Plasticity within the corticostriatal network is known to regulate the balance between behavioral flexibility and automaticity. Repeated training of an action has been shown to bias behavior towards automaticity, suggesting that training may trigger activity-dependent corticostriatal plasticity. However, surprisingly little is known about the natural activity patterns that may drive plasticity or when they occur during long-term training. Here we chronically monitored neural activity from primary motor cortex (M1) and the dorsolateral striatum (DLS) during both training and offline periods, i.e., time away from training including sleep, throughout the development of an automatic reaching action. We first show that blocking striatal NMDA receptors during offline periods prevents the emergence of behavioral consistency, a hallmark of automaticity. We then show that, throughout the development of an automatic reaching action, corticostriatal functional connectivity increases during offline periods. Such increases track the emergence of consistent behavior and predictable cross-area neural dynamics. We then identify sleep spindles during non-REM sleep (NREM) as uniquely poised to mediate corticostriatal plasticity during offline periods. We show that sleep spindles are periods of maximal corticostriatal transmission within offline periods, that sleep spindles in post-training NREM reactivate neurons across areas, and that sleep-spindle modulation in post-training NREM is linked to observable changes in spiking relationships between individual pairs of M1 and DLS neurons. Our results indicate that offline periods, in general, and sleep spindles, specifically, play an important role in regulating behavioral flexibility through corticostriatal network plasticity.

中文翻译：

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睡眠纺锤体在自动出现时协调皮层皮质的激活

已知皮质皮质网络中的可塑性调节行为灵活性和自动性之间的平衡。已经证明，重复训练某个动作会使行为偏向于自动化，这表明训练可能会触发依赖于活动的皮质纹状体可塑性。但是，令人惊讶的是，对于可能促进可塑性或当它们在长期训练中发生的自然活动模式知之甚少。在这里，我们在训练和脱机期间（即远离训练包括睡眠的时间），在自动达成动作的发展过程中，长期监测来自初级运动皮层（M1）和背外侧纹状体（DLS）的神经活动。我们首先表明，在离线时期阻断纹状体NMDA受体可防止行为一致性的出现，这是自动化的标志。然后，我们表明，在自动到达动作的整个开发过程中，皮质下颌骨功能连接在离线期间会增加。这样的增加跟踪了一致行为和可预测的跨区域神经动力学的出现。然后，我们将非快速眼动睡眠（NREM）期间的睡眠纺锤体确定为在离线期间介导皮层皮质可塑性的独特位置。我们显示睡眠纺锤体是离线时期内最大皮质皮质通道传输的时期，训练后NREM中的睡眠纺锤体会重新激活跨区域的神经元，训练后NREM中的睡眠纺锤体调制与各个对之间的尖峰关系的可观察到的变化有关M1和DLS神经元。我们的结果表明，一般来说，离线时期和睡眠纺锤特别是，