Carlyle Smith

Experience-dependent changes in cerebral activation during human Rem sleep

The function of rapid-eye-movement (REM) sleep is still unknown. One prevailing hypothesis suggests that REM sleep is important in processing memory traces. Here, using positron emission tomography (PET) and regional cerebral blood flow measurements, we show that waking experience influences regional brain activity during subsequent sleep. Several brain areas activated during the execution of a serial reaction time task during wakefulness were significantly more active during REM sleep in subjects previously trained on the task than in non-trained subjects. These results support the hypothesis that memory traces are processed during REM sleep in humans.

Sleep states and memory processes.

Evidence for the involvement of rapid eye movement (REM) sleep or paradoxical sleep (PS) with memory processing continues to accumulate. In animals, there is continuing evidence of relatively small, vulnerable paradoxical sleep windows (PSWs) following successful acquisition. These PSWs, which manifest as increases in PS over normal levels, appear to exhibit shorter latencies to onset when the amount of material presented during acquisition is increased. Prevention of the PSW results in memory deficits. In humans, there is now evidence that different types of tasks are differentially sensitive to rapid eye movement sleep deprivation (REMD). Memory for declarative or explicit types of tasks appear not to be affected by REM sleep loss, while memory for cognitive procedural or implicit types of material are impaired by REMD. Using post training auditory stimulation during REM sleep, memory enhancement of the procedural material is also possible. The memory for a fine motor task appears to be sensitive to post training stage 2 sleep loss. The important neural structures are generally not yet identifiable, although the hippocampus would appear to be important for place learning in the Morris water maze.

The function of the sleep spindle: a physiological index of intelligence and a mechanism for sleep-dependent memory consolidation.

Until recently, the electrophysiological mechanisms involved in strengthening new memories into a more permanent form during sleep have been largely unknown. The sleep spindle is an event in the electroencephalogram (EEG) characterizing Stage 2 sleep. Sleep spindles may reflect, at the electrophysiological level, an ideal mechanism for inducing long-term synaptic changes in the neocortex. Recent evidence suggests the spindle is highly correlated with tests of intellectual ability (e.g.; IQ tests) and may serve as a physiological index of intelligence. Further, spindles increase in number and duration in sleep following new learning and are correlated with performance improvements. Spindle density and sigma (14-16Hz) spectral power have been found to be positively correlated with performance following a daytime nap, and animal studies suggest the spindle is involved in a hippocampal-neocortical dialogue necessary for memory consolidation. The findings reviewed here collectively provide a compelling body of evidence that the function of the sleep spindle is related to intellectual ability and memory consolidation.

Learning-dependent changes in sleep spindles and Stage 2 sleep

It has become increasingly clear that sleep is necessary for efficient memory consolidation. Recently, it has been found that Stage 2 sleep disruption impairs procedural memory performance, and that memory performance is correlated with the duration of Stage 2 sleep; but the mechanisms involved in synaptic plasticity for procedural memory during sleep have not been identified. The present study examined the learning‐dependent changes in sleep, including Stage 2 sleep spindles. Following an intense period of simple motor procedural learning, the duration of Stage 2 sleep and spindle density increased. There were no changes observed in the duration of any other stage of sleep or in the density of rapid eye movements. These findings support the hypothesis that sleep spindles are involved in the off‐line reprocessing of simple motor procedural memory during Stage 2 sleep.

Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems

Sleep spindles and rapid eye movements have been found to increase following an intense period of learning on a combination of procedural memory tasks. It is not clear whether these changes are task specific, or the result of learning in general. The current study investigated changes in spindles, rapid eye movements, K-complexes and EEG spectral power following learning in good sleepers randomly assigned to one of four learning conditions: Pursuit Rotor (n=9), Mirror Tracing (n=9), Paired Associates (n=9), and non-learning controls (n=9). Following Pursuit Rotor learning, there was an increase in the duration of Stage 2 sleep, spindle density (number of spindles/min), average spindle duration, and an increase in low frequency sigma power (12-14Hz) at occipital regions during SWS and at frontal regions during Stage 2 sleep in the second half of the night. These findings are consistent with previous findings that Pursuit Rotor learning is consolidated during Stage 2 sleep, and provide additional data to suggest that spindles across all non-REM stages may be a mechanism for brain plasticity. Following Paired Associates learning, theta power increased significantly at central regions during REM sleep. This study provides the first evidence that REM sleep theta activity is involved in declarative memory consolidation. Together, these findings support the hypothesis that brain plasticity during sleep does not involve a unitary process; that is, different types of learning have unique sleep-related memory consolidation mechanisms that act in dissociable brain regions at different times throughout the night.

Impaired motor memory for a pursuit rotor task following Stage 2 sleep loss in college students.

SUMMARY  It has recently been reported that selective REM sleep deprivation (REMD) in college students results in memory impairment of the application of a set of rules in a logic task, but not recall of a paired associate task. The present experiments were designed to examine the effects of Total Sleep Deprivation (TSD) and (REMD) following acquisition of a pure motor task, the pursuit rotor. In Experiment 1, subjects (N= 90) were exposed to TSD for one of several nights following training. Results showed that TSD on the same night as training resulted in poorer performance on retest one week later. In Experiment 2, subjects (N= 42) were exposed to various kinds of sleep deprivation on the night of task acquisition. One group was subjected to REMD. Other groups included a non‐REM awakening control group (NREMA), a TSD group, a normally rested Control group and a group allowed the first 4h of sleep in the night before being subjected to TSD (LH‐TSD) for the rest of the night. Results showed the REMD and Control groups to have excellent memory for this task while the TSD and LH ‐ TSD subjects had significantly poorer memory for the task. The NREMA group showed a slight, but not significant deficit. It was concluded that Stage 2 sleep, rather than REM sleep was the important stage of sleep for efficient memory processing of the pursuit rotor task.

Sleep states, memory processes and synaptic plasticity

There is now a substantial body of data to suggest a relationship between sleep states, particularly paradoxical sleep (PS) or rapid eye movement (REM) sleep, and learning. In animal studies, PS increases have been observed following acquisition in formal tasks and following exposure to enriched environments (EE). Further, PS deprivation at certain post-training times is known to impair memory for recently acquired tasks. PS deprivation following EE exposure has been reported to impair the neural changes normally observed. It is argued that the prolonged PS increases observed following either formal training or EE exposure reflect the same kinds of neural change. It is proposed that accelerated neural plasticity takes place during elevated post-training PS and is especially vulnerable to disruption at specific post-training time periods called PS windows. Further, it is proposed that similar processes take place in the post-training sleep of humans.

Evidence for a paradoxical sleep window for place learning in the Morris water maze.

Sprague-Dawley rats were given 4 consecutive days of training in the hidden platform version of the Morris water maze. They were then given paradoxical sleep deprivation (PSD) for 12 h either immediately after each training session or after a 12-h delay. The former group showed impaired learning on the second day of training compared to the 12-h-delayed PSD group or a nondeprived control group. In a second experiment, three groups of rats were trained as before and then given PSD for a 4-h interval beginning either immediately after, 4 h after, or 8 h after the end of each training session. Only rats exposed to PSD during the period beginning 4 h after the end of training each day showed an acquisition deficit. In a third experiment, rats were trained in a visible platform version of the water maze and exposed to PSD for a 12-h period either beginning immediately after the last training trial each day or after a 12-h rest delay. Neither of these groups was impaired on the task compared to a non-PSD control group. These results suggest that there is a PS window for place, but not cue, learning in the Morris water maze.

Rates of cerebral protein synthesis are linked to slow wave sleep in the rat

Using L-[1-14C]leucine autoradiography, rates of cerebral and local cerebral protein synthesis were studied during wakefulness, slow wave sleep (SWS) and REM sleep in the rat. In the cerebrum as a whole, the rate at which labelled leucine was incorporated into tissues was positively correlated with the occurrence of slow wave sleep. We failed to observe a significant correlation of protein synthesis rate with either wakefulness or REM sleep. As in the cerebrum as a whole, most discrete brain regions showed moderate positive correlations between the occurrence of SWS and rates of protein synthesis. There were no brain regions in which rates of protein synthesis showed striking correlations with sleep-wake states. Thus, the occurrence of SWS is associated with higher rates of protein synthesis throughout the brain. These data suggest that SWS sleep favors the restoration of cerebral proteins.

Brief Paradoxical Sleep Deprivation Impairs Reference, but Not Working, Memory in the Radial Arm Maze Task

Selective deprivation of paradoxical sleep after learning results in memory deficits in a variety of tasks. The present experiment was designed to examine the effects of paradoxical sleep deprivation (PSD) upon spatial working and reference memory. Adult male Sprague-Dawley rats were trained for 10 days in an eight-arm radial maze. Food rewards were available in four of the arms, while the other four arms were never baited. After each daily training session, different groups of rats were given 4 h of PSD, beginning either immediately, 4 h, or 8 h after the training experience. An additional group received PSD during the period 13-24 h following daily training. The group that received PSD for 4 h immediately following daily training showed significant impairment compared to the other groups, but the deficit was limited to the reference component of the task. This result suggests that PSD causes deficits only in long-term forms of spatial memory.