Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas.

Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas.
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DOI:
10.1371/journal.pbio.0020024
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发表时间:
2004-01
期刊:
影响因子:
9.8
通讯作者:
Nicolelis MA
Nicolelis MA
中科院分区:
生物学1区
文献类型:
--
作者:
Ribeiro S;Gervasoni D;Soares ES;Zhou Y;Lin SC;Pantoja J;Lavine M;Nicolelis MA

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在慢波(SW)和快速眼动(REM)睡眠期间发现的经验依赖性大脑再激活导致了最近获得的记忆痕迹的巩固需要睡眠期间的神经重放的概念。然而,到目前为止,一些观察结果继续破坏这一假设。为了解决这些异议,我们研究了短暂的新经验对大鼠前脑神经元活动长期演变的影响。我们观察到,最初产生的触觉探索新的对象的神经元合奏活动的时空模式复发长达48小时,在大脑皮层,海马,壳核,丘脑。这种新颖性诱导的复发的特点是低,但显着的相关性值。当动物在物体之间移动而不接触它们时,神经元活动的采样结果几乎相同。相反,当动物探索熟悉的环境时,观察到的神经元模式可以忽略不计的复发。虽然过去的神经元活动模式的混响是最强的SW睡眠,清醒与神经元混响的减少。快速眼动睡眠在动物中表现出更多的可变结果。在与海马位置细胞的数据相比,我们没有发现任何证据的时间压缩或扩大的采样前脑区的神经元混响。我们的研究结果表明,持续的经验依赖性神经元混响是一个多前脑结构的一般属性。它并不包括对先前活动的精确重放,而是定义了对显著神经集合放电模式的温和且一致的偏好。这些结果与缓慢和渐进的记忆巩固过程相一致,反映了新奇相关的神经元集合关系,似乎是上下文而不是刺激特异性的。根据我们目前和以前的研究结果,我们提出,睡眠的两个主要阶段发挥不同的和互补的作用,在记忆巩固:转录前回忆在SW睡眠和转录存储在REM睡眠。在清醒期间暴露于新物体的大鼠产生的神经活动与随后的睡眠事件中观察到的模式相关
The discovery of experience-dependent brain reactivation during both slow-wave (SW) and rapid eye-movement (REM) sleep led to the notion that the consolidation of recently acquired memory traces requires neural replay during sleep. To date, however, several observations continue to undermine this hypothesis. To address some of these objections, we investigated the effects of a transient novel experience on the long-term evolution of ongoing neuronal activity in the rat forebrain. We observed that spatiotemporal patterns of neuronal ensemble activity originally produced by the tactile exploration of novel objects recurred for up to 48 h in the cerebral cortex, hippocampus, putamen, and thalamus. This novelty-induced recurrence was characterized by low but significant correlations values. Nearly identical results were found for neuronal activity sampled when animals were moving between objects without touching them. In contrast, negligible recurrence was observed for neuronal patterns obtained when animals explored a familiar environment. While the reverberation of past patterns of neuronal activity was strongest during SW sleep, waking was correlated with a decrease of neuronal reverberation. REM sleep showed more variable results across animals. In contrast with data from hippocampal place cells, we found no evidence of time compression or expansion of neuronal reverberation in any of the sampled forebrain areas. Our results indicate that persistent experience-dependent neuronal reverberation is a general property of multiple forebrain structures. It does not consist of an exact replay of previous activity, but instead it defines a mild and consistent bias towards salient neural ensemble firing patterns. These results are compatible with a slow and progressive process of memory consolidation, reflecting novelty-related neuronal ensemble relationships that seem to be context- rather than stimulus-specific. Based on our current and previous results, we propose that the two major phases of sleep play distinct and complementary roles in memory consolidation: pretranscriptional recall during SW sleep and transcriptional storage during REM sleep. Rats exposed to novel objects during periods of wakefulness generate neural activity that is correlated with patterns observed in subsequent sleep episodes
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