Hemisphere- and condition-specific alpha oscillations support semantic and spatial cognition in aging

IF 5.4 2区 医学 Q1 GERIATRICS & GERONTOLOGY GeroScience Pub Date : 2025-04-09 DOI:10.1007/s11357-025-01651-4
Maggie P. Rempe, Danae S. Manta, Kayle Cohen, Ryan J. Glesinger, Hannah J. Okelberry, Jason A. John, Anna T. Coutant, Lucy K. Horne, Grant M. Garrison, Kennedy A. Kress, Lucas Weyrich, Chloe C. Casagrande, Madelyn P. Willett, Hallie J. Johnson, Alex I. Wiesman, Elizabeth Heinrichs-Graham, Rachel K. Spooner, Christine M. Embury, Tony W. Wilson
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Abstract

Neuroimaging studies have shown age-related alterations in brain structure and function supporting semantic knowledge, although the significance of these is not fully understood. Herein, we report novel temporal, spectral, and spatial information on age-related changes from the largest dynamic functional mapping study of semantic processing. Participants (N = 130, age range 21–87 years, Mage = 51.05, SD = 14.73, 68 females) performed a semantic judgement task during magnetoencephalography (MEG), and significant task-related oscillatory responses were projected into anatomical space using a beamformer. Voxel-wise linear mixed-effects models were performed to assess semantic-related neural oscillations, irrespective of and influenced by age. Mediation analyses were performed to assess if local oscillations mediated the relationship between age and reaction time. Whole-brain analyses revealed stronger left-lateralized alpha/beta oscillations in frontotemporal cortices during semantic trials and stronger right-lateralized alpha/beta responses in temporoparietal regions during length trials (all ps <.001). Older adults showed stronger left temporoparietal alpha and left frontal beta during semantic processing and stronger alpha in the right temporal cortex during the length condition (all ps <.001). Alpha oscillations further mediated the relationship between age and reaction time in a hemisphere- and condition-specific manner, whereby right temporal activity mediated the age-behavior relationship in the length but not semantic condition (Z = 2.01, p =.022), while left temporoparietal activity significantly mediated this relationship in the semantic but not length condition (Z = − 2.41, p =.008). Altogether, our findings demonstrate accentuated oscillations in aging which are hemisphere- and condition-specific and support compensatory processing to aid in maintaining adequate behavioral performance, lending clear support to leading neuroscientific models of aging.

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半球和条件特异性α振荡支持语义和空间认知衰老
神经影像学研究表明,支持语义知识的大脑结构和功能与年龄相关的改变,尽管这些变化的意义尚不完全清楚。在此,我们报告了最大的语义处理动态功能映射研究中有关年龄相关变化的新的时间、光谱和空间信息。参与者(N = 130,年龄21-87岁,Mage = 51.05, SD = 14.73, 68名女性)在脑磁图(MEG)中执行语义判断任务,并使用波束形成器将显著的任务相关振荡反应投射到解剖空间。采用体素线性混合效应模型来评估语义相关的神经振荡,而不考虑年龄的影响。中介分析进行评估,如果局部振荡介导年龄和反应时间之间的关系。全脑分析显示,在语义试验期间,额颞叶皮层的左侧α / β振荡更强,而在长度试验期间,颞顶叶区域的右侧α / β反应更强(均ps <;.001)。老年人在语义加工过程中表现出较强的左颞顶α和左额叶β,在长度条件下表现出较强的右颞叶α(均p <;.001)。α振荡进一步以半球和条件特异性的方式介导年龄和反应时间之间的关系,其中右颞叶活动在长度条件下介导年龄-行为关系,而在语义条件下不介导年龄-行为关系(Z = 2.01, p = 0.022),而左颞顶叶活动在语义条件下显著介导年龄-行为关系,而在长度条件下不介导年龄-行为关系(Z = - 2.41, p = 0.008)。总之,我们的研究结果表明,衰老过程中的振荡加剧是半球和条件特异性的,并支持代偿处理,以帮助维持适当的行为表现,为领先的衰老神经科学模型提供明确的支持。
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来源期刊
GeroScience
GeroScience Medicine-Complementary and Alternative Medicine
CiteScore
10.50
自引率
5.40%
发文量
182
期刊介绍: GeroScience is a bi-monthly, international, peer-reviewed journal that publishes articles related to research in the biology of aging and research on biomedical applications that impact aging. The scope of articles to be considered include evolutionary biology, biophysics, genetics, genomics, proteomics, molecular biology, cell biology, biochemistry, endocrinology, immunology, physiology, pharmacology, neuroscience, and psychology.
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