Abstract
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 (SOs), 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-hour retention interval during which the sleep-associated EEG and hippocampal local field potentials (LFP) 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 SO-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.
SIGNIFICANT 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.
Footnotes
The authors declare no competing interests.
We thank Ilona Sauter for technical assistance. We thank Carlos Oyanedel, Ernesto Duran, Shan Xia, Eva-Maria Kurz and Ioannis Zouridis for help with conducting the experiments and data analysis. This research was supported by grants from the Deutsche Forschungsgemeinschaft to M.I. (DFG In 279/1-1) and the European Research Council to J.B. (ERC AdG 883098 SleepBalance). MI is supported by the Hertie Foundation (Hertie Network of Excellence in Clinical Neuroscience).
