Development of learning and memory in mice after brief paradoxical sleep deprivation

Shiromani, Priyattam J.; Gutwein, Baruch M.; Fishbein, William

doi:10.1016/0031-9384(79)90343-3

Cited by 43 publications

(17 citation statements)

References 18 publications

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“…These results agree with previous animal studies using various sleep-deprivation protocols and learning test paradigms that have consistently shown that post-training REM sleep deprivation can partially or even totally block improved performance (Fishbein, 1971;Pearlman, 1973;Pearlman and Becker, 1973;Shiromani and Fishbein, 1979;Smith and Butler, 1982;Smith et al, 1998). In addition to mechanical deprivation methods, another study has shown that during the post-training REM sleep window, intraperitoneal injection of the general protein synthesis inhibitor anisomycin and the cholinergic antagonist scopolamine induces marked learningmemory impairment in the rat .…”

Section: Effects Of Rem Sleep Deprivation On Learning Performancesupporting

confidence: 90%

Activation of Phasic Pontine-Wave Generator Prevents Rapid Eye Movement Sleep Deprivation-Induced Learning Impairment in the Rat: A Mechanism for Sleep-Dependent Plasticity

Datta¹,

Mavanji²,

Ulloor³

et al. 2004

J. Neurosci.

150

167

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Animal and human studies of sleep and learning have demonstrated that training on various tasks increases subsequent rapid eye movement (REM) sleep and phasic pontine-wave (P-wave) activity, followed by improvement in performance on the learned task. It is well documented that REM sleep deprivation after learning trials blocks the expected improvement in performance on subsequent retesting. Our aim was to test whether experimentally induced P-wave generator activation could eliminate the learning impairment produced by post-training REM sleep deprivation. Rats were trained on a two-way active avoidance-learning task. Immediately thereafter, two groups of those rats received a control vehicle (100 nl saline) microinjection and one group received a carbachol (50 ng in 100 nl saline) microinjection into the P-wave generator. The carbachol-injected group and one of the two control saline microinjected groups were selectively deprived of REM sleep during a 6 hr polygraphic recording session. All rats were then tested on the avoidance-learning task. The rats that received both the control saline injection and REM sleep deprivation showed learning deficits compared with the control saline-injected rats that were allowed to sleep normally. In contrast, the rats that received the carbachol microinjection and REM sleep deprivation demonstrated normal learning. These results demonstrate, for the first time, that carbachol-induced activation of the P-wave generator prevents the memory-impairing effects of post-training REM sleep deprivation. This evidence supports our hypothesis that the activation of the P-wave generator during REM sleep deprivation enhances a physiological process of memory, which occurs naturally during post-training REM sleep.

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Section: Effects Of Rem Sleep Deprivation On Learning Performancesupporting

confidence: 90%

Activation of Phasic Pontine-Wave Generator Prevents Rapid Eye Movement Sleep Deprivation-Induced Learning Impairment in the Rat: A Mechanism for Sleep-Dependent Plasticity

Datta¹,

Mavanji²,

Ulloor³

et al. 2004

J. Neurosci.

150

167

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“…Despite early insight (Jenkins and Dallenbach 1924), it was not until the 1970s that science began to recognize the key role of sleep in memory consolidation. The main findings supporting this view are the detrimental effects of sleep deprivation on learning (Pearlman 1969(Pearlman , 1973Leconte and Bloch 1970;Fishbein 1971;Pearlman and Becker 1974;Linden et al 1975;Shiromani et al 1979;Smith and Butler 1982;Smith and Kelly 1988;Smith and MacNeill 1993;Karni et al 1994;Smith and Rose 1996;Stickgold et al 2000a;Walker et al 2002;Maquet et al 2003;Mednick et al 2003), the improved memory retention in rats when REM sleep is enhanced (Wetzel et al 2003), the increase in sleep amounts following memory acquisition (Lucero 1970;Leconte and Hennevin 1971;Fishbein et al 1974;Smith et al 1974Smith et al , 1980Smith andLapp 1986, 1991;Smith and Wong 1991), and the fact that theta rhythm, a learning-related (Adey et al 1960;Elazar and Adey 1967;Landfield et al 1972;Bennett 1973;Bennett et al 1973;Winson 1978;Sederberg et al 2003) hippocampal oscillation typical of high arousal (Green and Arduini 1954;Brown 1968;Sainsbury 1970;Harper 1971;<...>…”

supporting

confidence: 48%

Reverberation, storage, and postsynaptic propagation of memories during sleep

Ribeiro¹,

Nicolelis²

2004

Learn. Mem.

131

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In mammals and birds, long episodes of nondreaming sleep ("slow-wave" sleep, SW) are followed by short episodes of dreaming sleep ("rapid-eye-movement" sleep, REM). Both SW and REM sleep have been shown to be important for the consolidation of newly acquired memories, but the underlying mechanisms remain elusive. Here we review electrophysiological and molecular data suggesting that SW and REM sleep play distinct and complementary roles on memory consolidation: While postacquisition neuronal reverberation depends mainly on SW sleep episodes, transcriptional events able to promote long-lasting memory storage are only triggered during ensuing REM sleep. We also discuss evidence that the wake-sleep cycle promotes a postsynaptic propagation of memory traces away from the neural sites responsible for initial encoding. Taken together, our results suggest that basic molecular and cellular mechanisms underlie the reverberation, storage, and propagation of memory traces during sleep. We propose that these three processes alone may account for several important properties of memory consolidation over time, such as deeper memory encoding within the cerebral cortex, incremental learning several nights after memory acquisition, and progressive hippocampal disengagement.In mammals and birds, long episodes of nondreaming sleep ("slow-wave" sleep, SW) are followed by short episodes of dreaming sleep ("rapid-eye-movement" sleep, REM) (Aserinsky and Kleitman 1953; Dement and Kleitman 1957a,b;Dement 1958;Jouvet et al. 1959;Roffwarg et al. 1962;Tradardi 1966;Jouvet 1967;Rechtschaffen and Kales 1968;Ayala-Guerrero et al. 2003). Despite early insight (Jenkins and Dallenbach 1924), it was not until the 1970s that science began to recognize the key role of sleep in memory consolidation. The main findings supporting this view are the detrimental effects of sleep deprivation on learning (Pearlman 1969(Pearlman , 1973Leconte and Bloch 1970;Fishbein 1971;Pearlman and Becker 1974;Linden et al. 1975;Shiromani et al. 1979;Smith and Butler 1982;Smith and Kelly 1988;Smith and MacNeill 1993;Karni et al. 1994;Smith and Rose 1996;Stickgold et al. 2000a;Walker et al. 2002;Maquet et al. 2003;Mednick et al. 2003), the improved memory retention in rats when REM sleep is enhanced (Wetzel et al. 2003), the increase in sleep amounts following memory acquisition (Lucero 1970;Leconte and Hennevin 1971;Fishbein et al. 1974;Smith et al. 1974Smith et al. , 1980Smith andLapp 1986, 1991;Smith and Wong 1991), and the fact that theta rhythm, a learning-related (Adey et al. 1960;Elazar and Adey 1967;Landfield et al. 1972;Bennett 1973;Bennett et al. 1973;Winson 1978;Sederberg et al. 2003) hippocampal oscillation typical of high arousal (Green and Arduini 1954;Brown 1968;Sainsbury 1970;Harper 1971;Arnolds et al. 1980;Stewart and Fox 1991;Kahana et al. 1999), also characterizes REM sleep (Vanderwolf 1969;Timo-Iaria et al. 1970;Winson 1974;Cantero et al. 2003). Given the involvement of the hippocampus in memory acquisition (Scoville and Milner 1957;Mishkin 1978;Kesner...

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“…We are not the first to show that REM sleep deprivation is not associated with concurrent performance deficits (Albert et al 1970;Miller et al 1971;Sloan 1972;Shiromani et al 1979;Van Hulzen and Coenen 1979;Marti-Nicolovius et al 1988;Gisquet-Verrier and Smith 1989;Yang et al 2002). Even across the studies reporting REM sleep deprivation-associated deficits in performance, the results can be varying or contradictory (e.g., Youngblood et al 1997;Yang et al 2002;Ruskin et al 2006).…”

Section: Initial Spatial Learning Concurrent To Rem Sleep Deprivationmentioning

confidence: 90%

“…To date, there has been much controversy on whether learning is facilitated by REM sleep (Fishbein 1971;Pearlman 1973;Leconte et al 1974;Fishbein and Gutwein 1977;Gutwein and Fishbein 1980a,b;Smith and Butler 1982;Hars et al 1985;Smith 1985Smith , 1995Smith and Lapp 1991;Smith and Wong 1991;Hennevin et al 1995;Rose 1996, 1997;Youngblood et al 1997;Smith et al 1998;Poe et al 2000;Le Marec et al 2001;Bjorness et al 2005;Silvestri 2005;Fu et al 2007;Yang et al 2008;Li et al 2009;Wang et al 2009) or is independent of REM sleep (Albert et al 1970;Miller et al 1971;Sloan 1972;McGrath and Cohen 1978;Shiromani et al 1979;Van Hulzen and Coenen 1979;Horne and McGrath 1984;Smith 1985;Horne 1988;Yang et al 2008). Only a few studies have focused on the effect of REM sleep deprivation on the consolidation of spatial learning Rose 1996, 1997;Youngblood et al 1997;Bjorness et al 2005;Yang et al 2008;Li et al 2009;Wang et al 2009).…”

Section: Is Rem Sleep Essential For Learning?mentioning

confidence: 99%

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

Walsh

Booth²,

Poe³

2011

Learn. Mem.

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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

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Development of learning and memory in mice after brief paradoxical sleep deprivation

Cited by 43 publications

References 18 publications

Activation of Phasic Pontine-Wave Generator Prevents Rapid Eye Movement Sleep Deprivation-Induced Learning Impairment in the Rat: A Mechanism for Sleep-Dependent Plasticity

Activation of Phasic Pontine-Wave Generator Prevents Rapid Eye Movement Sleep Deprivation-Induced Learning Impairment in the Rat: A Mechanism for Sleep-Dependent Plasticity

Reverberation, storage, and postsynaptic propagation of memories during sleep

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

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