The role of sleep in the organization of spatial representations during memory formation
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2022
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Abstract
The study of place cells, discovered by O'Keefe (1971), has focused the spatial representation system in the processes and functions led by the hippocampus. Among these functions, the hippocampus plays a preponderant role in establishing spatial memory, in which sleep is fundamental, suggesting a plausible relationship between sleep and the spatial representations provided by place cells. In this line, there is intense research to establish whether sleep participates in the consolidation and configuration of spatial representations given by place cells and if this is related to spatial memory performance.
In this study, we evaluated the influence of sleep on the variations in the configuration of a spatial map given by changes in spatial context during a spatial memory task. Specifically, we first evaluated the influence of sleep on the performance of a spatial memory task, the object in place recognition (OPR), and performed single unit and local field potential recordings in the dorsal CA1 hippocampus in adult rats. Then, we evaluated the influence of sleep and its cardinal oscillations in the configuration of the spatial representations generated by place cells during OPR.
Our results show that sleep, specifically non-REM sleep, and its oscillatory patterns (SWRs, spindles, and delta waves), are directly correlated with performance in the OPR memory test. In addition, concerning single-unit recordings, we detected and isolated 612 units. In this line, the detection and classification of individual units were implemented successfully, which was crucial to evaluate the representation system by detecting place cells. We selected units according to their spatial activity, where 41 % were classified as place cells, and the remaining 59 % were classified as non-spatial cells. Also, during post-learning sleep, place cells were highly time-correlated with non-REM oscillatory patterns, like SWRs and spindles. In addition, we evaluated mean firing rate and sparsity during the OPR task showing a general and sleep-independent increase in both parameters after sleep, which is possibly associated with novelty during test. Also, there was a sleep-dependent decrease in mean firing rate during post-learning sleep. Finally, we evaluated the stability of the spatial map on the task through a spatial correlation vector, showing that spatial stability in the novel, but not in the familiar arena zone, decreased associated with a longer duration of post-learning sleep.
In conclusion, our results suggest that Non-REM sleep and its oscillations affected spatial representation through the flexibility in the configuration of spatial maps due to changes in the environment. This is also associated with improved spatial memory since instability of place cell spatial configuration is relevant for memory updating during environment exploration.
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Tesis (Doctor en Neurociencia)--Pontificia Universidad Católica de Chile, 2022