Distinct age-related alterations in alpha-beta neural oscillatory activity during verbal working memory encoding in children and adolescents

IF 4.4 2区 医学 Q1 NEUROSCIENCES Journal of Physiology-London Pub Date : 2025-03-07 DOI:10.1113/JP287372
Augusto Diedrich, Yasra Arif, Brittany K. Taylor, Zhiying Shen, Phillip M. Astorino, Wai Hon Lee, Ryan W. McCreery, Elizabeth Heinrichs-Graham
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引用次数: 0

Abstract

Emerging imaging studies of working memory (WM) have identified significant WM-related oscillatory events that are unique to each phase of working memory (e.g. encoding, maintenance). Although many previous imaging studies have shown age-related changes within the frontoparietal network when performing a WM task, understanding of the age-related changes in the oscillatory dynamics underlying each phase of WM during development and their relationships to other cognitive function is still in its infancy. To this end, we enrolled a group of 74 typically-developing youths aged 7–15 years to perform a letter-based Sternberg WM task during magnetoencephalography. Trial-wise data were transformed into the time-frequency domain, and significant oscillatory responses during the encoding and maintenance phases of the task were independently imaged using beamforming. Our results revealed widespread age-related power differences in alpha-beta oscillatory activity during encoding throughout left frontal, parietal, temporal, occipital and cerebellar regions. By contrast, age-related differences in maintenance-related activity were limited to a small area in the superior temporal gyrus and parieto-occipital regions. Follow-up exploratory factor analysis of age-related encoding alpha-beta activity revealed two distinct factors, and these factors were each found to significantly mediate age-related improvements in both verbal and non-verbal cognitive ability. Additionally, late maintenance alpha activity was related to reaction time on the task. Taken together, our results indicate that the neural dynamics in the alpha and beta bands are uniquely sensitive to age-related changes throughout this developmental period and are related to both task performance and other aspects of cognitive development.

Key points

  • Understanding of the age-related changes in neural oscillatory dynamics serving verbal working memory function is in its infancy.
  • This study identified the age-related neural alterations during each phase of working memory processing in youths.
  • Developmental differences during working memory processing were primarily isolated to alpha-beta activity during the encoding phase.
  • Alpha-beta activity during encoding significantly mediated age-related improvements in both verbal and non-verbal ability.
  • This study establishes new brain–behaviour relationships linking working memory function to other aspects of cognitive development.

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在儿童和青少年的言语工作记忆编码中,α - β神经振荡活动的明显年龄相关改变。
新兴的工作记忆成像研究已经确定了与工作记忆相关的重要振荡事件,这些振荡事件在工作记忆的每个阶段(如编码、维持)都是独一无二的。尽管许多先前的成像研究表明,在执行脑皮层任务时,额顶叶网络中存在与年龄相关的变化,但对脑皮层发育过程中每个阶段的振荡动力学中与年龄相关的变化及其与其他认知功能的关系的理解仍处于起步阶段。为此,我们招募了74名7-15岁的典型发展青少年,在脑磁图期间执行基于字母的Sternberg WM任务。试验数据被转换到时频域,并且在任务的编码和维持阶段的显著振荡响应使用波束形成独立成像。我们的研究结果揭示了编码过程中α - β振荡活动在左额叶、顶叶、颞叶、枕叶和小脑区域广泛存在与年龄相关的功率差异。相比之下,维持相关活动的年龄相关差异仅限于颞上回和顶枕区域的一小块区域。年龄相关编码α - β活性的随访探索性因素分析揭示了两个不同的因素,这些因素都被发现显著调节语言和非语言认知能力的年龄相关改善。此外,后期维持α活动与任务的反应时间有关。综上所述,我们的研究结果表明,在整个发育时期,α和β带的神经动力学对与年龄相关的变化非常敏感,并且与任务表现和认知发展的其他方面有关。重点:对语言工作记忆功能中与年龄相关的神经振荡动力学变化的理解尚处于起步阶段。本研究确定了青少年在工作记忆加工的各个阶段与年龄相关的神经变化。工作记忆加工过程中的发育差异主要与编码阶段的α - β活动有关。编码过程中的α - β活动显著调节了语言和非语言能力的年龄相关改善。这项研究建立了新的大脑行为关系,将工作记忆功能与认知发展的其他方面联系起来。
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来源期刊
Journal of Physiology-London
Journal of Physiology-London 医学-神经科学
CiteScore
9.70
自引率
7.30%
发文量
817
审稿时长
2 months
期刊介绍: The Journal of Physiology publishes full-length original Research Papers and Techniques for Physiology, which are short papers aimed at disseminating new techniques for physiological research. Articles solicited by the Editorial Board include Perspectives, Symposium Reports and Topical Reviews, which highlight areas of special physiological interest. CrossTalk articles are short editorial-style invited articles framing a debate between experts in the field on controversial topics. Letters to the Editor and Journal Club articles are also published. All categories of papers are subjected to peer reivew. The Journal of Physiology welcomes submitted research papers in all areas of physiology. Authors should present original work that illustrates new physiological principles or mechanisms. Papers on work at the molecular level, at the level of the cell membrane, single cells, tissues or organs and on systems physiology are all acceptable. Theoretical papers and papers that use computational models to further our understanding of physiological processes will be considered if based on experimentally derived data and if the hypothesis advanced is directly amenable to experimental testing. While emphasis is on human and mammalian physiology, work on lower vertebrate or invertebrate preparations may be suitable if it furthers the understanding of the functioning of other organisms including mammals.
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