective effect of lifetime intellectual cognitive reserve on cognition in the elderly
title_fullStr Frontotemporal structure preservation underlies the protective effect of lifetime intellectual cognitive reserve on cognition in the elderly
title_full_unstemmed Frontotemporal structure preservation underlies the protective effect of lifetime intellectual cognitive reserve on cognition in the elderly
title_short Frontotemporal structure preservation underlies the protective effect of lifetime intellectual cognitive reserve on cognition in the elderly
title_sort frontotemporal structure preservation underlies the protective effect of lifetime intellectual cognitive reserve on cognition in the elderly
topic Lifetime intellectual cognitive reserve (LICR)
Cognitive function
Macro- and micro-structural preservation
Neural mechanism
Successful cognitive aging
MCI
url https://doi.org/10.1186/s13195-024-01613-6
work_keys_str_mv AT dandanwang frontotemporalstructurepreservationunderliestheprotectiveeffectoflifetimeintellectualcognitivereserveoncognitionintheelderly
AT xinli frontotemporalstructurepreservationunderliestheprotectiveeffectoflifetimeintellectualcognitivereserveoncognitionintheelderly
AT mingxidang frontotemporalstructurepreservationunderliestheprotectiveeffectoflifetimeintellectualcognitivereserveoncognitionintheelderly
AT shaokunzhao frontotemporalstructurepreservationunderliestheprotectiveeffectoflifetimeintellectualcognitivereserveoncognitionintheelderly
AT fengsang frontotemporalstructurepreservationunderliestheprotectiveeffectoflifetimeintellectualcognitivereserveoncognitionintheelderly
AT zhanjunzhang frontotemporalstructurepreservationunderliestheprotectiveeffectoflifetimeintellectualcognitivereserveoncognitionintheelderly