Killanin Abraham D, Ward Thomas W, Rice Danielle L, Ende Grace C, Coutant Anna T, Steiner Erica, Embury Christine M, Calhoun Vince D, Wang Yu-Ping, Stephen Julia M, Picci Giorgia, Heinrichs-Graham Elizabeth, Wilson Tony W
Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA.
Center for Pediatric Brain Health, Boys Town National Research Hospital, Boys Town, NE, USA.
J Physiol. 2025 May;603(10):3107-3121. doi: 10.1113/JP287721. Epub 2025 May 5.
The neural network serving verbal working memory processes undergoes dramatic changes during the transition from childhood to adolescence, including changes in cortical thickness, activation levels, connectivity and inherent dynamics. Of all these neural properties, maturational changes in dynamic functional connectivity among developmentally sensitive regions within this network are among the least understood. To address this, we examined 75 typically developing youth (age range 6-14 years), who completed a verbal working memory task during magnetoencephalography (MEG). All MEG data were imaged and the phase-locking value was computed as an index of functional connectivity between regions exhibiting significant relationships with chronological age. Our results suggested developmental differences in functional connectivity during specific phases of working memory processing. During encoding, connectivity increased with age between left prefrontal and inferior parietal, with such age-related increases varying by sex between right frontal and left occipitotemporal regions. During the maintenance period, connectivity increased with age between left occipitotemporal and right posterior parietal areas and decreased with age between left frontal and right occipital cortices. These findings suggest that neural oscillations within regions serving working memory processing, as well as functional connectivity among these regions, are modulated by development during the transition from childhood to adolescence. KEY POINTS: With development from childhood to adolescence, verbal working memory processing becomes increasingly left lateralized in the prefrontal, parietal and temporal cortices. Several electrophysiological studies have shown that alpha oscillations within these brain regions become stronger with increasing chronological age during the transition from childhood to adolescence. Although such oscillatory power differences are well established, age-related changes in functional connectivity among these brain regions is far less understood. Here, we report novel findings suggesting that functional connectivity between developmentally sensitive cortical regions supporting verbal working memory scales with age among visual, language and attention-related brain systems. These results help to refine models of functional neural development supporting verbal working memory ability for future application in both basic research and clinical studies of typical and atypical cognitive development.
负责言语工作记忆过程的神经网络在从童年到青春期的过渡期间会发生巨大变化,包括皮质厚度、激活水平、连通性和内在动力学的变化。在所有这些神经特性中,该网络内发育敏感区域之间动态功能连通性的成熟变化是了解最少的。为了解决这个问题,我们研究了75名发育正常的青少年(年龄范围6 - 14岁),他们在脑磁图(MEG)检查期间完成了一项言语工作记忆任务。对所有MEG数据进行成像,并计算锁相值,作为与实际年龄呈现显著关系的区域之间功能连通性的指标。我们的结果表明,在工作记忆处理的特定阶段,功能连通性存在发育差异。在编码期间,左前额叶和顶下叶之间的连通性随年龄增加,而这种与年龄相关的增加在右额叶和左枕颞叶区域因性别而异。在维持期,左枕颞叶和右后顶叶区域之间的连通性随年龄增加,而左额叶和右枕叶皮质之间的连通性随年龄下降。这些发现表明,在从童年到青春期的过渡过程中,负责工作记忆处理的区域内的神经振荡以及这些区域之间的功能连通性受到发育的调节。要点:从童年到青春期的发育过程中,言语工作记忆处理在额叶、顶叶和颞叶皮质中越来越偏向左侧化。多项电生理研究表明,在从童年到青春期的过渡过程中,这些脑区的α振荡随着实际年龄的增加而增强。尽管这种振荡功率差异已得到充分证实,但这些脑区之间功能连通性的年龄相关变化却知之甚少。在此,我们报告了新的发现,表明支持言语工作记忆的发育敏感皮质区域之间的功能连通性在视觉、语言和注意力相关脑系统中随年龄增长。这些结果有助于完善支持言语工作记忆能力的功能性神经发育模型,以便未来在典型和非典型认知发育的基础研究和临床研究中应用。
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