Distinctive effects of executive dysfunction and loss of learning/memory abilities on resting-state brain activity

Hideyuki Hoshi,Sayuri Ichikawa,Víctor Rodríguez-González,Jesús Poza,Momoko Kobayashi,Carlos Gómez,Yoshihito Shigihara,Yuki Sakamoto,Yoko Hirata,Keisuke Fukasawa

doi:10.1038/s41598-022-07202-7

Abstract

Dementia is a syndrome characterised by cognitive impairments, with a loss of learning/memory abilities at the earlier stages and executive dysfunction at the later stages. However, recent studies have suggested that impairments in both learning/memory abilities and executive functioning might co-exist. Cognitive impairments have been primarily evaluated using neuropsychological assessments, such as the Mini-Mental State Examination (MMSE). Recently, neuroimaging techniques such as magnetoencephalography (MEG), which assess changes in resting-state brain activity, have also been used as biomarkers for cognitive impairment. However, it is unclear whether these changes reflect dysfunction in executive function as well as learning and memory. In this study, parameters from the MEG for brain activity, MMSE for learning/memory, and Frontal Assessment Battery (FAB) for executive function were compared within 207 individuals. Three MEG parameters were used as representatives of resting-state brain activity: median frequency, individual alpha frequency, and Shannon’s spectral entropy. Regression analysis showed that median frequency was predicted by both the MMSE and FAB scores, while individual alpha frequency and Shannon’s spectral entropy were predicted by MMSE and FAB scores, respectively. Our results indicate that MEG spectral parameters reflect both learning/memory and executive functions, supporting the utility of MEG as a biomarker of cognitive impairment.

Highlights

Dementia is a syndrome characterised by progressive deterioration of cognitive functioning due to various brain pathologies
We considered only the healthy individuals’ dataset, as cognitive decline due to healthy ageing and pathological change could lead to different relationships between MEG spectral parameters and neuropsychological assesment scores; we used the dataset of 34 individuals with healthy ageing in the control analysis
This study showed that both sub-domains of cognitive functions—learning/memory and executive function— were associated with MEG spectral parameters

Summary

Introduction

Dementia is a syndrome characterised by progressive deterioration of cognitive functioning due to various brain pathologies. The loss of learning/memory abilities is often the chief complaint of patients with earlystage dementia[2] These functions are served by the temporal cortex, where pathological change initially starts[2]. The Mini-Mental State Examination (MMSE), which is the most commonly used assessment tool for dementia screening[3], primarily evaluates learning/memory performance[4]. Executive function is another sub-domain of cognitive function that includes attention, inhibition, working memory, interference control, and cognitive flexibility[5], which is served by the prefrontal c ortex[6]. MMSE frontal-executive dysfunction[10], and fails to detect mild cognitive impairment (MCI) in approximately a third of individuals[11] Both neuropsychological assessments are validated and easy to use in clinical settings, they have inherent limitations, such as skill dependence, subjectivity, ceiling effects, and practice effects. Our analyses aimed to determine whether MEG biomarkers are sensitive to learning/memory and executive function

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Conclusion