William Fishbein

A daytime nap containing solely non-REM sleep enhances declarative but not procedural memory

The specialized role that sleep-specific brain physiology plays in memory processing is being rapidly clarified with a greater understanding of the dynamic, complex, and exquisitely orchestrated brain state that emerges during sleep. Behaviorally, the facilitative role of non-REM (NREM) sleep (primarily slow wave sleep) for declarative but not procedural memory performance in humans has been demonstrated in a number of nocturnal sleep studies. However, subjects in these studies were tested after periods of sleep that contained REM sleep in addition to NREM sleep, and comparison wake groups were subjected to mild sleep deprivation. To add some clarity to the findings of these nocturnal studies, we assessed performance on declarative and procedural memory tasks following a daytime training-retest interval containing either a short nap that included NREM without REM sleep, or wakefulness. Consistent with previous findings we show that, after a comparatively brief sleep episode, subjects that take a nap improve more on a declarative memory task than subjects that stay awake, but that improvement on a procedural memory task is the same regardless of whether subjects take a nap or remain awake. Slow wave sleep was the only sleep parameter to correlate positively with declarative memory improvement. These findings are discussed with reference to the general benefits of napping and within the broader context of a growing literature suggesting a role for NREM-specific physiology for the processing of declarative memory.

Paradoxical sleep and memory storage processes

This paper advances the view that during the paradoxical sleep (PS) phase, the brain sets in motion a “chain-of-events” that is necessary for learning ability and that these events are an integral component of memory storage processes. The evidence supporting the position taken in this paper comes from experiments showing that: (1) PS deprivation (PSD), prior to training or immediately thereafter, impairs the formation of a permanent memory trace; (2) prolonged PSD following learning interferes with the state of a consolidated memory trace; (3) in the course of distributed learning, each learning session is followed by a brief augmentation of PS; (4) massed learning, in which registration of a learned response is incomplete, is followed by a protracted augmentation of PS; (5) pharmacological alterations of brain protein synthesis, cholinergic and catecholaminergic neurotransmitter activity are paralleled by the appearance or disappearance of PS periods, with concomitant changes in memory. The accumulated data suggest that the events occurring during the PS phase play an integral part in memory storage processes in two ways: (1) provide conditions which facilitate the conversion of a learned response into a stable long-term memory, and (2) actively maintain the stability of a consolidated memory trace.

Paradoxical sleep: Prolonged augmentation following learning

Abstract This experiment provides evidence that learning induces a protracted augmentation of paradoxical sleep (PS) time, lasting for at least 24 h. Albino mice are studied in a counterbalanced crossover design experiment in which each animal is used as its own baseline control and yoke control. The animals are trained for 1 h in an active avoidance task in which the experimental subjects learn to avoid shock as compared to yoke controls receiving an equal number of shocks, but are unable to escape. The statistical analyses reveal that slow wave sleep (SWS) is augmented in the experimental and yoke control subjects, whereas PS is only augmented in the experimentals. The analyses also reveal that the PS augmentation is primarily a function of a specific increase of the number of PS periods, without any change in the average duration of each PS phase. Further analyses between a slow learning group of animals and fast learners indicate that the PS augmentation is most marked in the slow learners. The results suggest that SWS augmentation is related to the CS-footshock contingency, whereas PS augmentation is a function of something quite unique about a mouse learning to escape or avoid a footshock. This study, taken together with our previous work, suggests that PS augmentation may be a neurobiological expression of the long-term process of memory consolidation.

Continuous pontine cholinergic microinfusion via mini-pump induces sustained alterations in rapid eye movement (REM) sleep ☆

Although there is much evidence that single microinjections of cholinomimetics into the pontine reticular formation (PRF) evokes rapid eye movement sleep (REMS), no study has yet demonstrated whether protracted manipulations of PRF cholinergic levels can produce sustained alteration of this sleep state. In this study, in rats, an indwelling, chronically implanted osmotic mini-pump was used to infuse carbachol, scopolamine, or saline solutions into various brainstem regions or the fourth ventricle for a period of five consecutive days. Throughout the period of pump operation, carbachol infusions chiefly in the PRF produced sustained REMS augmentation primarily during the night cycle, whereas scopolamine produced a sustained decrease in REMS primarily during the day cycle. The findings provide considerable support for a PRF cholinergic hypothesis of REMS generation and regulation and suggest that the alterations in REMS result from a muscarinic receptor mediated change in PRF neuronal activity.

Sex differences in paradoxical sleep : influences of estrus cycle and ovariectomy

Previously, we reported that paradoxical sleep (PS) is sexually dimorphic in mice and rats. Since some early studies indicate that PS is suppressed during proestrus night, it is important to know whether the estrus cycle and accompanying circulating ovarian hormones could explain the sexual dimorphism of PS. To examine this, sleep patterns of male rats were compared with those of normal cycling female rats and ovariectomized females in a 12:12 h light/dark cycle. Slow wave sleep and total sleep time are indistinguishable between the males, cycling females and ovariectomized females. However, normal males display significantly more PS than cycling females during both daytime and nighttime (average of all estrus stages). On the other hand, while ovariectomy has no visible effect on daytime sleep--the sexual dimorphism of PS is unchanged by ovariectomy--during nighttime, ovariectomy produces a selective increase of PS, eliminating the sex difference during the night. In sum, normal cycling females show no change in daytime sleep patterns across the estrus cycle, but have significantly less PS during proestrus nights than during metestrus and diestrus nights. The results indicate that the sex difference in nighttime PS is due to the suppression of PS by ovarian hormones during proestrus and, to a less extent, estrus nights. The sex difference in daytime PS, on the other hand, appears to be independent of circulating ovarian hormones.

Retrograde amnesia: electroconvulsive shock effects after termination of rapid eye movement sleep deprivation.

Mice that were deprived of rapid eye movement sleep for 2 days immediately after one-trial training in an inhibitory avoidance task and were given an electroconvulsive shock after deprivation displayed retrograde amnesia on a retention test given 24 hours later. Electroconvulsive shock produced no amnesia in comparable groups of animals that were not deprived of rapid eye movement sleep.

Daytime napping: Effects on human direct associative and relational memory

Sleep facilitates declarative memory processing. However, we know little about whether sleep plays a role in the processing of a fundamental feature of declarative memory, relational memory - the flexible representation of items not directly learned prior to sleep. Thirty-one healthy participants first learned at 12 pm two sets of face-object photograph pairs (direct associative memory), in which the objects in each pair were common to both lists, but paired with two different faces. Participants either were given approximately 90 min to have a NREM-only daytime nap (n=14) or an equivalent waking period (n=17). At 4:30 pm, participants who napped demonstrated significantly better retention of direct associative memory, as well as better performance on a surprise task assessing their relational memory, in which participants had to associate the two faces previously paired with the same object during learning. Particularly noteworthy, relational memory performance was correlated with the amount of NREM sleep during the nap, with only slow-wave sleep predicting relational memory performance. Sleep stage data did not correlate with direct associative memory retention. These results suggest an active role for sleep in facilitating multiple processes that are not limited to the mere strengthening of rote memories, but also the binding of items that were not directly learned together, reorganizing them for flexible use at a later time.

The impact of sleep duration and subject intelligence on declarative and motor memory performance: how much is enough?

Recent findings clearly demonstrate that daytime naps impart substantial memory benefits compared with equivalent periods of wakefulness. Using a declarative paired associates task and a procedural motor sequence task, this study examined the effect of two lengthier durations of nocturnal sleep [either a half night (3.5 h) or a full night (7.5 h) of sleep] on over‐sleep changes in memory performance. We also assessed whether subject intelligence is associated with heightened task acquisition and, more importantly, whether greater intelligence translates to greater over‐sleep declarative and procedural memory enhancement. Across both tasks, we demonstrate that postsleep performance gains are nearly equivalent, regardless of whether subjects obtain a half night or a full night of sleep. Remarkably, the over‐sleep memory changes observed on both tasks are very similar to findings from studies examining performance following a daytime nap. Consistent with previous research, we also observed a strong positive correlation between amount of Stage 2 sleep and motor skill performance in the full‐night sleep group. This finding contrasts with a highly significant correlation between spectral power in the spindle frequency band (12–15 Hz) and motor skill enhancement only in the half‐night group, suggesting that sigma power and amount of Stage 2 sleep are both important for optimal motor memory processing. While subject intelligence correlated positively with acquisition and retest performance on both tasks, it did not correlate with over‐sleep changes in performance on either task, suggesting that intelligence may not be a powerful modulator of sleep’s effect on memory performance.

Slow wave sleep during a daytime nap is necessary for protection from subsequent interference and long-term retention

While it is now generally accepted that sleep facilitates the processing of newly acquired declarative information, questions still remain as to the type and length of sleep necessary to best benefit declarative memories. A better understanding could lend support in one direction or another as to the much-debated role of sleep, be it passive, permissive, or active, in memory processing. The present study employed a napping paradigm and compared performance on a bimodal paired-associates task of those who obtained a 10-min nap, containing only Stages 1 and 2 sleep, to those whose nap contained slow-wave sleep (SWS) and rapid eye movement (REM) sleep (60-min nap), as well as to subjects who remained awake. Measurements were obtained for baseline performance at training, after a sleep/no sleep interval for short-term retention, after a subsequent stimulus-related interference task, and again after a weeklong retention period. While all groups learned the information similarly, both nap groups performed better than the Wake group when examining short-term retention, approximately 1.5h after training (10-min p=.052, 60-min p=.002). However, performance benefits seen in the 10-min nap group proved to be temporary. Performance after a stimulus-related interference task revealed significantly better memory retention in the 60-min nap group, with interference disrupting the memory trace far less than both the Wake and 10-min nap groups (p<.001, p=.006, respectively). After a weeklong retention period, sleeps benefit to memory persisted in the 60-min nap group, with performance significantly greater than both the Wake and 10-min nap groups (p<.001, p=.004, respectively). It is our conclusion that SWS, obtained only by those in the 60-min nap group, served to actively facilitate the consolidation of learned bimodal paired-associates, supported by theories such as the Standard Theory of Consolidation as well as the Synaptic Homeostasis Hypothesis.

Relational Memory: A Daytime Nap Facilitates the Abstraction of General Concepts

It is increasingly evident that sleep strengthens memory. However, it is not clear whether sleep promotes relational memory, resultant of the integration of disparate memory traces into memory networks linked by commonalities. The present study investigates the effect of a daytime nap, immediately after learning or after a delay, on a relational memory task that requires abstraction of general concept from separately learned items. Specifically, participants learned English meanings of Chinese characters with overlapping semantic components called radicals. They were later tested on new characters sharing the same radicals and on explicitly stating the general concepts represented by the radicals. Regardless of whether the nap occurred immediately after learning or after a delay, the nap participants performed better on both tasks. The results suggest that sleep – even as brief as a nap – facilitates the reorganization of discrete memory traces into flexible relational memory networks.