Cueing motor memory reactivation during NREM sleep engenders learning-related changes in precuneus and sensorimotor structures

Rakowska, Martyna; Bagrowska, Paulina; Lazari, Alberto; Navarrete, Miguel; Abdellahi, Mahmoud E. A.; Johansen‐Berg, Heidi; Lewis, Penelope A.

doi:10.1101/2022.01.27.477838

Cited by 3 publications

(20 citation statements)

References 85 publications

(109 reference statements)

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“…MD has recently been shown to decrease in precuneus in response to a series of repeated learning-retrieval epochs during wake 30 , which could be regarded of as a proxy of memory reactivation during sleep 33 . We thus hypothesised that TMR during sleep would also lead to rapid MD-driven plasticity within precuneus, thereby supporting the functional activation of this structure in association with TMR that we observed in our previous work 24 . However, we expected the motor-related regions to undergo long-term microstructural changes, thereby reflecting their slowly evolving reorganisation 34-38 , as well as long-term functional engagement and volumetric increase in response to TMR 24 .…”

Section: Introductionsupporting

confidence: 86%

“…We thus hypothesised that TMR during sleep would also lead to rapid MD-driven plasticity within precuneus, thereby supporting the functional activation of this structure in association with TMR that we observed in our previous work 24 . However, we expected the motor-related regions to undergo long-term microstructural changes, thereby reflecting their slowly evolving reorganisation 34-38 , as well as long-term functional engagement and volumetric increase in response to TMR 24 . In the current study, we also used Restricted Water Fraction (Fr), as modelled by the CHARMED framework 32 .…”

Section: Introductionsupporting

confidence: 86%

“…In recent years, TMR has become a valuable tool to study the mechanisms of sleep-dependent memory processes. It has allowed us to establish a causal link between memory reactivation and consolidation 20,21 , and to identify brain regions that are functionally involved in such relationship 13,18,22-24 . Our prior studies further demonstrated that the behavioural effects of TMR develop over time and can last up to three weeks 19,24 .…”

Section: Introductionmentioning

confidence: 99%

“…It has allowed us to establish a causal link between memory reactivation and consolidation 20,21 , and to identify brain regions that are functionally involved in such relationship 13,18,22-24 . Our prior studies further demonstrated that the behavioural effects of TMR develop over time and can last up to three weeks 19,24 . However, the physical brain changes driving the long-term functional and behavioural benefits of TMR remain poorly understood.…”

Section: Introductionmentioning

confidence: 99%

“…However, the physical brain changes driving the long-term functional and behavioural benefits of TMR remain poorly understood. We have recently shown that TMR can impact on grey matter volume within the task-related regions, thus shaping their functional response and the behavioural benefit of cueing in the long run 24 . Yet, it is still unclear whether repeated reactivation of a memory trace can also modify tissue microstructure and what the time scale of such changes might be.…”

Section: Introductionmentioning

confidence: 99%

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Distributed and gradual microstructure changes track the emergence of behavioural benefit from memory reactivation

Rakowska¹,

Lazari

Cercignani³

et al. 2022

Preprint

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Memory traces develop gradually and link to neural plasticity. Memory reactivation during sleep is crucial for consolidation, but its precise impact on plasticity and contribution to long-term memory storage remains unclear. We used multimodal diffusion-weighted imaging to track the location and timescale of microstructural changes following Targeted Memory Reactivation (TMR) of a motor task. This showed continuous microstructure plasticity in precuneus across 10 days post-TMR, paralleling the gradual development of behavioural benefit. Both early (0 - 24 h post-TMR) and late (24 h - 10 days post-TMR) microstructural changes in striatum and sensorimotor cortex were associated with the emergence of behavioural effects of TMR at day 20. Furthermore, the baseline microstructural architecture of sensorimotor cortex predicted TMR susceptibility. These findings demonstrate that repeated reactivation of memory traces during sleep engenders microstructural plasticity which continues days after the stimulation night and is associated with the emergence of memory benefits at the behavioural level.

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Section: Introductionsupporting

confidence: 86%

Section: Introductionsupporting

confidence: 86%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Distributed and gradual microstructure changes track the emergence of behavioural benefit from memory reactivation

Rakowska¹,

Lazari

Cercignani³

et al. 2022

Preprint

Self Cite

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An update on recent advances in targeted memory reactivation during sleep

Carbone,

Diekelmann

2024

npj Sci. Learn.

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Targeted Memory Reactivation (TMR) is a noninvasive tool to manipulate memory consolidation during sleep. TMR builds on the brain’s natural processes of memory reactivation during sleep and aims to facilitate or bias these processes in a certain direction. The basis of this technique is the association of learning content with sensory cues, such as odors or sounds, that are presented during subsequent sleep to promote memory reactivation. Research on TMR has drastically increased over the last decade with rapid developments. The aim of the present review is to highlight the most recent advances of this research. We focus on effects of TMR on the strengthening of memories in the declarative, procedural and emotional memory domain as well as on ways in which TMR can be used to promote forgetting. We then discuss advanced technical approaches to determine the optimal timing of TMR within the ongoing oscillatory activity of the sleeping brain as well as the specificity of TMR for certain memory contents. We further highlight the specific effects of TMR during REM sleep and in influencing dream content. Finally, we discuss recent evidence for potential applications of TMR for mental health, educational purposes and in the home setting. In conclusion, the last years of research have provided substantial advances in TMR that can guide future endeavors in research and application.

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Cognitive neuroscience perspective on memory: overview and summary

Sridhar

Khamaj

Asthana

2023

Front. Hum. Neurosci.

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This paper explores memory from a cognitive neuroscience perspective and examines associated neural mechanisms. It examines the different types of memory: working, declarative, and non-declarative, and the brain regions involved in each type. The paper highlights the role of different brain regions, such as the prefrontal cortex in working memory and the hippocampus in declarative memory. The paper also examines the mechanisms that underlie the formation and consolidation of memory, including the importance of sleep in the consolidation of memory and the role of the hippocampus in linking new memories to existing cognitive schemata. The paper highlights two types of memory consolidation processes: cellular consolidation and system consolidation. Cellular consolidation is the process of stabilizing information by strengthening synaptic connections. System consolidation models suggest that memories are initially stored in the hippocampus and are gradually consolidated into the neocortex over time. The consolidation process involves a hippocampal-neocortical binding process incorporating newly acquired information into existing cognitive schemata. The paper highlights the role of the medial temporal lobe and its involvement in autobiographical memory. Further, the paper discusses the relationship between episodic and semantic memory and the role of the hippocampus. Finally, the paper underscores the need for further research into the neurobiological mechanisms underlying non-declarative memory, particularly conditioning. Overall, the paper provides a comprehensive overview from a cognitive neuroscience perspective of the different processes involved in memory consolidation of different types of memory.

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Cueing motor memory reactivation during NREM sleep engenders learning-related changes in precuneus and sensorimotor structures

Cited by 3 publications

References 85 publications

Distributed and gradual microstructure changes track the emergence of behavioural benefit from memory reactivation

Distributed and gradual microstructure changes track the emergence of behavioural benefit from memory reactivation

An update on recent advances in targeted memory reactivation during sleep

Cognitive neuroscience perspective on memory: overview and summary

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