Spatial and reversal learning in the Morris water maze are largely resistant to six hours of REM sleep deprivation following training

Abstract

This first test of the role of REM (rapid eye movement) sleep in reversal spatial learning is also the first attempt to replicate a much cited pair of papers reporting that REM sleep deprivation impairs the consolidation of initial spatial learning in the Morris water maze. We hypothesized that REM sleep deprivation following training would impair both hippocampusdependent spatial learning and learning a new target location within a familiar environment: reversal learning. A 6-d protocol was divided into the initial spatial learning phase (3.5 d) immediately followed by the reversal phase (2.5 d). During the 6 h following four or 12 training trials/day of initial or reversal learning phases, REM sleep was eliminated and non-REM sleep left intact using the multiple inverted flowerpot method. Contrary to our hypotheses, REM sleep deprivation during four or 12 trials/day of initial spatial or reversal learning did not affect training performance. However, some probe trial measures indicated REM sleep-deprivation-associated impairment in initial spatial learning with four trials/ day and enhancement of subsequent reversal learning. In naive animals, REM sleep deprivation during normal initial spatial learning was followed by a lack of preference for the subsequent reversal platform location during the probe. Our findings contradict reports that REM sleep is essential for spatial learning in the Morris water maze and newly reveal that short periods of REM sleep deprivation do not impair concurrent reversal learning. Effects on subsequent reversal learning are consistent with the idea that REM sleep serves the consolidation of incompletely learned items.While it has been widely shown that both total sleep deprivation and sleep fragmentation impair learning, there remains much debate over the role of REM sleep deprivation for learning (for reviews, see Smith 1995;Hobson and Pace-Schott 2002;Vertes 2004;Rauchs et al. 2005;Stickgold and Walker 2005;Vertes and Siegel 2005). Increases in REM sleep have been described following learning (e.g., Lucero 1970;Hennevin et al. 1971;Leconte and Hennevin 1971;Fishbein et al. 1974;Smith et al. 1980;Smith and Butler 1982;Smith and Lapp 1986;Portell-Cortes et al. 1989;Smith and Wong 1991;Bramham et al. 1994;Smith and Rose 1997;Mavanji and Datta 2003) that imply a functional relationship. Some studies suggest that REM sleep is tightly linked with specific types of learning such as spatial learning (e

Effects of acute sleep deprivation on motor and reversal learning in mice

“…These observations are consistent with prior studies showing deficits in reversal learning in a land Y-maze with food rewards following chronic sleep deprivation (Hagewoud et al, 2010b), although interestingly, in that study a greater deficit in reversal was seen when the chronic sleep deprivation occurred after training trials than after reversal trials. While some forms of spatial reversal learning in rats appear to be resistant to either REM sleep deprivation (Walsh et al, 2011) or 12 hours of total sleep deprivation prior to the opportunity for reversal (Leenaars et al, 2012a), our findings are predominantly consistent with effects of sleep deprivation on related tasks requiring prefrontal and orbitofrontal cortex such as task-switching in both rats (Leenaars et al, 2012b) and humans (Bratzke et al, 2009) and in extra-dimensional set shifting in rats (McCoy et al, 2007). …”

Animal Studies on the Role of Sleep in Memory: From Behavioral Performance to Molecular Mechanisms

“…The observation that REM sleep is critical for the spatial learning in the Morris water maze has been confirmed by some laboratories (Youngblood et al 1997;Guan et al 2004;Yang et al 2008;Li et al 2009), but not by some others (Wang et al 2009;Walsh et al 2011). The apparent inconsistent findings on the consequences of sleep deprivation in the water maze may be explained by the fact that animals while undergoing training can adopt alternative behavioral learning strategies that are not necessarily dependent on the hippocampus (Bjorness et al 2005;Hairston et al 2005).…”

Antidepressant Suppression of Non-REM Sleep Spindles and REM Sleep Impairs Hippocampus-Dependent Learning While Augmenting Striatum-Dependent Learning

“…Here we report for the first time that REM suppression impairs reconsolidation of a familiar spatial memory, and that the often overlooked transition-to-REM sleep state (TR) is involved in the process of new memory consolidation (Walsh et al, 2011). Both reconsolidation and novel memory consolidation are dependent on normal hippocampal activity (Morris et al, 1986; van der Meulen et al, 2003).…”

“…DMI has a relatively low side effect profile (Goodman et al, 2006) and elevates noradrenaline (NA) at all targets of the locus ceoruleus (LC), suppressing REM sleep through inactivation of REM-ON cholinergic pontine neurons (Baumann et al, 1983). Short term REM sleep deprivation following new hippocampus dependent learning can impair consolidation, depending on the type of task being performed and the intensity of training (Smith et al, 1998; Bjorness et al, 2005; Walsh et al, 2011), while striatal dependent procedural learning is largely unaffected by REM sleep deprivation (Wimmer et al, 1992; Smith et al, 1998; Bjorness et al, 2005; Hagewoud et al, 2010; Walsh et al, 2011). Individuals using REM sleep suppressing antidepressants do not self-report marked reductions in memory function beyond those already associated with depression, although some have been documented (Brooks and Hoblyn, 2007).…”