Eyes-state-dependent alterations of magnetoencephalographic connectivity associated with delayed recall in Alzheimer's disease via graph theory approach

Keigo Yuasa; Tetsu Hirosawa; Daiki Soma; Naoki Furutani; Masafumi Kameya; Masuhiko Sano; Koji Kitamura; Minehisa Ueda; Mitsuru Kikuchi

doi:10.3389/fpsyt.2023.1272120

Eyes-state-dependent alterations of magnetoencephalographic connectivity associated with delayed recall in Alzheimer's disease via graph theory approach

Front Psychiatry. 2023 Oct 24:14:1272120. doi: 10.3389/fpsyt.2023.1272120. eCollection 2023.

Authors

Keigo Yuasa¹, Tetsu Hirosawa², Daiki Soma¹, Naoki Furutani¹, Masafumi Kameya¹, Masuhiko Sano¹, Koji Kitamura¹, Minehisa Ueda², Mitsuru Kikuchi¹

Affiliations

¹ Department of Psychiatry and Neurobiology, Graduate School of Medical Science, Kanazawa University, Kanazawa, Japan.
² Research Center for Child Mental Development, Kanazawa University, Kanazawa, Japan.

Abstract

Introduction: Alzheimer’s disease (AD) is a neurodegenerative disorder characterized by memory impairment and cognitive decline. Electroencephalography (EEG) and magnetoencephalography (MEG) studies using graph theory show altered “Small-Worldness (SW)” properties in AD. This study aimed to investigate whether eye-state-dependent alterations in SW differ between patients with AD and healthy controls, considering the symptoms of AD.

Methods: Nineteen patients with AD and 24 healthy controls underwent MEG under different conditions (eyes-open [EO] and eyes-closed [EC]) and the Wechsler Memory Scale-Revised (WMS-R) with delayed recall. After the signal sources were mapped onto the Desikan–Killiany brain atlas, the statistical connectivity of five frequency bands (delta, theta, alpha, beta, and gamma) was calculated using the phase lag index (PLI), and binary graphs for each frequency band were constructed based on the PLI. Next, we measured SW as a graph metric and evaluated three points: the impact of AD and experimental conditions on SW, the association between SW and delayed recall, and changes in SW across experimental conditions correlated with delayed recall.

Results: SW in the gamma band was significantly lower in patients with AD (z = −2.16, p = 0.031), but the experimental conditions did not exhibit a significant effect in any frequency band. Next, in the AD group, higher scores on delayed recall correlated with diminished SW across delta, alpha, and beta bands in the EO condition. Finally, delayed recall scores significantly predicted relative differences in the SW group in the alpha band (t = −2.98, p = 0.009).

Discussion: Given that network studies could corroborate the results of previous power spectrum studies, our findings contribute to a multifaceted understanding of functional brain networks in AD, emphasizing that the SW properties of these networks change according to disease status, cognitive function, and experimental conditions.

Keywords: Alzheimer’s disease; delayed recall; eyes-closed; eyes-open; graph theory; magnetoencephalography.