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From creation to consolidation: a novel framework for memory processing.

Robertson EM - PLoS Biol. (2009)

View Article: PubMed Central - PubMed

Affiliation: Berenson-Allen Centerfor Non-Invasive Brain Stimulation, Harvard Medical School, Beth Israel Deaconess Medical Center, Boston, Massachusetts, USA. emrobert@bidmc.harvard.edu

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These studies have contrasted the patterns of activation before and after consolidation to reveal how the brain has been changed by consolidation... Yet just because the activation of a brain area is changed by consolidation does not mean that area was responsible for supporting consolidation... Disrupting the function of these activated areas, by using TMS or through lesion studies, would determine which areas are necessary for consolidation... Thus, the challenge for future studies is to identify those circuits activated during consolidation, as opposed to those circuits altered by consolidation, and use this as a foundation to define those circuits making a functional contribution to consolidation... These motor skill components are processed offline over different brain states (i.e., sleep versus wakefulness), and so differences in the relative size of these component may restrict the benefits of consolidation to a specific brain state... Potentially, this leads to motor skill acquisition that is predominately goal-based, and as this component is preferentially processed over sleep, to a task that shows sleep-dependent consolidation (; see also )... These heterogeneous changes in functional connectivity during NREM sleep may support reduced connectivity between memory systems, allowing disengagement, while simultaneously supporting enhanced or maintained connectivity within memory systems, allowing the offline processing necessary for memory consolidation... Alternatively, a decrease in functional connectivity may be associated with a specific sleep stage—such as NREM—while other sleep stages support the offline processing within specific memory systems... This alternative implies that when declarative and procedural memories are acquired simultaneously, consolidation will be dependent upon NREM sleep when memory systems are disengaged... Consistent with this prediction are observations that the consolidation of motor skills, when acquired along with declarative knowledge for the skill, is correlated with NREM sleep, whereas when the same motor skill is acquired in isolation, its subsequent consolidation is correlated with REM sleep... Evidence that the memory processing benefits of sleep can be replicated over wakefulness through the loss of declarative knowledge (, Figure 3) implies that the loss of declarative knowledge may be critical for memory processing during sleep... Yet the sleep-related memory processing benefits can occur without a permanent loss of declarative knowledge... Yet this unique framework extends beyond accounting for observations by also making experimentally testable predictions for future work (Box 6)... Direct evidence for a differential organization supporting the offline processing of declarative memories is awaited, and a greater understanding of the relationship between biological events, such as decreases in functional connectivity and the disengagement between memory systems during sleep, is required.

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Distinct Mechanisms Are Engaged To Support the Offline Processing of Motor Skill Memories over Wakefulness and SleepOne set of mechanisms, engaged over wakefulness, is supported by a circuit that includes the M1. In contrast, over sleep, a different circuit that may include the prefrontal and parietal cortices is engaged to support motor skill consolidation. Distinct mechanisms that are differentially engaged over sleep and wakefulness may also be responsible for the consolidation of perceptual and declarative memories. Overlying this differential organization within memory systems are reciprocal interactions between memory systems. Declarative processing can block procedural consolidation, and the reciprocal relationship also occurs, with procedural processing blocking declarative consolidation. These interactions are present over wakefulness (solid arrows) but not over sleep (outline arrows).DLPFC, dorsolateral prefrontal cortex; IPL, inferior parietal lobule.
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pbio-1000019-g005: Distinct Mechanisms Are Engaged To Support the Offline Processing of Motor Skill Memories over Wakefulness and SleepOne set of mechanisms, engaged over wakefulness, is supported by a circuit that includes the M1. In contrast, over sleep, a different circuit that may include the prefrontal and parietal cortices is engaged to support motor skill consolidation. Distinct mechanisms that are differentially engaged over sleep and wakefulness may also be responsible for the consolidation of perceptual and declarative memories. Overlying this differential organization within memory systems are reciprocal interactions between memory systems. Declarative processing can block procedural consolidation, and the reciprocal relationship also occurs, with procedural processing blocking declarative consolidation. These interactions are present over wakefulness (solid arrows) but not over sleep (outline arrows).DLPFC, dorsolateral prefrontal cortex; IPL, inferior parietal lobule.

Mentions: The concepts presented here allow many contemporary observations to be reconciled within a single unified framework (Figure 5). Yet this unique framework extends beyond accounting for observations by also making experimentally testable predictions for future work (Box 6). Direct evidence for a differential organization supporting the offline processing of declarative memories is awaited, and a greater understanding of the relationship between biological events, such as decreases in functional connectivity and the disengagement between memory systems during sleep, is required. Such work will inevitably challenge and perhaps falsify the framework. But the utility of the framework lies within its potential to steer this fledgling and recently rejuvenated field away from the quagmire of disconnected findings and toward more fertile pastures. By so doing, it will help illuminate our understanding of the processing beyond the moment of memory creation, into how memories are consolidated, and so extend our appreciation for how we adapt to this ever changing world.


From creation to consolidation: a novel framework for memory processing.

Robertson EM - PLoS Biol. (2009)

Distinct Mechanisms Are Engaged To Support the Offline Processing of Motor Skill Memories over Wakefulness and SleepOne set of mechanisms, engaged over wakefulness, is supported by a circuit that includes the M1. In contrast, over sleep, a different circuit that may include the prefrontal and parietal cortices is engaged to support motor skill consolidation. Distinct mechanisms that are differentially engaged over sleep and wakefulness may also be responsible for the consolidation of perceptual and declarative memories. Overlying this differential organization within memory systems are reciprocal interactions between memory systems. Declarative processing can block procedural consolidation, and the reciprocal relationship also occurs, with procedural processing blocking declarative consolidation. These interactions are present over wakefulness (solid arrows) but not over sleep (outline arrows).DLPFC, dorsolateral prefrontal cortex; IPL, inferior parietal lobule.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2631067&req=5

pbio-1000019-g005: Distinct Mechanisms Are Engaged To Support the Offline Processing of Motor Skill Memories over Wakefulness and SleepOne set of mechanisms, engaged over wakefulness, is supported by a circuit that includes the M1. In contrast, over sleep, a different circuit that may include the prefrontal and parietal cortices is engaged to support motor skill consolidation. Distinct mechanisms that are differentially engaged over sleep and wakefulness may also be responsible for the consolidation of perceptual and declarative memories. Overlying this differential organization within memory systems are reciprocal interactions between memory systems. Declarative processing can block procedural consolidation, and the reciprocal relationship also occurs, with procedural processing blocking declarative consolidation. These interactions are present over wakefulness (solid arrows) but not over sleep (outline arrows).DLPFC, dorsolateral prefrontal cortex; IPL, inferior parietal lobule.
Mentions: The concepts presented here allow many contemporary observations to be reconciled within a single unified framework (Figure 5). Yet this unique framework extends beyond accounting for observations by also making experimentally testable predictions for future work (Box 6). Direct evidence for a differential organization supporting the offline processing of declarative memories is awaited, and a greater understanding of the relationship between biological events, such as decreases in functional connectivity and the disengagement between memory systems during sleep, is required. Such work will inevitably challenge and perhaps falsify the framework. But the utility of the framework lies within its potential to steer this fledgling and recently rejuvenated field away from the quagmire of disconnected findings and toward more fertile pastures. By so doing, it will help illuminate our understanding of the processing beyond the moment of memory creation, into how memories are consolidated, and so extend our appreciation for how we adapt to this ever changing world.

View Article: PubMed Central - PubMed

Affiliation: Berenson-Allen Centerfor Non-Invasive Brain Stimulation, Harvard Medical School, Beth Israel Deaconess Medical Center, Boston, Massachusetts, USA. emrobert@bidmc.harvard.edu

AUTOMATICALLY GENERATED EXCERPT
Please rate it.

These studies have contrasted the patterns of activation before and after consolidation to reveal how the brain has been changed by consolidation... Yet just because the activation of a brain area is changed by consolidation does not mean that area was responsible for supporting consolidation... Disrupting the function of these activated areas, by using TMS or through lesion studies, would determine which areas are necessary for consolidation... Thus, the challenge for future studies is to identify those circuits activated during consolidation, as opposed to those circuits altered by consolidation, and use this as a foundation to define those circuits making a functional contribution to consolidation... These motor skill components are processed offline over different brain states (i.e., sleep versus wakefulness), and so differences in the relative size of these component may restrict the benefits of consolidation to a specific brain state... Potentially, this leads to motor skill acquisition that is predominately goal-based, and as this component is preferentially processed over sleep, to a task that shows sleep-dependent consolidation (; see also )... These heterogeneous changes in functional connectivity during NREM sleep may support reduced connectivity between memory systems, allowing disengagement, while simultaneously supporting enhanced or maintained connectivity within memory systems, allowing the offline processing necessary for memory consolidation... Alternatively, a decrease in functional connectivity may be associated with a specific sleep stage—such as NREM—while other sleep stages support the offline processing within specific memory systems... This alternative implies that when declarative and procedural memories are acquired simultaneously, consolidation will be dependent upon NREM sleep when memory systems are disengaged... Consistent with this prediction are observations that the consolidation of motor skills, when acquired along with declarative knowledge for the skill, is correlated with NREM sleep, whereas when the same motor skill is acquired in isolation, its subsequent consolidation is correlated with REM sleep... Evidence that the memory processing benefits of sleep can be replicated over wakefulness through the loss of declarative knowledge (, Figure 3) implies that the loss of declarative knowledge may be critical for memory processing during sleep... Yet the sleep-related memory processing benefits can occur without a permanent loss of declarative knowledge... Yet this unique framework extends beyond accounting for observations by also making experimentally testable predictions for future work (Box 6)... Direct evidence for a differential organization supporting the offline processing of declarative memories is awaited, and a greater understanding of the relationship between biological events, such as decreases in functional connectivity and the disengagement between memory systems during sleep, is required.

Show MeSH
Related in: MedlinePlus