Institute of Neuroscience, Newcastle University, Newcastle NE2 4HH, United Kingdom.
Institute of Neuroscience, Newcastle University, Newcastle NE2 4HH, United Kingdom
J Neurosci. 2019 May 8;39(19):3698-3712. doi: 10.1523/JNEUROSCI.1408-18.2019. Epub 2019 Mar 6.
Sequential firing of neurons during sleep is thought to play a role in the consolidation of learning. However, direct evidence for such sequence replay is limited to only a few brain areas and sleep states mainly in rodents. Using a custom-designed wearable neural data logger and chronically implanted electrodes, we made long-term recordings of neural activity in the primary motor cortex of two female nonhuman primates during free behavior and natural sleep. We used the local field potential (LFP) spectrogram to characterize sleep cycles, and examined firing rates, correlations, and sequential firing of neurons at different frequency bands through the cycle. Slow-wave sleep (SWS) was characterized by low neural firing rates and high synchrony, reflecting slow oscillations between cortical down and up states. However, the order in which neurons entered up states was similar to the sequence of neural activity observed at low frequencies during waking behavior. In addition, we found evidence of brief bursts of theta oscillation, associated with non-SWS states, during which neurons fired in strikingly regular sequential order phase-locked to the LFP. Theta sequences were preserved between waking and sleep, but appeared not to resemble the order of neural activity observed at lower frequencies. The sequential firing of neurons during slow oscillations and theta bursts may contribute to the consolidation of procedural memories during sleep. Replay of sequential neural activity during sleep is believed to support consolidation of daytime learning. Despite a wealth of studies investigating sequential replay in association with episodic and spatial memory, it is unknown whether similar sequences occur in motor areas during sleep. Within long-term neural recordings from monkey motor cortex, we found two distinct patterns of sequential activity during different phases of the natural sleep cycle. Slow-wave sleep was associated with delta-band sequences that resembled low-frequency activity during movement, while occasional brief bursts of theta oscillation were associated with a different order of sequential firing. Our results are the first report of sequential sleep replay in the motor cortex, which may play an important role in consolidation of procedural learning.
在睡眠期间神经元的顺序放电被认为在学习的巩固中起作用。然而，这种序列回放的直接证据仅限于少数几个脑区和主要在啮齿动物中的睡眠状态。使用定制设计的可穿戴神经数据记录器和慢性植入电极，我们在两只雌性非人类灵长类动物的初级运动皮层中进行了长期的自由行为和自然睡眠期间的神经活动记录。我们使用局部场电位（LFP）频谱图来描述睡眠周期，并通过整个周期检查不同频段的神经元的放电率、相关性和顺序放电。慢波睡眠（SWS）的特征是神经元放电率低且同步性高，反映了皮质下和上状态之间的缓慢振荡。然而，神经元进入上状态的顺序与在清醒行为期间观察到的低频神经活动的序列相似。此外，我们发现了与非 SWS 状态相关的短暂 theta 振荡爆发的证据，在此期间，神经元以惊人的规则顺序放电，与 LFP 相位锁定。theta 序列在清醒和睡眠之间被保留，但似乎与在较低频率下观察到的神经活动的顺序不同。在慢波振荡和 theta 爆发期间神经元的顺序放电可能有助于睡眠期间程序性记忆的巩固。睡眠期间的神经活动回放被认为支持白天学习的巩固。尽管有大量研究调查与情景和空间记忆相关的序列回放，但尚不清楚在睡眠期间运动区域是否会发生类似的序列。在猴子运动皮层的长期神经记录中，我们发现自然睡眠周期的不同阶段存在两种不同的序列活动模式。慢波睡眠与 delta 波段序列相关，这些序列类似于运动期间的低频活动，而偶尔的 theta 爆发短暂爆发与不同的顺序放电顺序相关。我们的结果首次报道了运动皮层中的序列睡眠回放，这可能在程序性学习的巩固中起重要作用。
