Transcranial electrical stimulation during wakeful rest can support early memory consolidation in arithmetic learning.

IntroductionSlow, oscillatory, transcranial electrical stimulation (so-tES) applies a current over the scalp that oscillates in intensity at a frequency associated with slow wave sleep (SWS; 0.75Hz). When applied during SWS, so-tES can enhance SWS EEG power compared to sham stimulation, as well as overnight declarative memory consolidation. When applied during wake, so-tES can enhance local EEG power in the slow wave frequency range (0.5–4.5Hz) compared to sham. Therefore, this study will investigate whether so-tES can enhance the early consolidation of new learning compared to sham, when applied during wake. A preliminary analysis of data will be presented.MethodsHealthy, young, right-handed adults (18–35 years) practiced a motor sequence learning task for 30 minutes, before receiving 15 minutes of active or sham so-tES (0.75Hz) during quiet wakefulness. Task performance was assessed by recording the total number of correct sequences performed in 30 seconds before practice, after practice, and after stimulation. Performance improvements will be compared between stimulation conditions. Non-invasive, electrophysiological corticospinal excitability measurements (i.e., motor-evoked potentials) were also recorded at six timepoints throughout each session, to investigate whether active so-tES can modulate corticospinal excitability differently to sham.Progress to dateData collection is ongoing, and completion is expected by late 2021.Intended outcome and impactWe expect so-tES to enhance early skill consolidation during wake, and that enhanced consolidation will be associated with less variable measurements of corticospinal excitability, when compared with sham stimulation.

Introduction Past research has demonstrated that sleep benefits the consolidation of memories. However, more recent studies have suggested that quiet rest could have similar benefits for memory. Here, we examined the effect of a brief period of sleep, quiet rest, or active wakefulness on declarative and procedural memory. We hypothesized that sleep and quiet rest would equally benefit memory, compared to a period of active wakefulness. Methods After completing a declarative (Icelandic-English word pairs) and procedural memory task (the Motor Sequence Task (MST)), participants began a 30-min retention period with PSG monitoring, in which they either slept (n=24), quietly rested with their eyes closed (n=22), or completed a distractor task (n=28). Following the retention period, participants were tested on the same memory tasks they completed earlier. Results Percent improvement on the MST from the end of training to the end of the test session differed by condition, F(2, 73)=4.21, p=.019. Sleep and quiet rest led to nearly identical improvement (p=.95), with improvement in both of these conditions being significantly greater than in active wake (sleep vs. active wake: p=.01; quiet rest vs. active wake: p=.02). Similarly, retention of the Icelandic-English word pairs differed by condition (F(2, 73)=5.68, p=.005), with sleep and quiet rest demonstrating nearly identical memory change over time (p=.81), and retention in both of these conditions being significantly higher than in active wake (sleep vs. active wake: p=.007; quiet rest vs. active wake: p=.004). Conclusion These data suggest that sleep and quiet rest can exert an equivalent effect on memory consolidation for both declarative and procedural memory, at least across very brief retention durations. Therefore, neurobiology specific to sleep might not be necessary to induce offline improvement in memory across short intervals. Support This research was supported by National Institutes of Health Award R15MH107891.

Sleep following learning facilitates the consolidation of memories. This effect has often been attributed to sleep-specific factors, such as the presence of sleep spindles or slow waves in the electroencephalogram (EEG). However, recent studies suggest that simply resting quietly while awake could confer a similar memory benefit. In the current study, we examined the effects of sleep, quiet rest, and active wakefulness on the consolidation of declarative and procedural memory. We hypothesized that sleep and eyes-closed quiet rest would both benefit memory compared with a period of active wakefulness. After completing a declarative and a procedural memory task, participants began a 30-min retention period with PSG (polysomnographic) monitoring, in which they either slept (n = 24), quietly rested with their eyes closed (n = 22), or completed a distractor task (n = 29). Following the retention period, participants were again tested on their memory for the two learning tasks. As hypothesized, sleep and quiet rest both led to better performance on the declarative and procedural memory tasks than did the distractor task. Moreover, the performance advantages conferred by rest were indistinguishable from those of sleep. These data suggest that neurobiology specific to sleep might not be necessary to induce the consolidation of memory, at least across very short retention intervals. Instead, offline memory consolidation may function opportunistically, occurring during either sleep or stimulus-free rest, provided a favorable neurobiological milieu and sufficient reduction of new encoding.

Memory Consolidation during Waking Rest

Individuals spend roughly two-thirds of their day awake, with about half of that time in an offline state. This period may appear unproductive, potentially leading to perceived inefficiency. However, this period appears to be an essential component of our daily lives. Studies have increasingly found that quiet and wakeful rest after learning facilitates the consolidation of newly acquired memories, and enhances memory performance. Few studies quantitatively assessed the overall effect size of wakeful rest on memory consolidation, or examined the potential moderating factors. Therefore, we conducted this meta-analysis, compiled from 37 studies, including a total of 63 experiments that contributed 82 comparisons to this meta-analysis. We used a multilevel random-effects model to reveal a significant effect of wakeful rest on memory consolidation (Hedges's g = 0.448, 95% CI [0.339, 0.557], Z = 8.044, p < .001), and this effect persists even after 7days (Hedges's g = 0.270, 95% CI [0.024, 0.516], Z = 2.153, p = .031). The effect of wakeful rest was influenced by age, with older adults deriving greater benefits compared with younger adults. Across different outcome measurements, the effect was better reflected by recall than by recognition. Additionally, the duration of wakeful rest, whether the eyes are open or closed, the luminance level, and the body posture do not seem to influence the wakeful rest effect. This meta-analysis offers a deep understanding of the effects of wakeful rest on memory consolidation and provides guidance for the experimental designs of future research in this area.

IntroductionThere is ample evidence that overnight sleep and daytime naps benefit memory retention, compared to comparable amounts of active wakefulness. Yet recent evidence also suggests that a period of post-training rest (eg, quiet wakefulness with eyes closed) provides a similar memory benefit compared to wake. However, the relative benefits of sleep vs quiet waking rest on memory remain poorly understood. Here, we assessed the extent to which sleep provides a unique memory benefit, above and beyond that conferred by quiet waking rest.MethodsIn a sample of healthy undergraduate students (N=83), we tested the effect of 30 mins of post-learning sleep, rest, or active wake on concept learning (dot pattern classification) and declarative memory (word pair associates) across a 4-hr daytime training-retest interval.Results and ConclusionsContrary to our hypotheses, we found no differences in performance between the three conditions for either task. The findings are interpreted with reference to methodological considerations including the length of the experimental interval, the nature of the tasks used, and challenges inherent in creating experimental conditions that can be executed by participants.

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Accumulating evidence suggests that wakeful rest (a period of minimal cognitive stimulation) enhances memory in clinical populations with memory impairment. However, no study has previously examined the efficacy of this technique in stroke survivors, despite the high prevalence of post-stroke memory difficulties. We aimed to investigate whether wakeful rest enhances verbal memory in stroke survivors and healthy controls. Twenty-four stroke survivors and 24 healthy controls were presented with two short stories; one story was followed by a 10-minute period of wakeful rest and the other was followed by a 10-minute visual interference task. A mixed factorial analysis of variance (ANOVA) with pairwise comparisons was used to compare participants' story retention at two time points. After 15-30 minutes, stroke survivors (p = .002, d = .73), and healthy controls (p = .001, d = .76) retained more information from the story followed by wakeful rest, compared with the story followed by an interference task. While wakeful rest remained the superior condition in healthy controls after 7 days (p = .01, d = .58), the beneficial effect was not maintained in stroke survivors (p = .35, d = .19). Wakeful rest is a promising technique, which significantly enhanced verbal memory after 15-30 minutes in both groups; however, no significant benefit of wakeful rest was observed after 7 days in stroke survivors. Preliminary findings suggest that wakeful rest enhances early memory consolidation processes by protecting against the effects of interference after learning in stroke survivors.

Memory formation and storage rely on multiple interconnected brain areas, the contribution of which varies during memory consolidation. The medial prefrontal cortex, in particular the prelimbic cortex (PL), was traditionally found to be involved in remote memory storage, but recent evidence points toward its implication in early consolidation as well. Nevertheless, the inputs to the PL governing these dynamics remain unknown. Here, we first performed a brain-wide, rabies-based retrograde tracing screen of PL engram cells activated during contextual fear memory formation in male mice to identify relevant PL input regions. Next, we assessed the specific activity pattern of these inputs across different phases of memory consolidation, from fear memory encoding to recent and remote memory recall. Using projection-specific chemogenetic inhibition, we then tested their functional role in memory consolidation, which revealed a hitherto unknown contribution of claustrum to PL inputs at encoding, and of insular cortex to PL inputs at recent memory recall. Both of these inputs further impacted how PL engram cells were reactivated at memory recall, testifying to their relevance for establishing a memory trace in the PL. Collectively, these data identify a spatiotemporal shift in PL inputs important for early memory consolidation, and thereby help to refine the working model of memory formation.

Memory formation and storage rely on multiple interconnected brain areas, the contribution of which varies during memory consolidation. The medial prefrontal cortex, in particular the prelimbic cortex (PL), was traditionally found to be involved in remote memory storage, but recent evidence points toward its implication in early consolidation as well. Nevertheless, the inputs to the PL governing these dynamics remain unknown. Here, we first performed a brain-wide, rabies-based retrograde tracing screen of PL engram cells activated during contextual fear memory formation in male mice to identify relevant PL input regions. Next, we assessed the specific activity pattern of these inputs across different phases of memory consolidation, from fear memory encoding to recent and remote memory recall. Using projection-specific chemogenetic inhibition, we then tested their functional role in memory consolidation, which revealed a hitherto unknown contribution of claustrum to PL inputs at encoding, and of insular cortex to PL inputs at recent memory recall. Both of these inputs further impacted how PL engram cells were reactivated at memory recall, testifying to their relevance for establishing a memory trace in the PL. Collectively, these data identify a spatiotemporal shift in PL inputs important for early memory consolidation, and thereby help to refine the working model of memory formation.

We studied the participation of the brain dopaminergic system in cognitive processes in rats on the model of spatial learning in the Morris water maze. Administration of the dopamine D1/5-receptor agonist dihydrexidine hydrochloride during repeated training in the Morris water maze resulted in improvement of early memory consolidation by the platform search time index selectively in animals with low abilities to perform the task at this stage of training, but not in individuals with high abilities to early memory consolidation. The agonist was also ineffective in rats with low memory consolidation abilities at all stages of memory formation. In the retrieval phase after repeated training, the agonist improved the retrieval of the skill in rats with low abilities to perform the task. The results illustrate the involvement of the brain dopaminergic system in rats not only in the processes of early spatial memory consolidation, but also in the retrieval of the memory trace after learning.

SummaryElectrophysiological studies in humans and animals suggest that noninvasive neurostimulation methods such as transcranial direct current stimulation (tDCS) can elicit long-lasting [1], polarity-dependent [2] changes in neocortical excitability. Application of tDCS can have significant and selective behavioral consequences that are associated with the cortical location of the stimulation electrodes and the task engaged during stimulation [3–8]. However, the mechanism by which tDCS affects human behavior is unclear. Recently, functional magnetic resonance imaging (fMRI) has been used to determine the spatial topography of tDCS effects [9–13], but no behavioral data were collected during stimulation. The present study is unique in this regard, in that both neural and behavioral responses were recorded using a novel combination of left frontal anodal tDCS during an overt picture-naming fMRI study. We found that tDCS had significant behavioral and regionally specific neural facilitation effects. Furthermore, faster naming responses correlated with decreased blood oxygen level-dependent (BOLD) signal in Broca's area. Our data support the importance of Broca's area within the normal naming network and as such indicate that Broca's area may be a suitable candidate site for tDCS in neurorehabilitation of anomic patients, whose brain damage spares this region.

Memory consolidation is the process in which memory traces are strengthened over time for later retrieval. Although some theories hold that consolidation can only occur during sleep, accumulating evidence suggests that brief periods of wakeful rest may also facilitate consolidation. Interestingly, however, Varma and colleagues reported that a demanding 2-back task following encoding produced a similar performance to a wakeful reset condition. We tested whether participants’ recall would be best following a wakeful rest condition as compared to other distractor conditions, consistent with the extant wakeful rest literature, or whether we would replicate the finding by Varma and colleagues such that participants’ memory benefitted from both a rest and a 2-back task following encoding. Across two experiments, we used similar (Experiment 1) and the same (Experiment 2) encoding material as used the one by Varma and colleagues, employed a wakeful rest condition adapted for online testing, and compared participants’ recall across post-encoding conditions. In the first experiment, we used a between-subjects design and compared participants’ cued recall performance following a period of wakeful rest, a 2-back task, or a rest + sounds condition. The second experiment more closely replicated the experimental design used by Varma and colleagues using a within-subjects manipulation. Ultimately, our findings more consistently aligned with the canonical wakeful rest finding, such that recall was better following the rest condition than all other post-encoding conditions. These results support the notion that wakeful rest may allow for consolidation by protecting recently encoded information from interference, thereby improving memory performance.

Studies of waking rest, whereby passive rest is compared with an active task, have shown a benefit for declarative memory during short waking rest periods, which has been argued to result from the active task disrupting slow oscillations that occur during rest. Arshamian et al. (2018) found that nasal breathing while resting for an hour led to an advantage for olfactory memory consolidation compared with oral breathing, which has also been argued to result from the disruption of slow oscillations during oral breathing. In the present pre-registered research, we looked to see whether this oral breathing disruption extended to impair declarative memory consolidation, and if it is modulated by the presence of an active task. We used a 2 × 2 within-participants counterbalanced design of two sessions separated by a week where participants breathed either orally (induced by a nose clip) or nasally (induced through tape over the mouth). Each session involved learning two sets of pseudowords followed by either waking rest or an active task (N-back) for 15 min during the breathing manipulation. Memory performance was assessed by a recognition task. Our results show that the nasal advantage did not generalise to pseudowords, nor were we able to replicate the waking rest advantage or show an interaction between these factors. This study contributes to a growing body of evidence that challenges the consistency of the waking rest advantage and highlights the need for further exploration of the influence of breathing pathway on memory processes.

So far, studies that investigated interference effects of post-learning processes on episodic memory consolidation in humans have used tasks involving only complex and meaningful information. Such tasks require reallocation of general or encoding-specific resources away from consolidation-relevant activities. The possibility that interference can be elicited using a task that heavily taxes our limited brain resources, but has low semantic and hippocampal related long-term memory processing demands, has never been tested. We address this question by investigating whether consolidation could persist in parallel with an active, encoding-irrelevant, minimally semantic task, regardless of its high resource demands for cognitive processing. We distinguish the impact of such a task on consolidation based on whether it engages resources that are: (1) general/executive, or (2) specific/overlapping with the encoding modality. Our experiments compared subsequent memory performance across two post-encoding consolidation periods: quiet wakeful rest and a cognitively demanding n-Back task. Across six different experiments (total N = 176), we carefully manipulated the design of the n-Back task to target general or specific resources engaged in the ongoing consolidation process. In contrast to previous studies that employed interference tasks involving conceptual stimuli and complex processing demands, we did not find any differences between n-Back and rest conditions on memory performance at delayed test, using both recall and recognition tests. Our results indicate that: (1) quiet, wakeful rest is not a necessary prerequisite for episodic memory consolidation; and (2) post-encoding cognitive engagement does not interfere with memory consolidation when task-performance has minimal semantic and hippocampally-based episodic memory processing demands. We discuss our findings with reference to resource and reactivation-led interference theories.