Luca Matarazzo

Does sleep promote false memories

Memory is constructive in nature so that it may sometimes lead to the retrieval of distorted or illusory information. Sleep facilitates accurate declarative memory consolidation but might also promote such memory distortions. We examined the influence of sleep and lack of sleep on the cerebral correlates of accurate and false recollections using fMRI. After encoding lists of semantically related word associates, half of the participants were allowed to sleep, whereas the others were totally sleep deprived on the first postencoding night. During a subsequent retest fMRI session taking place 3 days later, participants made recognition memory judgments about the previously studied associates, critical theme words (which had not been previously presented during encoding), and new words unrelated to the studied items. Sleep, relative to sleep deprivation, enhanced accurate and false recollections. No significant difference was observed in brain responses to false or illusory recollection between sleep and sleep deprivation conditions. However, after sleep but not after sleep deprivation (exclusive masking), accurate and illusory recollections were both associated with responses in the hippocampus and retrosplenial cortex. The data suggest that sleep does not selectively enhance illusory memories but rather tends to promote systems-level consolidation in hippocampo-neocortical circuits of memories subsequently associated with both accurate and illusory recollections. We further observed that during encoding, hippocampal responses were selectively larger for items subsequently accurately retrieved than for material leading to illusory memories. The data indicate that the early organization of memory during encoding is a major factor influencing subsequent production of accurate or false memories.

Memory Reactivation during Rapid Eye Movement Sleep Promotes Its Generalization and Integration in Cortical Stores

STUDY OBJECTIVES Memory reactivation appears to be a fundamental process in memory consolidation. In this study we tested the influence of memory reactivation during rapid eye movement (REM) sleep on memory performance and brain responses at retrieval in healthy human participants. PARTICIPANTS Fifty-six healthy subjects (28 women and 28 men, age [mean ± standard deviation]: 21.6 ± 2.2 y) participated in this functional magnetic resonance imaging (fMRI) study. METHODS AND RESULTS Auditory cues were associated with pictures of faces during their encoding. These memory cues delivered during REM sleep enhanced subsequent accurate recollections but also false recognitions. These results suggest that reactivated memories interacted with semantically related representations, and induced new creative associations, which subsequently reduced the distinction between new and previously encoded exemplars. Cues had no effect if presented during stage 2 sleep, or if they were not associated with faces during encoding. Functional magnetic resonance imaging revealed that following exposure to conditioned cues during REM sleep, responses to faces during retrieval were enhanced both in a visual area and in a cortical region of multisensory (auditory-visual) convergence. CONCLUSIONS These results show that reactivating memories during REM sleep enhances cortical responses during retrieval, suggesting the integration of recent memories within cortical circuits, favoring the generalization and schematization of the information.

The Impact of Visual Perceptual Learning on Sleep and Local Slow-Wave Initiation

During non-rapid eye movement (NREM) sleep, a global decrease in synaptic strength associated with slow waves (SWs) would enhance signal-to-noise ratio of neural responses during subsequent wakefulness. To test this prediction, 32 human volunteers were trained to a coarse orientation discrimination task, in either the morning or evening. They were retested after 8 h of wakefulness or sleep, respectively. Performance was enhanced only after a night of sleep, in the absence of any change in the abundance of NREM SWs but in proportion to the number of SWs “initiated” in lateral occipital areas during posttraining NREM sleep. The sources of these waves overlapped with the lateral occipital complex, in which responses to the learned stimulus, as assessed by fMRI, were selectively increased the next morning. This response enhancement was proportional to rapid eye movement (REM) sleep duration. These results provide an example of local sleep in which local initiation of SWs during NREM sleep predicts later skill improvement and foreshadows locally enhanced neural signals the next day. In addition, REM sleep also promotes local learning-dependent activity, possibly by promoting synaptic plasticity.

Influence of acute sleep loss on the neural correlates of alerting, orientating and executive attention components.

The Attention Network Test (ANT) is deemed to assess the alerting, orientating and executive components of human attention. Capitalizing on the opportunity to investigate three facets of attention in a single task, we used functional magnetic resonance imaging (fMRI) to assess the effect of sleep deprivation (SD) on brain responses associated with the three attentional components elicited by the ANT. Twelve healthy volunteers were scanned in two conditions 1 week apart, after a normal night of sleep (rested wakefulness, RW) or after one night of total sleep deprivation. Sleep deprivation was associated with a global increase in reaction times, which did not affect specifically any of the three attention effects. Brain responses associated with the alerting effect did not differ between RW and SD. Higher‐order attention components (orientating and conflict effects) were associated with significantly larger thalamic responses during SD than during RW. These results suggest that SD influences different components of human attention non‐selectively, through mechanisms that might either affect centrencephalic structures maintaining vigilance or ubiquitously perturb neuronal function. Compensatory responses can counter these effects transiently by recruiting thalamic responses, thereby supporting thalamocortical function.

Offline processing of memories induced by perceptual visual learning during subsequent wakefulness and sleep: A behavioral study

To further characterize perceptual memory consolidation during sleep, we used a coarse orientation discrimination task in which participants had to discriminate the orientation of orthogonal gratings occluded by increasing levels of noise. In a first study (N = 11), we showed that the learning effect in this task is retinotopic (position-specific) and orientation specific. In a second experiment, we assessed the effect of nocturnal sleep, as opposed to the effect of time, on perceptual learning. A first group of participants was trained in the morning, tested in the evening and retested the next morning (morning-evening-morning, MEM, N = 11); a second group was trained in the evening, tested the next morning, and retested in the evening (evening-morning-evening; EME; N = 12). Between training and testing, EME subjects improved significantly more (after a night of sleep) than MEM subjects (after 12 waking hours). Similarly, between test and retest, performance of MEM subjects (after a full night of sleep) improved significantly more than in EME subjects (after 12 further waking hours). These results suggest a beneficial effect of sleep on coarse orientation discrimination. Further studies are needed to characterize the neural correlates of this perceptual learning and the offline consolidation of perceptual memory.

Experience-dependent induction of hypnagogic images during daytime naps: a combined behavioural and EEG study.

This study characterizes hypnagogic hallucinations reported during a polygraphically recorded 90‐min daytime nap following or preceding practice of the computer game Tetris. In the experimental group (N = 16), participants played Tetris in the morning for 2 h during three consecutive days, while in a first control group (N = 13, controlling the effect of experience) participants did not play any game, and in a second control group (N = 14, controlling the effect of anticipation) participants played Tetris after the nap. During afternoon naps, participants were repetitively awakened 15, 45, 75, 120 or 180 s after the onset of S1, and were asked to report their mental content. Reports content was scored by three judges (inter‐rater reliability 85%). In the experimental group, 48 out of 485 (10%) sleep‐onset reports were Tetris‐related. They mostly consisted of images and sounds with very little emotional content. They exactly reproduced Tetris elements or mixed them with other mnemonic components. By contrast, in the first control group, only one report out of 107 was scored as Tetris‐related (1%), and in the second control group only three reports out of 112 were scored as Tetris‐related (3%; between‐groups comparison; P = 0.006). Hypnagogic hallucinations were more consistently induced by experience than by anticipation (P = 0.039), and they were predominantly observed during the transition of wakefulness to sleep. The observed attributes of experience‐related hypnagogic hallucinations are consistent with the particular organization of regional brain activity at sleep onset, characterized by high activity in sensory cortices and in the default‐mode network.

Spontaneous neural activity during human non-rapid eye movement sleep.

Recent neuroimaging studies characterized the neural correlates of slow waves and spindles during human non-rapid eye movement (NREM) sleep. They showed that significant activity was consistently associated with slow (> 140 μV) and delta waves (75-140 μV) during NREM sleep in several cortical areas including inferior frontal, medial prefrontal, precuneus, and posterior cingulate cortices. Unexpectedly, slow waves were also associated with transient responses in the pontine tegmentum and in the cerebellum. On the other hand, spindles were associated with a transient activity in the thalami, paralimbic areas (anterior cingulate and insular cortices), and superior temporal gyri. Moreover, slow spindles (11-13 Hz) were associated with increased activity in the superior frontal gyrus. In contrast, fast spindles (13-15 Hz) recruited a set of cortical regions involved in sensorimotor processing, as well as the mesial frontal cortex and hippocampus. These findings indicate that human NREM sleep is an active state during which brain activity is temporally organized by spontaneous oscillations (spindles and slow oscillation) in a regionally specific manner. The functional significance of these NREM sleep oscillations is currently interpreted in terms of synaptic homeostasis and memory consolidation.

Neuroimaging of dreaming: state of the art and limitations.

During the last two decades, functional neuroimaging has been used to characterize the regional brain function during sleep in humans, at the macroscopic systems level. In addition, the topography of brain activity, especially during rapid eye movement sleep, was thought to be compatible with the general features of dreams. In contrast, the neural correlates of dreams remain largely unexplored. This review examines the difficulties associated with the characterization of dream correlates. ἓν οἶδα ὅτι οὐδὲν οἶδα Σωκράτης (The only thing I know is that I know nothing) Socrates.

Some facts about sleep relevant for Landau-Kleffner syndrome.

Our understanding of the neural mechanisms of non–rapid eye movement sleep (NREM) is steadily increasing. Given the intriguing activation of paroxysmal activity during NREM sleep in patients with Landau‐Kleffner syndrome (LKS), a thorough characterization of commonalities and differences between the neural correlates of LKS paroxysms and normal sleep oscillations might provide useful information on the neural underpinning of this disorder. Especially, given the suspected role of sleep in brain plasticity, this type of information is needed to assess the link between cognitive deterioration and electroencephalography (EEG) paroxysms during sleep.

Reciprocal interactions between wakefulness and sleep influence global and regional brain activity.

Reciprocal interactions between wakefulness and sleep substantially influence human brain function in both states of vigilance. On the one hand, there is evidence that regionally-specialized brain activity during wakefulness is modulated by the interaction between a local use-dependent buildup of homeostatic sleep pressure and circadian signals. On the other hand, brain activity during sleep, although mainly constrained by genuine sleep oscillations, shows wake-dependent regionally-specific modulations, which are involved in the dissipation of local homeostatic sleep pressure and memory consolidation.