fMRI and sleep correlates of the age‐related impairment in motor memory consolidation

Fogel, Stuart; Albouy, Geneviève; Vien, Catherine; Popovicci, Romana; King, Bradley R.; Hoge, Rick; Jbabdi, Saâd; Benali, Habib; Karni, Avi; Maquet, Pierre; Carrier, Julie; Doyon, Julien

doi:10.1002/hbm.22426

Cited by 134 publications

(163 citation statements)

References 104 publications

(194 reference statements)

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“…By contrast, performance on the motor, striatal-dependent memory trace was maintained, but not enhanced, irrespective of the sleep condition. These results are in agreement with an increasing number of studies linking hippocampal activity to sleep-related motor sequence memory consolidation processes (Albouy et al, 2008(Albouy et al, , 2013aFogel et al, 2014;Spencer et al, 2006;Steele and Penhune, 2010;Walker et al, 2005). Interestingly, our results also indicate that such sleep-related processes were not triggered for the striatal-dependent memory trace as performance was maintained, and not enhanced, during retest.…”

Section: Independence and Interaction Of The Striato-and Hippocampo-csupporting

confidence: 94%

Maintaining vs. enhancing motor sequence memories: Respective roles of striatal and hippocampal systems

et al. 2015

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Section: Independence and Interaction Of The Striato-and Hippocampo-csupporting

confidence: 94%

Maintaining vs. enhancing motor sequence memories: Respective roles of striatal and hippocampal systems

et al. 2015

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“…There are a few existing memory consolidation, sleep, and aging studies that have used napping paradigms, but these studies focused on procedural, or motor, memory consolidation. [56][57][58][59] The important point here is that whereas most research has indicated an age-related change in sleep-dependent procedural memory consolidation, 60 some researchers have reported that episodic memory consolidation is preserved in older adults. 61 The current evidence compels the conclusion that sleep intervals will not always benefit episodic memory consolidation in older adults, even when using methods that aim to minimize age deficits at encoding and retrieval.…”

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confidence: 95%

The Effects of an Afternoon Nap on Episodic Memory in Young and Older Adults

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Decker

et al. 2017

Sleep

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Study Objectives: In young adults, napping is hypothesized to benefit episodic memory retention (eg, via consolidation). Whether this relationship is present in older adults has not been adequately tested but is an important question because older adults display marked changes in sleep and memory. Design: Between-subjects design. Setting: Sleep laboratory at Emory University School of Medicine. Participants: Fifty healthy young adults (18-29) and 45 community-dwelling older adults (58-83). Intervention: Participants were randomly assigned to a 90-minute nap opportunity or an equal interval of quiet wakefulness. Measurements and Results: Participants underwent an item-wise directed forgetting learning procedure in which they studied words that were individually followed by the instruction to "remember" or "forget." Following a 90-minute retention interval filled with quiet wakefulness or a nap opportunity, they were asked to free recall and recognize those words. Young adults retained significantly more words following a nap interval than a quiet wakefulness interval on both free recall and recognition tests. There was modest evidence for greater nap-related retention of "remember" items relative to "forget" items for free recall but not recognition. Older adults' memory retention did not differ across nap and quiet wakefulness conditions, although they demonstrated greater fragmentation, lower N3, and lower rapid eye movement duration than the young adults. Conclusions: In young adults, an afternoon nap benefits episodic memory retention, but such benefits decrease with advancing age.

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“…Healthy older adults show general slowing in the execution of sequence learning tasks and fail to demonstrate a sleep benefit (Spencer et al 2007;Wilson et al 2012;Fogel et al 2013). While prior studies in older adults showed no global change in response times following sleep or wake (Spencer et al 2007;Wilson et al 2012), no previous work has examined item-specific changes following sleep in an aging population.…”

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“…Consequently, efficient learning of the MSL task relies on motor chunk concatenation, represented behaviorally as faster transitions between chunks (Verwey 2001;Wright et al 2010). Kuriyama et al (2004) demonstrated that this selective enhancement of the slowest transitions occurs maximally over sleep in young adults.Post-sleep enhancement of MSL is reduced in older age (Spencer et al 2007;Wilson et al 2012;Fogel et al 2013;Gudberg et al 2015). Healthy older adults show general slowing in the execution of sequence learning tasks and fail to demonstrate a sleep benefit (Spencer et al 2007;Wilson et al 2012;Fogel et al 2013).…”

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Insufficient chunk concatenation may underlie changes in sleep-dependent consolidation of motor sequence learning in older adults

et al. 2016

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Sleep enhances motor sequence learning (MSL) in young adults by concatenating subsequences ("chunks") formed during skill acquisition. To examine whether this process is reduced in aging, we assessed performance changes on the MSL task following overnight sleep or daytime wake in healthy young and older adults. Young adult performance enhancement was correlated with nREM2 sleep, and facilitated by preferential improvement of slowest within-sequence transitions. This effect was markedly reduced in older adults, and accompanied by diminished sigma power density (12-15 Hz) during nREM2 sleep, suggesting that diminished chunk concatenation following sleep may underlie reduced consolidation of MSL in older adults.[Supplemental material is available for this article.]Optimal execution of motor skills relies on precise temporal sequencing of associated events. For young adults, sleep following learning, in the absence of further practice, enhances performance on motor sequence learning (MSL) tasks (Walker et al. 2002;Fischer et al. 2005;Nishida and Walker 2007;Doyon et al. 2009;Barakat et al. 2011;Wilson et al. 2012;Pace-Schott and Spencer 2013). This enhancement is significantly greater than that observed over an equivalent interval of wake, and is not merely a consequence of general increases in motor responding (Fischer et al. 2002;Spencer et al. 2006Spencer et al. , 2007.Recent work has suggested the importance of stage 2 nonrapid eye movement sleep (nREM2) for enhancing MSL (Walker et al. 2002;Nishida and Walker 2007;Peters et al. 2007;Tucker and Fishbein 2009). High frequency (12-15 Hz) thalamocortical oscillations, or sleep spindles, occurring during nREM2 have been implicated as a possible mechanism for sleep-related MSL improvements. These electrophysiological events induce longterm potentiation in the neocortex, a process crucial for memory consolidation (Sejnowskli and Destexhe 2000;Rosanova and Ulrich 2005;Fogel and Smith 2006;Nishida and Walker 2007;Bergmann et al. 2008;Tucker and Fishbein 2009; Foge et al. 2013).As motor sequence learning develops, distinct subsequences of movements are grouped together, a process termed "chunking" (Rosenbaum et al. 1983;Klapp 1995;Sakai et al. 2003). For instance, during the execution of a seven-item sequence (e.g., 2 -4-2-3 -4 -1 -3), items may be represented in memory as smaller subsequences, or "chunks" (e.g., 2 -4 -2, 3 -4, and 1 -3; Kennerley et al. 2004;). With each chunk representing a distinct memory unit, slowest transitions are expected "between" chunks, reflecting additional memory retrieval effort. Conversely, the fastest transitions indicate movements "within" chunks, or within a memory unit. Consequently, efficient learning of the MSL task relies on motor chunk concatenation, represented behaviorally as faster transitions between chunks (Verwey 2001;Wright et al. 2010). Kuriyama et al. (2004) demonstrated that this selective enhancement of the slowest transitions occurs maximally over sleep in young adults.Post-sleep enhancement of MSL is reduced in older a...

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fMRI and sleep correlates of the age‐related impairment in motor memory consolidation

Cited by 134 publications

References 104 publications

Maintaining vs. enhancing motor sequence memories: Respective roles of striatal and hippocampal systems

Maintaining vs. enhancing motor sequence memories: Respective roles of striatal and hippocampal systems

The Effects of an Afternoon Nap on Episodic Memory in Young and Older Adults

Insufficient chunk concatenation may underlie changes in sleep-dependent consolidation of motor sequence learning in older adults

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