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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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Motor Skill Memories Are Differentially Processed over Wakefulness and Sleep(A) The spatial goal of a motor skill is processed over sleep but not during wakefulness, whereas the skilled movements are processed over wakefulness but not over sleep [15]. This double dissociation implies that distinct mechanisms are engaged to support consolidation over wakefulness and sleep. The offline processing of memories during consolidation can be expressed as an offline increase in motor skill [8,46]. (B) Using high-density EEG, the parietal cortex has been implicated in supporting motor skill improvements over sleep [20]. The high-density electrodes (yellow dots) were aligned with a magnetic resonance image of a participant's brain. Following motor skill learning, a cluster of electrodes (white dots, enclosed by a red circle) centered over the parietal cortex showed an increase in slow-wave activity during sleep. (C) In contrast, a circuit that includes M1 makes a critical contribution to the consolidation of motor skills over wakefulness but not over sleep [16–18]. Disruption of M1, by applying TMS, blocks the development of motor skills over wakefulness but not over sleep.
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pbio-1000019-g002: Motor Skill Memories Are Differentially Processed over Wakefulness and Sleep(A) The spatial goal of a motor skill is processed over sleep but not during wakefulness, whereas the skilled movements are processed over wakefulness but not over sleep [15]. This double dissociation implies that distinct mechanisms are engaged to support consolidation over wakefulness and sleep. The offline processing of memories during consolidation can be expressed as an offline increase in motor skill [8,46]. (B) Using high-density EEG, the parietal cortex has been implicated in supporting motor skill improvements over sleep [20]. The high-density electrodes (yellow dots) were aligned with a magnetic resonance image of a participant's brain. Following motor skill learning, a cluster of electrodes (white dots, enclosed by a red circle) centered over the parietal cortex showed an increase in slow-wave activity during sleep. (C) In contrast, a circuit that includes M1 makes a critical contribution to the consolidation of motor skills over wakefulness but not over sleep [16–18]. Disruption of M1, by applying TMS, blocks the development of motor skills over wakefulness but not over sleep.

Mentions: Important clues about the offline processing of memories can be gleaned from understanding how the brain initially encodes memories. The motor skill memories acquired by a squash player, for example, ensure the production of rapid and powerful arm movements, either backhand or forehand, to hit a ball. The goal is always the same—to hit a ball; however, the exact movements can be very different. This classical distinction between goal and movement can be mapped onto distinct brain circuits (Figure 1, [3,12,13]). These distinct circuits are differentially affected by wakefulness and sleep: activity within the goal-component circuit changes substantially between wakefulness and sleep, with far smaller changes in activity occurring within the movement-based circuit [14]. Having differential changes in activity may produce a differential processing of the motor skill components during wakefulness and sleep. Consistent with this idea, experimental work has shown that only the movement component is processed during wakefulness; whereas only the goal component is processed during sleep (Figure 2, [15]). Converging with this behavioral work are observations from functional imaging and transcranial magnetic stimulation (TMS) studies showing that distinct circuits are engaged during wakefulness and sleep to support offline processing (Figure 2, [16–20]).


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

Robertson EM - PLoS Biol. (2009)

Motor Skill Memories Are Differentially Processed over Wakefulness and Sleep(A) The spatial goal of a motor skill is processed over sleep but not during wakefulness, whereas the skilled movements are processed over wakefulness but not over sleep [15]. This double dissociation implies that distinct mechanisms are engaged to support consolidation over wakefulness and sleep. The offline processing of memories during consolidation can be expressed as an offline increase in motor skill [8,46]. (B) Using high-density EEG, the parietal cortex has been implicated in supporting motor skill improvements over sleep [20]. The high-density electrodes (yellow dots) were aligned with a magnetic resonance image of a participant's brain. Following motor skill learning, a cluster of electrodes (white dots, enclosed by a red circle) centered over the parietal cortex showed an increase in slow-wave activity during sleep. (C) In contrast, a circuit that includes M1 makes a critical contribution to the consolidation of motor skills over wakefulness but not over sleep [16–18]. Disruption of M1, by applying TMS, blocks the development of motor skills over wakefulness but not over sleep.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2631067&req=5

pbio-1000019-g002: Motor Skill Memories Are Differentially Processed over Wakefulness and Sleep(A) The spatial goal of a motor skill is processed over sleep but not during wakefulness, whereas the skilled movements are processed over wakefulness but not over sleep [15]. This double dissociation implies that distinct mechanisms are engaged to support consolidation over wakefulness and sleep. The offline processing of memories during consolidation can be expressed as an offline increase in motor skill [8,46]. (B) Using high-density EEG, the parietal cortex has been implicated in supporting motor skill improvements over sleep [20]. The high-density electrodes (yellow dots) were aligned with a magnetic resonance image of a participant's brain. Following motor skill learning, a cluster of electrodes (white dots, enclosed by a red circle) centered over the parietal cortex showed an increase in slow-wave activity during sleep. (C) In contrast, a circuit that includes M1 makes a critical contribution to the consolidation of motor skills over wakefulness but not over sleep [16–18]. Disruption of M1, by applying TMS, blocks the development of motor skills over wakefulness but not over sleep.
Mentions: Important clues about the offline processing of memories can be gleaned from understanding how the brain initially encodes memories. The motor skill memories acquired by a squash player, for example, ensure the production of rapid and powerful arm movements, either backhand or forehand, to hit a ball. The goal is always the same—to hit a ball; however, the exact movements can be very different. This classical distinction between goal and movement can be mapped onto distinct brain circuits (Figure 1, [3,12,13]). These distinct circuits are differentially affected by wakefulness and sleep: activity within the goal-component circuit changes substantially between wakefulness and sleep, with far smaller changes in activity occurring within the movement-based circuit [14]. Having differential changes in activity may produce a differential processing of the motor skill components during wakefulness and sleep. Consistent with this idea, experimental work has shown that only the movement component is processed during wakefulness; whereas only the goal component is processed during sleep (Figure 2, [15]). Converging with this behavioral work are observations from functional imaging and transcranial magnetic stimulation (TMS) studies showing that distinct circuits are engaged during wakefulness and sleep to support offline processing (Figure 2, [16–20]).

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