Offline persistence of memory-related cerebral activity during active wakefulness.
ABSTRACT: Much remains to be discovered about the fate of recent memories in the human brain. Several studies have reported the reactivation of learning-related cerebral activity during post-training sleep, suggesting that sleep plays a role in the offline processing and consolidation of memory. However, little is known about how new information is maintained and processed during post-training wakefulness before sleep, while the brain is actively engaged in other cognitive activities. We show, using functional magnetic resonance imaging, that brain activity elicited during a new learning episode modulates brain responses to an unrelated cognitive task, during the waking period following the end of training. This post-training activity evolves in learning-related cerebral structures, in which functional connections with other brain regions are gradually established or reinforced. It also correlates with behavioral performance. These processes follow a different time course for hippocampus-dependent and hippocampus-independent memories. Our experimental approach allowed the characterization of the offline evolution of the cerebral correlates of recent memories, without the confounding effect of concurrent practice of the learned material. Results indicate that the human brain has already extensively processed recent memories during the first hours of post-training wakefulness, even when simultaneously coping with unrelated cognitive demands.
Project description:It is now well established that postlearning sleep is beneficial for human memory performance. Meanwhile, human and animal studies have demonstrated that learning-related neural activity is re-expressed during posttraining nonrapid eye movement (NREM) sleep. NREM sleep processes appear to be particularly beneficial for hippocampus-dependent forms of memory. These observations suggest that learning triggers the reactivation and reorganization of memory traces during sleep, a systems-level process that in turn enhances behavioral performance. Here, we hypothesized that dreaming about a learning experience during NREM sleep would be associated with improved performance on a hippocampus-dependent spatial memory task. Subjects were trained on a virtual navigation task and then retested on the same task 5 hr after initial training. Improved performance at retest was strongly associated with task-related dream imagery during an intervening afternoon nap. Task-related thoughts during wakefulness, in contrast, did not predict improved performance. These observations suggest that sleep-dependent memory consolidation in humans is facilitated by the offline reactivation of recently formed memories, and furthermore that dream experiences reflect this memory processing. That similar effects were not observed during wakefulness suggests that these mnemonic processes are specific to the sleep state.
Project description:Numerous studies have examined sleep's influence on a range of hippocampus-dependent declarative memory tasks, from text learning to spatial navigation. In this study, we examined the impact of sleep, wake, and time-of-day influences on the processing of declarative information with strong semantic links (semantically related word pairs) and information requiring the formation of novel associations (unrelated word pairs). Participants encoded a set of related or unrelated word pairs at either 9 am or 9 pm, and were then tested after an interval of 30 min, 12 hr, or 24 hr. The time of day at which subjects were trained had no effect on training performance or initial memory of either word pair type. At 12 hr retest, memory overall was superior following a night of sleep compared to a day of wakefulness. However, this performance difference was a result of a pronounced deterioration in memory for unrelated word pairs across wake; there was no sleep-wake difference for related word pairs. At 24 hr retest, with all subjects having received both a full night of sleep and a full day of wakefulness, we found that memory was superior when sleep occurred shortly after learning rather than following a full day of wakefulness. Lastly, we present evidence that the rate of deterioration across wakefulness was significantly diminished when a night of sleep preceded the wake period compared to when no sleep preceded wake, suggesting that sleep served to stabilize the memories against the deleterious effects of subsequent wakefulness. Overall, our results demonstrate that 1) the impact of 12 hr of waking interference on memory retention is strongly determined by word-pair type, 2) sleep is most beneficial to memory 24 hr later if it occurs shortly after learning, and 3) sleep does in fact stabilize declarative memories, diminishing the negative impact of subsequent wakefulness.
Project description:With respect to behavior, the term memory "consolidation" has canonically been used to describe increased fidelity during testing to a learned behavior shaped during training. While the sleeping brain appears to certainly aid in consolidation by this definition for a variety of memories, including motor memories, growing evidence suggests that sleep allows for much more flexible use of the information encountered during prior wakefulness. Sleep has been shown to augment the extraction of gist or patterns from wake experience in human subjects, but this has been difficult to recapitulate in animal models owing to the semantic requirements in many such tasks. Here we establish a model of motor gist learning in mice in which two bouts of exclusive forward running on the rotarod significantly augments the first experience of exclusive backward running. This augmentation does not occur if sleep is disrupted following the forward running template behavior or if a period of natural wakefulness follows one of the two bouts of exclusive forward running. This suggests that sleep is required for the extraction of the motor gist of forward running to apply to backward running.
Project description:It is known that sleep reshapes the neural representations that subtend the memories acquired while navigating in a virtual environment. However, navigation is not process-pure, as manifold learning components contribute to performance, notably the spatial and contextual memory constituents. In this context, it remains unclear whether post-training sleep globally promotes consolidation of all of the memory components embedded in virtual navigation, or rather favors the development of specific representations. Here, we investigated the effect of post-training sleep on the neural substrates of the consolidation of spatial and contextual memories acquired while navigating in a complex 3D, naturalistic virtual town. Using fMRI, we mapped regional cerebral activity during various tasks designed to tap either the spatial or the contextual memory component, or both, 72 h after encoding with or without sleep deprivation during the first post-training night. Behavioral performance was not dependent upon post-training sleep deprivation, neither in a natural setting that engages both spatial and contextual memory processes nor when looking more specifically at each of these memory representations. At the neuronal level however, analyses that focused on contextual memory revealed distinct correlations between performance and neuronal activity in frontal areas associated with recollection processes after post-training sleep, and in the parahippocampal gyrus associated with familiarity processes in sleep-deprived participants. Likewise, efficient spatial memory was associated with posterior cortical activity after sleep whereas it correlated with parahippocampal/medial temporal activity after sleep deprivation. Finally, variations in place-finding efficiency in a natural setting encompassing spatial and contextual elements were associated with caudate activity after post-training sleep, suggesting the automation of navigation. These data indicate that post-training sleep modulates the neural substrates of the consolidation of both the spatial and contextual memories acquired during virtual navigation.
Project description:The application of transcranial slow oscillation stimulation (tSOS; 0.75 Hz) was previously shown to enhance widespread endogenous EEG slow oscillatory activity when applied during a sleep period characterized by emerging endogenous slow oscillatory activity. Processes of memory consolidation typically occurring during this state of sleep were also enhanced. Here, we show that the same tSOS applied in the waking brain also induced an increase in endogenous EEG slow oscillations (0.4-1.2 Hz), although in a topographically restricted fashion. Applied during wakefulness tSOS, additionally, resulted in a marked and widespread increase in EEG theta (4-8 Hz) activity. During wake, tSOS did not enhance consolidation of memories when applied after learning, but improved encoding of hippocampus-dependent memories when applied during learning. We conclude that the EEG frequency and related memory processes induced by tSOS critically depend on brain state. In response to tSOS during wakefulness the brain transposes stimulation by responding preferentially with theta oscillations and facilitated encoding.
Project description:The ability to consolidate procedural memories declines with increasing age. Prior knowledge enhances learning and memory consolidation of novel but related information in various domains. Here, we present evidence that prior motor experience-in our case piano skills-increases procedural learning and has a protective effect against age-related decline for the consolidation of novel but related manual movements. In our main experiment, we tested 128 participants with a sequential finger-tapping motor task during two sessions 24 hours apart. We observed enhanced online learning speed and offline memory consolidation for piano players. Enhanced memory consolidation was driven by a strong effect in older participants, whereas younger participants did not benefit significantly from prior piano experience. In a follow up independent control experiment, this compensatory effect of piano experience was not visible after a brief offline period of 30 minutes, hence requiring an extended consolidation window potentially involving sleep. Through a further control experiment, we rejected the possibility that the decreased effect in younger participants was caused by training saturation. We discuss our results in the context of the neurobiological schema approach and suggest that prior experience has the potential to rescue memory consolidation from age-related cognitive decline.
Project description:People make inferences about the trustworthiness of others based on their observed gaze behavior. Faces that consistently look toward a target location are rated as more trustworthy than those that look away from the target. Representations of trust are important for future interactions; yet little is known about how they are consolidated in long-term memory. Sleep facilitates memory consolidation for incidentally learned information and may therefore support the retention of trust representations. We investigated the consolidation of trust inferences across periods of sleep or wakefulness. In addition, we employed a memory cueing procedure (targeted memory reactivation [TMR]) in a bid to strengthen certain trust memories over others. We observed no difference in the retention of trust inferences following delays of sleep or wakefulness, and there was no effect of TMR in either condition. Interestingly, trust inferences remained stable 1 week after learning, irrespective of the initial postlearning delay. A second experiment showed that this implicit learning occurs despite participants' being unable to explicitly recall the gaze behavior of specific faces immediately after encoding. Together, these results suggest that gist-like, social inferences are formed at the time of learning without retaining the original episodic memory and thus do not benefit from offline consolidation through replay. We discuss our findings in the context of a novel framework whereby trust judgments reflect an efficient, powerful, and adaptable storage device for social information. (PsycInfo Database Record (c) 2020 APA, all rights reserved).
Project description:Continual learning remains an unsolved problem in artificial neural networks. The brain has evolved mechanisms to prevent catastrophic forgetting of old knowledge during new training. Building upon data suggesting the importance of sleep in learning and memory, we tested a hypothesis that sleep protects old memories from being forgotten after new learning. In the thalamocortical model, training a new memory interfered with previously learned old memories leading to degradation and forgetting of the old memory traces. Simulating sleep after new learning reversed the damage and enhanced old and new memories. We found that when a new memory competed for previously allocated neuronal/synaptic resources, sleep replay changed the synaptic footprint of the old memory to allow overlapping neuronal populations to store multiple memories. Our study predicts that memory storage is dynamic, and sleep enables continual learning by combining consolidation of new memory traces with reconsolidation of old memory traces to minimize interference.
Project description:Across a broad spectrum of memory tasks, retention is superior following a night of sleep compared to a day of wake. However, this result alone does not clarify whether sleep merely slows the forgetting that would otherwise occur as a result of information processing during wakefulness, or whether sleep actually consolidates memories, protecting them from subsequent retroactive interference. Two influential studies suggested that sleep protects memories against the subsequent retroactive interference that occurs when participants learn new yet overlapping information (interference learning). In these studies, interference learning was much less detrimental to memory following a night of sleep compared to a day of wakefulness, an indication that sleep supports this important aspect of memory consolidation. In the current replication study, we repeated the protocol of and, additionally, we examined the impact of intrinsic motivation on performance in sleep and wake participants. We were unable to replicate the finding that sleep protects memories against retroactive interference, with the detrimental effects of interference learning being essentially the same in wake and sleep participants. We also found that while intrinsic motivation benefitted task acquisition it was not a modulator of sleep-wake differences in memory processing. Although we cannot accept the null hypothesis that sleep has no role to play in reducing the negative impact of interference, the findings draw into question prior evidence for sleep's role in protecting memories against interference. Moreover, the current study highlights the importance of replicating key findings in the study of sleep's impact on memory processing before drawing strong conclusions that set the direction of future research.
Project description:Increasing evidence demonstrates that motor-skill memories improve across a night of sleep, and that non-rapid eye movement (NREM) sleep commonly plays a role in orchestrating these consolidation enhancements. Here we show the benefit of a daytime nap on motor memory consolidation and its relationship not simply with global sleep-stage measures, but unique characteristics of sleep spindles at regionally specific locations; mapping to the corresponding memory representation.Two groups of subjects trained on a motor-skill task using their left hand - a paradigm known to result in overnight plastic changes in the contralateral, right motor cortex. Both groups trained in the morning and were tested 8 hr later, with one group obtaining a 60-90 minute intervening midday nap, while the other group remained awake. At testing, subjects that did not nap showed no significant performance improvement, yet those that did nap expressed a highly significant consolidation enhancement. Within the nap group, the amount of offline improvement showed a significant correlation with the global measure of stage-2 NREM sleep. However, topographical sleep spindle analysis revealed more precise correlations. Specifically, when spindle activity at the central electrode of the non-learning hemisphere (left) was subtracted from that in the learning hemisphere (right), representing the homeostatic difference following learning, strong positive relationships with offline memory improvement emerged-correlations that were not evident for either hemisphere alone.These results demonstrate that motor memories are dynamically facilitated across daytime naps, enhancements that are uniquely associated with electrophysiological events expressed at local, anatomically discrete locations of the brain.