Reverberation, storage, and postsynaptic propagation of memories during sleep

Abstract

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...

Prominent Burst Firing of Dopaminergic Neurons in the Ventral Tegmental Area during Paradoxical Sleep

“…This observation constitutes, to our knowledge, the first electrophysiological observation of such a long lasting activation of burst firing which may underlie the increase in dopamine levels reported during various behaviors such as feeding, reward, punishment, or sex (Schultz, 2002). The similarity between dopaminergic activity observed during PS and food consumption suggests that, even if sensory thresholds were high and the animal was not perceiving external stimuli, neuronal reactivations occurring during PS, throughout the brain (Louie and Wilson, 2001;Maquet et al, 2000;Peigneux et al, 2003;Ribeiro and Nicolelis, 2004), could underlie the perception of internally generated rewarding or at least salient experiences.…”

“…During the past 50 years of sleep research, PS has been associated with various functions, ranging from corneal respiration (Fitt and Gonzalez, 2006) to dreaming (Aserinsky and Kleitman, 1953). It has been proposed recently that one possible function of PS is to participate in reconsolidation of newly acquired memories during sleep via off-line replay of previously experienced events (Ribeiro and Nicolelis, 2004;Stickgold et al, 2001;Stickgold and Walker, 2005). Indeed, in humans, imaging studies showed that cerebral regions activated during learning are reactivated again during PS following the task (Maquet et al, 2000;Peigneux et al, 2003).…”

Impaired Off-Line Consolidation of Motor Memories After Combined Blockade of Cholinergic Receptors During REM Sleep-Rich Sleep

“…Candidate mechanisms supporting memory consolidation during REM sleep possibly involve increased protein synthesis and plasticity-related gene expression during this sleep stage. Whereas non-REM sleep is characterized by diminished activity of such genes and a greatly reduced ability to induce synaptic long-term potentiation, REM sleep provides a more adequate milieu of neurotransmitters and modulators for synaptic plastic changes (Ribeiro and Nicolelis, 2004;Bramham and Srebro, 1989). Ribeiro et al (Ribeiro et al, 1999 revealed an increased expression of the immediate early genes arc and zif-268 during REM sleep after induction of long-term potentiation during prior wakefulness.…”

Neuronal Correlates of Memory Formation in Motor Cortex after Adaptation to Force Field

“…Multiple brain areas (e.g., hippocampus, amygdala, cerebral cortex, striatum, cerebellum) seem to be involved in these processes (Attwell et al, 2002;Ribeiro and Nicolelis, 2004;Kassardjian et al, 2005;Ji and Wilson, 2007;Montgomery and Buzsáki, 2007;Karlsson and Frank, 2009). For example, similar cell ensembles in the amygdala of transgenic mice were found to be active during learning and retrieval of fear memory (Reijmers et al, 2007).…”