Sleep deprivation impairs spatial retrieval but not spatial learning in the non-human primate grey mouse lemur.

Anisur Rahman,Alexandra Auffret,Esther Schenker,Solène Languille,Fabienne Aujard,Jill Richardson,Olivier J Blin,Yves Lamberty,Martine Perret,Regis Bordet,Tom Jacob,Fabien Pifferi,Claudio Babiloni

doi:10.1371/journal.pone.0064493

Abstract

A bulk of studies in rodents and humans suggest that sleep facilitates different phases of learning and memory process, while sleep deprivation (SD) impairs these processes. Here we tested the hypothesis that SD could alter spatial learning and memory processing in a non-human primate, the grey mouse lemur (Microcebus murinus), which is an interesting model of aging and Alzheimer's disease (AD). Two sets of experiments were performed. In a first set of experiments, we investigated the effects of SD on spatial learning and memory retrieval after one day of training in a circular platform task. Eleven male mouse lemurs aged between 2 to 3 years were tested in three different conditions: without SD as a baseline reference, 8 h of SD before the training and 8 h of SD before the testing. The SD was confirmed by electroencephalographic recordings. Results showed no effect of SD on learning when SD was applied before the training. When the SD was applied before the testing, it induced an increase of the amount of errors and of the latency prior to reach the target. In a second set of experiments, we tested the effect of 8 h of SD on spatial memory retrieval after 3 days of training. Twenty male mouse lemurs aged between 2 to 3 years were tested in this set of experiments. In this condition, the SD did not affect memory retrieval. This is the first study that documents the disruptive effects of the SD on spatial memory retrieval in this primate which may serve as a new validated challenge to investigate the effects of new compounds along physiological and pathological aging.

Highlights

Sleep is an essential component of our life and is essential for maintaining normal daily life activities and key physiological functions such as thermoregulation [1], immune defense [2], energy conservation [3], tissue restoration [4] and brain plasticity [5]
Electroencephalogram findings We first recorded the 3 days of baseline sleep-wake cycle parameters including the daily profile of slow wave sleep (SWS), paradoxical sleep (PS), active wake (AW) and quiet wake (QW)
We showed that 8 h of total sleep deprivation (SD) impaired the retrieval, but not the learning, of a one-day spatial memory task in mouse lemurs

Summary

Introduction

Sleep is an essential component of our life and is essential for maintaining normal daily life activities and key physiological functions such as thermoregulation [1], immune defense [2], energy conservation [3], tissue restoration [4] and brain plasticity [5]. Paradoxical SD is usually obtained by placing the animal on a small platform surrounded by water [14], [15] This type of manipulation has been noted to induce memory deficits in several tasks such as inhibitory avoidance [16], Morris water maze [17], [18], radial arm maze [19] and plus-maze discriminative avoidance tasks [13], [20]. Total SD is achieved by removing or introducing objects within the cages [21] or by gently handling the animals to keep them awake [22] This procedure has been shown to induce memory retrieval deficits in contextual fear conditioning, inhibitory avoidance and plus-maze discriminative avoidance tasks [23]

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