Batterink Laura J, Creery Jessica D, Paller Ken A
Northwestern University, Evanston, Illinois 60208-2710
Northwestern University, Evanston, Illinois 60208-2710.
J Neurosci. 2016 Jan 27;36(4):1401-9. doi: 10.1523/JNEUROSCI.3175-15.2016.
Slow oscillations during slow-wave sleep (SWS) may facilitate memory consolidation by regulating interactions between hippocampal and cortical networks. Slow oscillations appear as high-amplitude, synchronized EEG activity, corresponding to upstates of neuronal depolarization and downstates of hyperpolarization. Memory reactivations occur spontaneously during SWS, and can also be induced by presenting learning-related cues associated with a prior learning episode during sleep. This technique, targeted memory reactivation (TMR), selectively enhances memory consolidation. Given that memory reactivation is thought to occur preferentially during the slow-oscillation upstate, we hypothesized that TMR stimulation effects would depend on the phase of the slow oscillation. Participants learned arbitrary spatial locations for objects that were each paired with a characteristic sound (eg, cat-meow). Then, during SWS periods of an afternoon nap, one-half of the sounds were presented at low intensity. When object location memory was subsequently tested, recall accuracy was significantly better for those objects cued during sleep. We report here for the first time that this memory benefit was predicted by slow-wave phase at the time of stimulation. For cued objects, location memories were categorized according to amount of forgetting from pre- to post-nap. Conditions of high versus low forgetting corresponded to stimulation timing at different slow-oscillation phases, suggesting that learning-related stimuli were more likely to be processed and trigger memory reactivation when they occurred at the optimal phase of a slow oscillation. These findings provide insight into mechanisms of memory reactivation during sleep, supporting the idea that reactivation is most likely during cortical upstates.
Slow-wave sleep (SWS) is characterized by synchronized neural activity alternating between active upstates and quiet downstates. The slow-oscillation upstates are thought to provide a window of opportunity for memory consolidation, particularly conducive to cortical plasticity. Recent evidence shows that sensory cues associated with previous learning can be delivered subtly during SWS to selectively enhance memory consolidation. Our results demonstrate that this behavioral benefit is predicted by slow-oscillation phase at stimulus presentation time. Cues associated with high versus low forgetting based on analysis of subsequent recall performance were delivered at opposite slow-oscillation phases. These results provide evidence of an optimal slow-oscillation phase for memory consolidation during sleep, supporting the idea that memory processing occurs preferentially during cortical upstates.
慢波睡眠（SWS）期间的慢振荡可能通过调节海马体与皮质网络之间的相互作用来促进记忆巩固。慢振荡表现为高振幅、同步的脑电图活动，对应于神经元去极化的上行状态和超极化的下行状态。记忆再激活在慢波睡眠期间自发发生，也可以通过在睡眠期间呈现与先前学习事件相关的学习线索来诱导。这种技术，即靶向记忆再激活（TMR），选择性地增强记忆巩固。鉴于记忆再激活被认为优先发生在慢振荡上行状态期间，我们假设TMR刺激效果将取决于慢振荡的相位。参与者学习了与特定声音（如猫叫声）配对的物体的任意空间位置。然后，在下午小睡的慢波睡眠期间，一半的声音以低强度呈现。随后测试物体位置记忆时，睡眠期间得到提示的那些物体的回忆准确率明显更高。我们在此首次报告，这种记忆益处是由刺激时的慢波相位预测的。对于得到提示的物体，根据午睡前后遗忘的程度对位置记忆进行分类。高遗忘与低遗忘的情况对应于不同慢振荡相位的刺激时间，这表明与学习相关的刺激在慢振荡的最佳相位出现时更有可能被处理并触发记忆再激活。这些发现为睡眠期间记忆再激活的机制提供了见解，支持了再激活最有可能发生在皮质上行状态期间的观点。
慢波睡眠（SWS）的特征是同步神经活动在活跃的上行状态和安静的下行状态之间交替。慢振荡上行状态被认为为记忆巩固提供了一个机会窗口，特别有利于皮质可塑性。最近的证据表明，与先前学习相关的感觉线索可以在慢波睡眠期间巧妙地传递，以选择性地增强记忆巩固。我们的结果表明，这种行为益处是由刺激呈现时的慢振荡相位预测的。根据后续回忆表现的分析，与高遗忘和低遗忘相关的线索在相反的慢振荡相位传递。这些结果提供了睡眠期间记忆巩固的最佳慢振荡相位的证据，支持了记忆处理优先发生在皮质上行状态期间的观点。
