Sleep and motor learning: Is there room for consolidation?

Pan, Steven C.; Rickard, Timothy C.

doi:10.1037/bul0000009

Cited by 154 publications

(230 citation statements)

References 74 publications

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“…Minutes in rapid eye movement (REM) sleep, on the other hand, are associated with improvements in implicit memory [e.g., unconscious, priming, procedural skills (4,5)]. However, recent reviews and meta-analyses of the literature report inconsistencies in these findings (6,7), suggesting that there may be unexplored factors critical to sleep-dependent memory consolidation.…”

mentioning

confidence: 94%

Autonomic activity during sleep predicts memory consolidation in humans

Whitehurst

Cellini

McDevitt

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Throughout history, psychologists and philosophers have proposed that good sleep benefits memory, yet current studies focusing on the relationship between traditionally reported sleep features (e.g., minutes in sleep stages) and changes in memory performance show contradictory findings. This discrepancy suggests that there are events occurring during sleep that have not yet been considered. The autonomic nervous system (ANS) shows strong variation across sleep stages. Also, increases in ANS activity during waking, as measured by heart rate variability (HRV), have been correlated with memory improvement. However, the role of ANS in sleepdependent memory consolidation has never been examined. Here, we examined whether changes in cardiac ANS activity (HRV) during a daytime nap were related to performance on two memory conditions (Primed and Repeated) and a nonmemory control condition on the Remote Associates Test. In line with prior studies, we found sleep-dependent improvement in the Primed condition compared with the Quiet Wake control condition. Using regression analyses, we compared the proportion of variance in performance associated with traditionally reported sleep features (model 1) vs. sleep features and HRV during sleep (model 2). For both the Primed and Repeated conditions, model 2 (sleep + HRV) predicted performance significantly better (73% and 58% of variance explained, respectively) compared with model 1 (sleep only, 46% and 26% of variance explained, respectively). These findings present the first evidence, to our knowledge, that ANS activity may be one potential mechanism driving sleep-dependent plasticity.sleep | heart rate variability | memory | consolidation | vagal activity S leep has been shown to facilitate the transformation of recent experiences into stable, long-term memories (i.e., consolidation), and specific electrophysiological sleep features have been implicated in this process (1). For example, minutes spent in slow wave sleep (SWS) and the number of sleep spindles [transient neural events in nonrapid eye movement (NREM) sleep, 12-15 Hz] in a posttraining sleep period correlate with the magnitude of explicit memory improvement [e.g., conscious, episodic memories (2, 3)]. Minutes in rapid eye movement (REM) sleep, on the other hand, are associated with improvements in implicit memory [e.g., unconscious, priming, procedural skills (4, 5)]. However, recent reviews and meta-analyses of the literature report inconsistencies in these findings (6, 7), suggesting that there may be unexplored factors critical to sleep-dependent memory consolidation.One possible influence that has received little attention in the sleep and memory literature is the autonomic nervous system (ANS). This lack of attention is somewhat surprising, considering that the literature describing ANS modulation of memory during wake is well established (8). Studies have found that memory storage of new information can be enhanced or impaired by directly modifying the activity of peripheral hormones following acquisition (9...

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mentioning

confidence: 94%

Autonomic activity during sleep predicts memory consolidation in humans

Whitehurst

Cellini

McDevitt

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…In several studies, researchers have identified a number of moderating variables that may account for at least a portion of the performance improvement following sleep (see Pan and Rickard, 2015, for a comprehensive review and meta-analysis). Some of these data even suggest that under some circumstances, skill performance after sleep may not be better than after a period of wakefulness (e.g., Backhaus et al, 2016), inviting a reconsideration of sleep’s theoretical role in the consolidation of procedural memories (Nettersheim et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Task Complexity Modulates Sleep-Related Offline Learning in Sequential Motor Skills

Blischke

Malangré

2017

Front. Hum. Neurosci.

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Recently, a number of authors have advocated the introduction of gross motor tasks into research on sleep-related motor offline learning. Such tasks are often designed to be more complex than traditional key-pressing tasks. However, until now, little effort has been undertaken to scrutinize the role of task complexity in any systematic way. Therefore, the effect of task complexity on the consolidation of gross motor sequence memory was examined by our group in a series of three experiments. Criterion tasks always required participants to produce unrestrained arm movement sequences by successively fitting a small peg into target holes on a pegboard. The sequences always followed a certain spatial pattern in the horizontal plane. The targets were visualized prior to each transport movement on a computer screen. The tasks differed with respect to sequence length and structural complexity. In each experiment, half of the participants initially learned the task in the morning and were retested 12 h later following a wake retention interval. The other half of the subjects underwent practice in the evening and was retested 12 h later following a night of sleep. The dependent variables were the error rate and total sequence execution time (inverse to the sequence execution speed). Performance generally improved during acquisition. The error rate was always low and remained stable during retention. The sequence execution time significantly decreased again following sleep but not after waking when the sequence length was long and structural complexity was high. However, sleep-related offline improvements were absent when the sequence length was short or when subjects performed a highly regular movement pattern. It is assumed that the occurrence of sleep-related offline performance improvements in sequential motor tasks is associated with a sufficient amount of motor task complexity.

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“…Sleep is critical for learning and memory consolidation38. For declarative memory, slow wave sleep has a beneficial effect on the consolidation of memories acquired during preceding wakefulness338.…”

Section: Discussionmentioning

confidence: 99%

“…For declarative memory, slow wave sleep has a beneficial effect on the consolidation of memories acquired during preceding wakefulness338. Sleep/wake cycles are controlled by the super chiasmic nucleus in the hypothalamus, but can be disrupted by diseases of the nervous system, causing sleep disorders.…”

Section: Discussionmentioning

confidence: 99%

Imbalance between TNFα and progranulin contributes to memory impairment and anxiety in sleep-deprived mice

Zhang

Feng

et al. 2017

Sci Rep

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Sleep disorder is becoming a widespread problem in current society, and is associated with impaired cognition and emotional disorders. Progranulin (PGRN), also known as granulin epithelin precursor, promotes neurite outgrowth and cell survival, and is encoded by the GRN gene. It is a tumor necrosis factor α receptor (TNFR) ligand which is implicated in many central nervous system diseases. However, the role PGRN in sleep disorder remains unclear. In the present study, we found that sleep deprivation (S-DEP) impaired the memory and produced thigmotaxis/anxiety-like behaviors in mice. S-DEP increased the levels of TNFα but decreased PGRN levels in the hippocampus. The intracerebroventricular (ICV) injection of PGRN or intraperitoneal injection of TNFα synthesis blocker thalidomide (25 mg/kg), prevented the memory impairment and anxiety behaviors induced by S-DEP. PGRN treatment also restored dendritic spine density in the hippocampus CA1 region and neurogenesis in hippocampus dentate gyrus (DG). These results indicate that an imbalance between TNFα and PGRN contributes to memory impairment and thigmotaxis/anxiety caused by sleep deprivation.

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Sleep and motor learning: Is there room for consolidation?

Cited by 154 publications

References 74 publications

Autonomic activity during sleep predicts memory consolidation in humans

Autonomic activity during sleep predicts memory consolidation in humans

Task Complexity Modulates Sleep-Related Offline Learning in Sequential Motor Skills

Imbalance between TNFα and progranulin contributes to memory impairment and anxiety in sleep-deprived mice

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