Cued Reactivation of Motor Learning during Sleep Leads to Overnight Changes in Functional Brain Activity and Connectivity.
Cued Reactivation of Motor Learning during Sleep Leads to Overnight Changes in Functional Brain Activity and Connectivity.
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DOI：
10.1371/journal.pbio.1002451
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发表时间：
2016-05
期刊：
影响因子：
9.8
通讯作者：
Lewis PA
中科院分区：
文献类型：
--
作者：
Cousins JN;El-Deredy W;Parkes LM;Hennies N;Lewis PA
睡眠在记忆巩固中起着重要作用。睡眠后表现和神经可塑性的提高证明了这一点。有针对性的记忆再激活（TMR）可以通过在睡眠中有意地偏置特定记忆的重播来操纵睡眠依赖性巩固，但这些改变记忆的潜在神经基础尚不清楚。我们使用功能性磁共振成像（fMRI）来显示慢波睡眠（SWS）中目标再激活后运动记忆的神经表征的变化。参与者学习了两个序列反应时间任务（SRTT）序列，这些序列与不同的听觉音调（高音或低音）相关。在随后的SWS中，通过重放相关的音调来重新激活一个序列。第二天，参与者在fMRI中对这两个序列进行了重新测试。正如预测的那样，在目标记忆重新激活后，他们对提示序列的反应速度更快。此外，双侧尾状核和海马的活动增加相对于未被提示的序列与SWS的时间有关，而小脑和皮质运动活动增加与快速眼动（REM）睡眠的时间有关。靶性记忆再激活后，尾状核和海马之间的功能连通性也有所增强。这些发现表明，与记忆再激活相关的离线表现提升是由关键认知和运动网络功能活动的改变所支持的，而这种巩固是由快速眼动睡眠和静醒睡眠不同地介导的。慢波睡眠和快速眼动睡眠与不同大脑网络中运动技能的重新激活和巩固有关。在学习了一项运动技能之后，记忆经历了“离线”处理，因此即使没有进一步的练习，也会有所改善。睡眠已被证明可以加强这种巩固，并在此过程中重组相关的大脑区域。然而，目前尚不清楚睡眠是如何做到这一点的，以及不同的睡眠阶段是否有不同的贡献。一种流行的观点是，记忆痕迹在慢波睡眠期间被重新激活。慢波睡眠是一种由脑电图（EEG）记录的以低频率和高振幅同步活动为特征的睡眠时期，它驱动大脑内的记忆重组。为了在人类身上测试这一点，我们利用了“有针对性的记忆再激活”，即通过学习过程中出现的声音来提示特定记忆的重播。睡眠后，暗示记忆的运动表现更快，这表明这种痕迹在睡眠期间得到了巩固。与此同时，暗示记忆的大脑激活和几个运动学习区域的连通性得到了增强。此外，大脑活动的一些变化与慢波睡眠的时间有关，而另一些变化与快速眼动睡眠的时间有关。这些观察结果表明，离线技能的增强依赖于特定记忆的重新激活，而神经活动的相关变化可能依赖于在睡眠不同阶段展开的处理，从而进一步深入了解睡眠在记忆巩固中的独特作用。
Sleep plays a role in memory consolidation. This is demonstrated by improved performance and neural plasticity underlying that improvement after sleep. Targeted memory reactivation (TMR) allows the manipulation of sleep-dependent consolidation through intentionally biasing the replay of specific memories in sleep, but the underlying neural basis of these altered memories remains unclear. We use functional magnetic resonance imaging (fMRI) to show a change in the neural representation of a motor memory after targeted reactivation in slow-wave sleep (SWS). Participants learned two serial reaction time task (SRTT) sequences associated with different auditory tones (high or low pitch). During subsequent SWS, one sequence was reactivated by replaying the associated tones. Participants were retested on both sequences the following day during fMRI. As predicted, they showed faster reaction times for the cued sequence after targeted memory reactivation. Furthermore, increased activity in bilateral caudate nucleus and hippocampus for the cued relative to uncued sequence was associated with time in SWS, while increased cerebellar and cortical motor activity was related to time in rapid eye movement (REM) sleep. Functional connectivity between the caudate nucleus and hippocampus was also increased after targeted memory reactivation. These findings suggest that the offline performance gains associated with memory reactivation are supported by altered functional activity in key cognitive and motor networks, and that this consolidation is differentially mediated by both REM sleep and SWS. Slow-wave sleep and rapid eye movement sleep are associated with the reactivation and consolidation of a motor skill within distinct brain networks. After a motor skill is learned, the memory undergoes "offline" processing so that improvement occurs even without further practice. Sleep has been shown to enhance this consolidation and, in the process, to reorganize the brain regions involved. However, it remains unclear how sleep does this, and whether different sleep stages have different contributions. One popular idea is that the memory trace is reactivated during slow-wave sleep—a period of sleep characterized by synchronized activity at a slow frequency and high amplitude, as recorded by electroencephalography (EEG)—which drives memory reorganization within the brain. To test this in humans, we took advantage of "targeted memory reactivation," where replay of specific memories is cued by presentation of a sound that was present during learning. After sleep, motor performance was faster for cued memories, suggesting that the trace was consolidated during sleep. Coupled with this, brain activation and connectivity in several motor-learning areas was enhanced for the cued memory. Furthermore, some changes in brain activity were associated with time spent in slow-wave sleep, while others were associated with time spent in rapid-eye movement sleep. These observations provide further insight into sleep's unique role in memory consolidation by showing that offline skill enhancement depends on the reactivation of specific memories, and the associated changes in neural activity may rely upon processing that unfolds across different stages of sleep.