Learning capacities during sleep: A preliminary study in a group of schizophrenic inpatients

The relationship between sleep and learning processes is analysed in a sample of schizophrenic patients, starting from more recent hypotheses about the function of REM sleep in learning and memory processes. This is done by means of two experiments: in the first AA. evaluate the possibility to elicit a simple motor conditional reflex acquired during daytime in different sleep stages. With the second experiment daytime learning performances are evaluated with and without a reinforcement administered during REM sleep. Results for the first experiment underline a qualitative difference between REM and nREM sleep in a reflexological perspective. In nREM sleep the conditional response is better maintained than in REM sleep. The second experiment confirms the possibility to improve daytime learning performances after an additional presentation of learning material in REM. The joint study of sleep abnormalities and learning and cognitive impairment in schizophrenic patients is finally suggested.     

Information processing during sleep onset and sleep.

This Special Section examines the extent of information processing during sleep onset and sleep itself. It is generally agreed that, stimulus input is markedly inhibited during sleep, thus preventing conscious awareness of the external environment. Overt behavioural responses are rarely made within sleep. Two neurophysiological measures are therefore often used. The electrical activity of the brain (the EEG) can be employed to distinguish waking (conscious) from sleeping (unconscious) states. It is also possible to quantify the EEG prior to and following a detection (or a failure of a detection) of a stimulus. Such measures can thus be used to predict conscious awareness. A second measure that frequently has been employed is the brain's response to an external stimulus (the evoked potential). Different components of the evoked potential can be used to trace the extent of information processing during the different states of consciousness. Some are associated with a preconscious detection while others are associated with conscious awareness. Other evoked potentials may be unique to sleep.     

Memory reactivation and consolidation during sleep

Do our memories remain static during sleep, or do they change? We argue here that memory change is not only a natural result of sleep cognition, but further, that such change constitutes a fundamental characteristic of declarative memories. In general, declarative memories change due to retrieval events at various times after initial learning and due to the formation and elaboration of associations with other memories, including memories formed after the initial learning episode. We propose that declarative memories change both during waking and during sleep, and that such change contributes to enhancing binding of the distinct representational components of some memories, and thus to a gradual process of cross-cortical consolidation. As a result of this special form of consolidation, declarative memories can become more cohesive and also more thoroughly integrated with other stored information. Further benefits of this memory reprocessing can include developing complex networks of interrelated memories, aligning memories with long-term strategies and goals, and generating insights based on novel combinations of memory fragments. A variety of research findings are consistent with the hypothesis that cross-cortical consolidation can progress during sleep, although further support is needed, and we suggest some potentially fruitful research directions. Determining how processing during sleep can facilitate memory storage will be an exciting focus of research in the coming years.The idea that memory storage is supported by events that take place in the brain while a person is sleeping is an idea that is only rarely acknowledged in the neuroscience community. At present, most memory research proceeds with no mention of any influence of sleep on memory. Nonetheless, this hypothesis is gaining empirical support. Research into connections between memory and sleep represents a burgeoning enterprise at the crossroads of traditional memory research and sleep research, an enterprise poised to provide novel insights into the human experience.This article presents some speculations about connections between memory and sleep. We entertain the notion that declarative memories are subject to modification during sleep, and that enduring storage of such memories is systematically influenced by neural events taking place during sleep. Although other types of memory may also be subject to change during sleep (see Maquet et al. 2003), we emphasize declarative memory here.This article also functions as an introduction to the set of papers selected for this special issue of Learning & Memory. These papers together outline portions of the current empirical basis for memory-sleep connections, including research in humans and in nonhuman animals. The findings are tantalizing, and yet there are undoubtedly major gaps in our knowledge about the functions of sleep and about how sleep may be related to memory storage. Future research on this topic is bound to grow in exciting and unpredictable ways. Here, we explore questions about declarative memory and sleep that may serve as a useful guide for such research.     

Consolidation of sensorimotor learning during sleep

Consolidation of nondeclarative memory is widely believed to benefit from sleep. However, evidence is mainly limited to tasks involving rote learning of the same stimulus or behavior, and recent findings have questioned the extent of sleep-dependent consolidation. We demonstrate consolidation during sleep for a multimodal sensorimotor skill that was trained and tested in different visual-spatial virtual environments. Participants performed a task requiring the production of novel motor responses in coordination with continuously changing audio-visual stimuli. Performance improved with training, decreased following waking retention, but recovered and stabilized following sleep. These results extend the domain of sleep-dependent consolidation to more complex, adaptive behaviors.     

Learning during stressful times

Stressful life events can have profound effects on our cognitive and motor abilities, from those that could be construed as adaptive to those not so. In this review, I discuss the general notion that acute stressful experience necessarily impairs our abilities to learn and remember. The effects of stress on operant conditioning, that is, learned helplessness, as well as those on classical conditioning procedures are discussed in the context of performance and adaptation. Studies indicating sex differences in learning during stressful times are discussed, as are those attributing different responses to the existence of multiple memory systems and nonlinear relationships. The intent of this review is to highlight the apparent plasticity of the stress response, how it might have evolved to affect both performance and learning processes, and the potential problems with interpreting stress effects on learning as either good or bad. An appreciation for its plasticity may provide new avenues for investigating its underlying neuronal mechanisms.     

System consolidation of memory during sleep

Over the past two decades, research has accumulated compelling evidence that sleep supports the formation of long-term memory. The standard two-stage memory model that has been originally elaborated for declarative memory assumes that new memories are transiently encoded into a temporary store (represented by the hippocampus in the declarative memory system) before they are gradually transferred into a long-term store (mainly represented by the neocortex), or are forgotten. Based on this model, we propose that sleep, as an offline mode of brain processing, serves the ‘active system consolidation’ of memory, i.e. the process in which newly encoded memory representations become redistributed to other neuron networks serving as long-term store. System consolidation takes place during slow-wave sleep (SWS) rather than rapid eye movement (REM) sleep. The concept of active system consolidation during sleep implicates that (a) memories are reactivated during sleep to be consolidated, (b) the consolidation process during sleep is selective inasmuch as it does not enhance every memory, and (c) memories, when transferred to the long-term store undergo qualitative changes. Experimental evidence for these three central implications is provided: It has been shown that reactivation of memories during SWS plays a causal role for consolidation, that sleep and specifically SWS consolidates preferentially memories with relevance for future plans, and that sleep produces qualitative changes in memory representations such that the extraction of explicit and conscious knowledge from implicitly learned materials is facilitated.     

Anticipatory attention during the sleep onset period

To examine whether anticipatory attention or expectancy is a cognitive process that is automatic or requires conscious control, we employed a paired-stimulus event-related potential (ERP) paradigm during the transition to sleep. The slow negative ERP wave observed between two successive stimuli, the Contingent Negative Variation (CNV), reflects attention and expectancy to the second stimulus. Thirteen good sleepers were instructed to respond to the second stimulus in a pair during waking sessions. In a non-response paradigm modified for sleep, participants then fell asleep while tones played. As expected, N1 decreased and P2 increased in amplitude systematically with the loss of consciousness at sleep onset; the CNV was increasingly more positive. Sleep onset latency was correlated with the amplitude of the CNV. The systematic attenuation of the CNV waveform at sleep onset and its absence in sleep indicates that anticipatory attention requires endogenous conscious control.     

ERPs studies of cognitive processing during sleep

In the last few decades, several works on cognitive processing during sleep have emerged. The study of cognitive processing with event related potentials (ERPs) during sleep is a topic of great interest, since ERPs allow the study of stimulation with passive paradigms (without conscious response or behavioural response), opening multiple research possibilities during different sleep phases. We review ERPs modulated by cognitive processes during sleep: N1, Mismatch Negativity (MMN), P2, P3, N400-like, N300-N550, among others. The review shows that there are different cognitive discriminations during sleep related to the frequency, intensity, duration, saliency, novelty, proportion of appearance, meaning, and even sentential integration of stimuli. The fascinating results of cognitive processing during sleep imply serious challenges for cognitive models. The studies of ERPs, together with techniques of neuroimaging, have demonstrated the existence of cognitive processing during sleep. A fundamental question to be considered is if these cognitive phenomena are similar to processing that occurs during wakefulness. Based on this question we discussed the existence of possible mechanisms associated with sleep, as well as the specific cognitive and neurophysiologic differences of wakefulness and sleep. Much knowledge is still required to even understand the conjunction of dramatic changes in cerebral dynamics and the occurrence of cognitive processes. We propose some insights based on ERPs research for further construction of theoretical models for integrating both cognitive processing and specific brain sleep dynamics.     

Memory consolidation during sleep: interactive effects of sleep stages and HPA regulation

Sleep is critically involved in the consolidation of previously acquired memory traces. However, nocturnal sleep is not uniform but is subject to distinct changes in electrophysiological and neuroendocrine activity. Specifically, the first half of the night is dominated by slow wave sleep (SWS), whereas rapid eye movement (REM) sleep prevails in the second half. Concomitantly, hypothalamo-pituitary-adrenal (HPA) activity as indicated by cortisol release is suppressed to a minimum during early sleep, while drastically increasing during late sleep. We have shown that the different sleep stages and the concomitant glucocorticoid release are interactively involved in the consolidation of different types of memories. SWS-rich early sleep has been demonstrated to benefit mainly the consolidation of hippocampus-dependent declarative memories (i.e. facts and episodes). In contrast, REM sleep-rich late sleep was shown to improve in particular emotional memories involving amygdalar function, as well as procedural memories (for skills) not depending on hippocampal or amygdalar function. Enhancing plasma glucocorticoid concentrations during SWS-rich early sleep counteracted hippocampus-dependent declarative memory consolidation, but did not affect hippocampus-independent procedural memory. Preventing the increase in cortisol during late REM sleep-rich sleep by administration of metyrapone impaired hippocampus-dependent declarative memory but enhanced amygdala-dependent emotional aspects of memory. The data underscore the importance of pituitary-adrenal inhibition during early SWS-rich sleep for efficient consolidation of declarative memory. The increase in cortisol release during late REM sleep-rich sleep may counteract an overshooting consolidation of emotional memories.     

Learning strategies during fear conditioning

This paper describes a model of fear learning, in which subjects have an option of behavioral responses to impending social defeat. The model generates two types of learning: social avoidance and classical conditioning, dependent upon (1) escape from or (2) social subordination to an aggressor. We hypothesized that social stress provides the impetus as well as the necessary information to stimulate dichotomous goal-oriented learning. Specialized tanks were constructed to subject rainbow trout to a conditioning paradigm where the conditioned stimulus (CS) is cessation of tank water flow (water off) and the unconditioned stimulus (US) is social aggression from a larger conspecific. Following seven daily CS/US pairings, approximately half of the test fish learned to consistently escape the aggression to a neutral chamber through a small escape hole available only during the interaction. The learning curve for escaping fish was dramatic, with an 1100% improvement in escape time over 7 days. Fish that did not escape exhibited a 400% increase in plasma cortisol and altered brain monoamine response to presentation of the CS alone. Elevated plasma cortisol levels represent classical fear conditioning in non-escaping fish, while a lack of fear conditioning and a decreased latency to escape over the training period in escapers indicates learned escape.     

Cognitive aspects of mental activity during sleep.

Upon nighttime experimental awakening of 27 subjects in four sleep conditions (sleep onset early; sleep onset late; Stage 2; and rapid eye movement, REM, sleep), 108 dream reports and their association reports were collected. Dream reports were analyzed for length (temporal units) and content categories (continuity; implausibility; presence of the dreamer [i.e., "the self"], a setting, characters). Associations were classified as episodic, abstract self-referred, and semantic memories. The two sets of results tend to show a basic homogeneity among mentation reports in the four sleep conditions considered. These findings are interpreted as supporting the hypothesis that the same cognitive mechanisms operate, at different levels of engagement, in dream generation rather than the hypothesis of multiple dream-generation systems dependent upon the physiological characteristics of the various sleep stages.     

Recovery of performance during sleep following sleep deprivation in older normal and insomniac adult males

Groups of 12 normal and insomniac male subjects aged 55 to 71 yr. were sleep deprived for 64 hr. In both groups, the sleep loss was preceded by four baseline sleep nights and followed by four recovery nights. Reaction time, immediate recall, sleepiness, and body temperature were measured at approximately 2300, 0115, 0330, 0530, and 0800 during baseline, deprivation and recovery nights. Significant performance or mood differences were not found between the normal and insomniac males on any measure or at any testing period throughout the study. Performance of both groups declined characteristically during sleep loss while subjective sleepiness increased. As in young adults, degraded performance was restored by 8 hr. of recovery sleep. However, subjective sleepiness did not return to baseline levels until early in the second recovery night. It was concluded that chronic insomnia does not result in group performance deficits similar to those seen after chronic sleep loss; and the restorative function of sleep operates as efficiently in older insomniac subjects (who apparently have reduced need to sleep) as in older normal subjects.