Aging-Related Changes in Cortical Sources of Sleep Oscillatory Neural Activity Following Motor Learning Reflect Contributions of Cortical Thickness and Pre-sleep Functional Activity.

Aging-Related Changes in Cortical Sources of Sleep Oscillatory Neural Activity Following Motor Learning Reflect Contributions of Cortical Thickness and Pre-sleep Functional Activity.
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DOI:
10.3389/fnagi.2021.787654
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发表时间:
2021
影响因子:
4.8
通讯作者:
Spencer RMC
Spencer RMC
中科院分区:
医学2区
文献类型:
--
作者:
Fitzroy AB;Jones BJ;Kainec KA;Seo J;Spencer RMC

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睡眠中的振荡神经活动,如在德尔马区和西格玛区的活动,对巩固运动学习很重要。这种活动随着典型的衰老而减少,这种减少可能导致与衰老相关的运动学习巩固能力的下降。有证据表明,参与运动学习的大脑区域有助于在随后的睡眠中产生振荡的神经活动。然而,运动学习后睡眠振荡活动的区域贡献与年龄相关的差异尚不清楚。为了表征这些差异,我们使用个人解剖信息估计了年轻人和老年人在运动学习后非快速眼动睡眠期间与巩固相关的振荡活动的皮质来源,并根据皮质厚度和睡前脑功能激活进行了分析。作为更大实验方案的一部分,在完成功能性磁共振成像系列反应时间任务后,在午睡期间记录了年轻人和老年人的高密度脑电。在左侧加权运动皮质网络中,睡眠增量活动随年龄增加而减少,包括运动前皮质、初级运动皮质、辅助运动区和辅助运动区,以及顶叶、颞叶、枕叶和扣带回的非运动区。在类似的左侧加权运动网络中,睡眠theta活动随着年龄的增长而减少,在非运动性前额叶和中扣带回区域也是如此。睡眠Sigma活动在左侧初级运动皮质、非运动右侧加权前额-颞叶网络和扣带区随年龄增加而减少。皮质变薄调节与衰老相关的外侧眶前皮质和额叶极的Sigma减少,以及部分调节海马旁回、梭形回和舌回的增量减少。睡眠前壳核、尾状核和顶叶下部皮质的激活以年龄调节的方式预测额叶和运动皮质对睡眠增量和theta活动的贡献,反映出年轻人的负面关系和老年人的积极或缺乏关系。总体而言,这些结果支持了局部睡眠假说,即学习过程中活跃的大脑区域有助于随后睡眠中与巩固相关的神经活动,并表明这些区域的睡眠振荡活动随着年龄的增长而减少。
Oscillatory neural activity during sleep, such as that in the delta and sigma bands, is important for motor learning consolidation. This activity is reduced with typical aging, and this reduction may contribute to aging-related declines in motor learning consolidation. Evidence suggests that brain regions involved in motor learning contribute to oscillatory neural activity during subsequent sleep. However, aging-related differences in regional contributions to sleep oscillatory activity following motor learning are unclear. To characterize these differences, we estimated the cortical sources of consolidation-related oscillatory activity using individual anatomical information in young and older adults during non-rapid eye movement sleep after motor learning and analyzed them in light of cortical thickness and pre-sleep functional brain activation. High-density electroencephalogram was recorded from young and older adults during a midday nap, following completion of a functional magnetic resonance imaged serial reaction time task as part of a larger experimental protocol. Sleep delta activity was reduced with age in a left-weighted motor cortical network, including premotor cortex, primary motor cortex, supplementary motor area, and pre-supplementary motor area, as well as non-motor regions in parietal, temporal, occipital, and cingulate cortices. Sleep theta activity was reduced with age in a similar left-weighted motor network, and in non-motor prefrontal and middle cingulate regions. Sleep sigma activity was reduced with age in left primary motor cortex, in a non-motor right-weighted prefrontal-temporal network, and in cingulate regions. Cortical thinning mediated aging-related sigma reductions in lateral orbitofrontal cortex and frontal pole, and partially mediated delta reductions in parahippocampal, fusiform, and lingual gyri. Putamen, caudate, and inferior parietal cortex activation prior to sleep predicted frontal and motor cortical contributions to sleep delta and theta activity in an age-moderated fashion, reflecting negative relationships in young adults and positive or absent relationships in older adults. Overall, these results support the local sleep hypothesis that brain regions active during learning contribute to consolidation-related neural activity during subsequent sleep and demonstrate that sleep oscillatory activity in these regions is reduced with aging.
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