Deepened sleep makes hippocampal spatial memory more persistent

Abstract

Ample evidence has indicated a beneficial role of sleep, and particularly of slow wave sleep (SWS) in memory consolidation. However, how basic features of sleep, its depth and duration, contribute to this process remained elusive. Here, we investigated spatial object-place recognition (OPR) memory in rats, to systematically dissociate effects of sleep depth and duration on the formation of recent and remote hippocampus-dependent memory. Encoding of the spatial configuration was followed by an experimental post-encoding period of either 2 or 4 h, during which the rats had either “regular sleep”, “deeper sleep”, or were kept awake. A deeper sleep was achieved by an extended habituation of the rats to the sleep environment. Retrieval was tested either immediately after the 2-hour post-encoding period (recent memory test) or 1 week later (remote memory test). Deeper sleep expressed itself in a selective increase in the time spent in SWS, and in numbers of slow oscillations, spindles, and hippocampal ripples during SWS, whereas preREM and REM sleep were not affected. At the recent test, OPR memory was preserved only after sleep, but independent of its depth. At the remote test, however, OPR memory was preserved only after deeper sleep, whereas the wake and the regularly sleeping rats did not show remote OPR memory, even with the longer 4-h post-encoding period. Our results indicate that, rather than a longer duration, deeper sleep, i.e., a longer time in SWS together with enhanced oscillatory signatures of mnemonic processing during this sleep stage, occurring within a 2-hour window after encoding, is the factor that makes hippocampus-dependent memory more persistent.