Daytime sleep condenses the time course of motor memory consolidation

Korman, Maria; Doyon, Julien; Doljansky, Julia; Carrier, Julie; Dagan, Yaron; Karni, Avi

doi:10.1038/nn1959

Cited by 369 publications

(453 citation statements)

References 49 publications

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“…Positive offline effects, which we observed only in the anodal tDCS group, are thus not a ubiquitous phenomenon in skill acquisition. Nevertheless, positive offline effects have garnered a great deal of attention in recent years as they have been reported in several influential studies of skill consolidation with finger-sequencing tasks (8,42). To the best of our knowledge, there has been little comment about why some skill tasks show a warm-up decrement whereas others show consolidation.…”

Section: Discussionmentioning

confidence: 99%

Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation

Reis

Schambra

Cohen

et al. 2009

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

1,201

1,130

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Motor skills can take weeks to months to acquire and can diminish over time in the absence of continued practice. Thus, strategies that enhance skill acquisition or retention are of great scientific and practical interest. Here we investigated the effect of noninvasive cortical stimulation on the extended time course of learning a novel and challenging motor skill task. A skill measure was chosen to reflect shifts in the task's speed-accuracy tradeoff function (SAF), which prevented us from falsely interpreting variations in position along an unchanged SAF as a change in skill. Subjects practiced over 5 consecutive days while receiving transcranial direct current stimulation (tDCS) over the primary motor cortex (M1). Using the skill measure, we assessed the impact of anodal (relative to sham) tDCS on both within-day (online) and betweenday (offline) effects and on the rate of forgetting during a 3-month follow-up (long-term retention). There was greater total (online plus offline) skill acquisition with anodal tDCS compared to sham, which was mediated through a selective enhancement of offline effects. Anodal tDCS did not change the rate of forgetting relative to sham across the 3-month follow-up period, and consequently the skill measure remained greater with anodal tDCS at 3 months. This prolonged enhancement may hold promise for the rehabilitation of brain injury. Furthermore, these findings support the existence of a consolidation mechanism, susceptible to anodal tDCS, which contributes to offline effects but not to online effects or long-term retention.long-term retention ͉ motor cortex ͉ motor learning ͉ transcranial direct current stimulation (tDCS) ͉ transcranial magnetic stimulation (TMS) A ccurate motor performance is essential to almost everything we do, from typing, to driving, to playing sports. Having a motor skill implies a level of performance in a given task that is only achievable through practice (1). Evidence indicates that motor skill learning can continue over a prolonged time period (2-5). Within-session performance improvements (online effects) occur in the minutes or hours of a single training session and continue over days and weeks of repeated training sessions until performance nears asymptotic levels. Changes in performance can also occur between training sessions (offline effects), i.e., performance at the beginning of session n ϩ 1 is different from performance at the end of session n (6, 7). We have intentionally chosen to avoid the use of the term ''offline learning'' because it has been used to refer to both a physiological process (consolidation) (6) and a particular measurement result (a positive offline effect) (8). Offline effects could also be negative, presumably because of forgetting processes (7). Skills can be retained to varying degrees over weeks to months after the completion of training (long-term retention) (5). Here we investigated the effect of noninvasive cortical stimulation on measurements of these 3 temporal components of skill learning (online effects, of...

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Section: Discussionmentioning

confidence: 99%

Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation

Reis

Schambra

Cohen

et al. 2009

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

1,201

1,130

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“…Naps, in contrast to caffeine, have been shown to enhance not only alertness and attention, but also some forms of memory consolidation. In particular, naps (daytime sleep between 5-90minutes) appear to improve performance on non-medio-temporal lobe dependent, procedural skills (Mednick et al 2002;Mednick et al 2003;Korman et al 2007;Nishida et al 2007). Mednick and colleagues reported that a mid-day nap can also reverse perceptual deterioration that builds with repeated within-day testing (Mednick et al 2002).…”

Section: Introductionmentioning

confidence: 99%

Comparing the benefits of caffeine, naps and placebo on verbal, motor and perceptual memory

Mednick

Cai

Kanady

et al. 2008

Behavioural Brain Research

108

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Caffeine, the world's most common psychoactive substance, is used by approximately 90% of North Americans everyday. Little is known, however, about its benefits for memory. Napping has been shown to increase alertness and promote learning on some memory tasks. We directly compared caffeine (200mg) with napping (60-90 minutes) and placebo on three distinct memory processes: declarative verbal memory, procedural motor skills, and perceptual learning. In the verbal task, recall and recognition for unassociated words were tested after a 7hr retention period (with a betweensession nap or drug intervention). A second, different, word list was administered post-intervention and memory was tested after a 20min retention period. The non-declarative tasks (finger tapping task and texture discrimination task) were trained before the intervention and then retested afterwards. Naps enhanced recall of words after a 7hr and 20min retention interval relative to both caffeine and placebo. Caffeine significantly impaired motor learning compared to placebo and naps. Napping produced robust perceptual learning compared with placebo; however, naps and caffeine were not significantly different. These findings provide evidence of the limited benefits of caffeine for memory improvement compared with napping. We hypothesize that impairment from caffeine may be restricted to tasks that contain explicit information; whereas strictly implicit learning is less compromised.

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“…Altogether, the results suggest that basic mechanisms of plasticity necessary for movement sequence learning, and its consolidation into long-term "how to" memory are preserved in moderatesevere patients with TBI, even in individuals with low functional baseline performance. Korman et al (2007) found, in healthy individuals, that the "offline" overnight improvements in performance, following a single training session, were on the order of the contribution of within-session gains. The patients with TBI in the current study, showed a pattern similar to that of the healthy controls ( Figure 3B) of both within-session and betweensession, consolidation phase, gains, although the high betweenindividuals variance and the small number of participants resulted in only marginally significant changes.…”

Section: Discussionmentioning

confidence: 90%

“…In both young (Korman et al, 2007) and older (Korman et al, 2015) healthy adults an interval of sleep has been implicated as a necessary factor in advancing procedural memory processes and the expression of delayed, "offline" gains in the FOS learning task. An association between sleep disturbances and motor learning has been demonstrated in patients with obstructive sleep apnea, with marked impairment in consolidation (Landry et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…(ii) Consolidation phase-a latent phase lasting several hours, wherein sensitivity to interference decreases and additional, delayed "offline" gains emerge. Post-training affordance of conflicting tasks and/or poor sleep can hamper the course of learning a new motor sequence, by interacting selectively with the consolidation processes (Brashers-Krug et al, 1996;Korman et al, 2007;Lohse et al, 2014;Albouy et al, 2016;Friedman and Korman, 2016). The offline gains in performance presumably indicate the successful completion of procedural memory consolidation processes, commenced by the practice session but requiring additional time, including time in sleep, to evolve (Diekelmann et al, 2009;Borragán et al, 2015).…”

Section: Memory Deficits In Tbimentioning

confidence: 99%

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Atypical within-session motor procedural learning after traumatic brain injury but well-preserved between-session procedural memory consolidation

Sacher

Cisamariu

Shaklai

et al. 2018

Annals of Physical and Rehabilitation Medicine

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Using the finger-to-thumb opposition sequence (FOS) learning task, we characterized motor skill learning in sub-acute patients hospitalized for rehabilitation following traumatic brain injury (TBI). Ten patients (Trained TBI) and 11 healthy participants (Trained Healthy) were trained using a multi-session protocol: a single session was afforded in the first week of the study, and four daily sessions were afforded during the second week. Intensity of practice was adapted to patients. Performance speed and accuracy were tested before and after each session. Retention was tested 1 month later. Ten patients (Control TBI) had no FOS training and were tested only at the beginning and the end of the 6 week period. Although baseline performance on the FOS was very slow, all three phases of skill learning found in healthy adults (acquisition, between-session consolidation gains, and long-term retention) could be identified in patients with TBI. However, their time-course of learning was atypical. The Trained TBI group improved in speed about double the spontaneous improvements observed in the Control TBI group, with no speed-accuracy tradeoff. Normalized to their initial performance on the FOS, the gains accrued by the Trained TBI group after a first training were comparable to those accrued by healthy adults. Only during the second week with daily training, the rate of improvement of the Trained TBI group lagged behind that of the Trained Healthy group, due to increasing within-sessions losses in performance speed; no such losses were found in healthy participants. The Functional Independence Measure scores at the start of the study correlated with the total gains attained at the end of the study; no correlations were found with severity of injury or explicit memory impairments. Despite within-sessions losses in performance, which we propose reflect cognitive fatigue, training resulted in robust overall learning and long-term retention in patients with moderate-severe TBI. Given that the gains in performance evolved mainly between sessions, as delayed, offline, gains, our results suggest that memory consolidation processes can be effectively engaged in patients with TBI. However, practice protocols and schedules may need to be optimized to better engage the potential for long-term plasticity in these patients.

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Daytime sleep condenses the time course of motor memory consolidation

Cited by 369 publications

References 49 publications

Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation

Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation

Comparing the benefits of caffeine, naps and placebo on verbal, motor and perceptual memory

Atypical within-session motor procedural learning after traumatic brain injury but well-preserved between-session procedural memory consolidation

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