During early development, memory systems gradually mature over time, in parallel with the gradual accumulation of knowledge. Yet, it is unknown whether and to what extent maturation is driven by discrete experience. Sleep is thought to contribute to the formation of long-term memory and knowledge through a systems consolidation process that is driven by specific sleep oscillations (i.e., ripples, spindles, and slow oscillations) in cortical and hippocampal networks. Based on these oscillatory signatures, we show here in rats that discrete spatial experience speeds the functional maturation of spatial memory systems during development. Juvenile male rats were exposed for 5 min periods to changes in the spatial configuration of two identical objects on postnatal day (PD)25, PD27, and PD29 (Spatial experience group), while a Control group was exposed on these occasions to the same two objects without changing their positions. On PD31, both groups were tested on a classical Object Place Recognition (OPR) task with a 3 h retention interval during which the sleep-associated EEG and hippocampal local field potentials were recorded. On PD31, consistent with forgoing studies, Control rats still did not express OPR memory. By contrast, rats with Spatial experience formed significant OPR memory and, in parallel, displayed an increased percentage of hippocampal ripples coupled to parietal slow oscillation-spindle complexes, and a stronger ripple-spindle phase-locking during the retention sleep. Our findings support the idea that experience promotes the maturation of memory systems during development by enhancing cortico-hippocampal information exchange and the formation of integrated knowledge representations during sleep.

SIGNIFICANCE STATEMENT Cognitive and memory capabilities mature early in life. We show here that and how discrete spatial experience contributes to this process. Using a simple recognition paradigm in developing rats, we found that exposure of the rat pups to three short-lasting experiences enhances spatial memory capabilities to adult-like levels. The adult-like capability of building spatial memory was connected to a more precise coupling of ripples in the hippocampus with slow oscillation-spindle complexes in the thalamo-cortical system when the memory was formed during sleep. Our findings support the view that discrete experience accelerates maturation of cognitive and memory capabilities by enhancing the dialogue between hippocampus and cortex when these experiences are reprocessed during sleep.

在早期发展过程中，记忆系统随着时间的推移逐渐成熟，同时知识也逐渐积累。然而，尚不清楚成熟是否以及在多大程度上是由离散经验驱动的。睡眠被认为通过由皮层和海马网络中特定的睡眠振荡（即波纹、纺锤波和慢振荡）驱动的系统巩固过程有助于长期记忆和知识的形成。基于这些振荡特征，我们在大鼠身上表明，离散的空间体验加速了空间记忆系统在发育过程中的功能成熟。幼年雄性大鼠在出生后 (PD)25、PD27 和 PD29（空间体验组）暴露于两个相同物体的空间配置变化 5 分钟，而对照组在这些情况下暴露于相同的两个物体物体不改变其位置。在 PD31 上，两组均接受了经典物体位置识别 (OPR) 任务的测试，保留时间间隔为 3 小时，在此期间记录了与睡眠相关的脑电图和海马局部场电位。在 PD31 上，与之前的研究一致，对照大鼠仍然不表达 OPR 记忆。相比之下，具有空间体验的大鼠形成了显着的 OPR 记忆，同时在保留睡眠期间表现出与顶叶慢振荡-纺锤体复合体耦合的海马波纹百分比增加，以及更强的波纹-纺锤体锁相。我们的研究结果支持这样的观点，即经验通过增强皮质-海马信息交换和睡眠期间综合知识表征的形成，促进发育过程中记忆系统的成熟。

意义陈述认知和记忆能力在生命早期就成熟了。我们在这里展示了离散的空间体验如何促进这一过程。在发育中的老鼠中使用简单的识别范式，我们发现，让幼鼠接触三种短暂的经历，可以将空间记忆能力增强到类似成人的水平。当记忆在睡眠期间形成时，类似成人的空间记忆形成能力与海马体波纹与丘脑皮质系统中缓慢振荡纺锤体复合体更精确的耦合有关。我们的研究结果支持这样的观点，即当这些经验在睡眠期间重新处理时，离散经验可以通过增强海马体和皮层之间的对话来加速认知和记忆能力的成熟。