Activation of the phasic pontine‐wave generator enhances improvement of learning performance: a mechanism for sleep‐dependent plasticity

Abstract

The aim of this study was to test the hypothesis that supplementary activation of the phasic pontine wave (P-wave) generator during rapid eye movement (REM) sleep enhances consolidation and integration of memories, resulting in improved learning. To test this hypothesis, two groups of rats were trained on a two-way active avoidance learning task in the morning. Immediately after training, one group of rats received a carbachol microinjection into the P-wave generator and the other group was microinjected with control saline into the same target area. After training trials and microinjections, rats were allowed a 6-h period of undisturbed sleep in the polygraphic recording chamber. At the end of 6 h of undisturbed sleep-wake recordings, rats were retested in a session of avoidance learning trials. After learning trials, the total percentage of time spent in REM sleep was significantly increased in both saline (15.36%)- and carbachol (17.70%)-microinjected rats. After learning trials, REM sleep P-wave density was significantly greater throughout the 6-h period of recordings in carbachol treated rats than in the saline treated rats. In the retrial session, the improvement in learning task performance was 22.75% higher in the carbachol-microinjected rats than in the saline-microinjected rats. These findings show that the consolidation and integration of memories create a homeostatic demand for P-waves. In addition, these findings provide experimental evidence, for the first time, that activation of the P-wave generator may enhance consolidation and integration of memories, resulting in improved performance on a recently learned task.

A role for sleep in brain plasticity

“…the pontine component of PGO-type waves recorded in rats) density not only substantially increases after aversive conditioning in rats [149], but the percentage of changes in P-wave density between REM sleep episodes was shown proportional to the improvement of task performance between sessions [72]. Moreover, activation of the phasic P-wave generator by carbachol microinjections is coupled with enhanced performance improvement on a two-way active avoidance learning task [154] and would eliminate the learning impairment produced by post-training REM sleep deprivation [155]. When induced by brainstem stimulation [156], PGO waves synchronize high-frequency activities , the expression of which can be experience-dependent during sleep [142].…”

Electrophysiological characterization of neurons in the dorsolateral pontine rapid-eye-movement sleep induction zone of the rat: Intrinsic membrane properties and responses to carbachol and orexins

“…Neurons in the SubC area neighbouring the brachium conjunctivum fire synchronized bursts preceding and phase-locked to PGO waves (McCarley et al, 1978;Sakai and Jouvet, 1980;Steriade et al, 1990;Datta, 1997), the pontine component of which (P-waves) can be recorded in rats using low-resistance electrodes Kaufman and Morrison, 1981;Datta et al, 1998). Small injections of carbachol into the SubC in the rat elicits an increase in the frequency of PGO waves which is correlated with a facilitation of learning and memory formation (Mavanji and Datta, 2003;Datta et al, 2004).…”

“…Neurons in the SubC area neighbouring the brachium conjunctivum fire synchronized bursts preceding and phase-locked to PGO waves (McCarley et al, 1978;Sakai and Jouvet, 1980;Steriade et al, 1990;Datta, 1997), the pontine component of which (P-waves) can be recorded in rats using low-resistance electrodes Kaufman and Morrison, 1981;Datta et al, 1998). Small injections of carbachol into the SubC in the rat elicits an increase in the frequency of PGO waves which is correlated with a facilitation of learning and memory formation (Mavanji and Datta, 2003;Datta et al, 2004).Previous in vitro intracellular recordings from reticular neurons in the pons have focused upon neurons located more medially and ventrally than the SubC in the nucleus pontine nucleus oralis (PnO) and pontine nucleus caudalis (PnC) (Greene et al, 1986;Gerber et al, 1989;Nunez et al, 1997). In addition, no data are available regarding the responses of SubC neurons in the rat to neurotransmitters involved in behavioural state control.…”

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

“…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.g., Rose 1996, 1997;Youngblood et al 1997;Smith et al 1998;Beaulieu and Godbout 2000;Le Marec et al 2001;Bjorness et al 2005;Ruskin et al 2006;Yang et al 2008;Li et al 2009;Wang et al 2009), which is hippocampus-dependent.…”