Elsevier

Neuroscience

Volume 133, Issue 4, 2005, Pages 911-917
Neuroscience

Behavioural neuroscience
Sleep-dependent motor memory plasticity in the human brain

https://doi.org/10.1016/j.neuroscience.2005.04.007Get rights and content

Abstract

Growing evidence indicates a role for sleep in off-line memory processing, specifically in post-training consolidation. In humans, sleep has been shown to trigger overnight learning on a motor-sequence memory task, while equivalent waking periods produce no such improvement. But while the behavioral characteristics of sleep-dependent motor learning become increasingly well characterized, the underlying neural basis remains unknown. Here we present functional magnetic resonance imaging data demonstrating a change in the representation of a motor memory after a night of sleep. Subjects trained on a motor-skill memory and 12 hours later, after either sleep or wake, were retested during functional magnetic resonance imaging. Following sleep relative to wake, regions of increased activation were expressed in the right primary motor cortex, medial prefrontal lobe, hippocampus and left cerebellum; changes that can support faster motor output and more precise mapping of key-press movements. In contrast, signal decreases were identified in parietal cortices, the left insular cortex, temporal pole and fronto-polar region, reflecting a reduced need for conscious spatial monitoring and a decreased emotional task burden. This evidence of an overnight, systems-level change in the representation of a motor memory holds important implications for acquiring real-life skills and in clinical rehabilitation following brain trauma, such as stroke.

Section snippets

Experimental procedures

The experiment was approved by the local human studies committee, and in accordance with the principles of the Declaration of Helsinki.

Behavioral data

At the end of the initial training sessions in the NIGHT-SLEEP and DAY-WAKE protocols (average of trials 10–12), subjects achieved near identical performance levels (Speed: 17.55 [1.59±S.E.M.] vs. 17.91 [1.79±S.E.M.] sequences/trial respectively, paired t-test [t(11)=0.46, P=0.64]; Error Rate: 0.11 [0.03±S.E.M.] vs. 0.13 [0.02±S.E.M.] errors/sequence respectively, paired t-test [t(11)=0.83, P=0.42]). Therefore, the post-training level of acquired skill did not differ between the two conditions,

Discussion

We have identified regionally specific differences in functional activation during retesting on a motor-sequence task following a night of sleep, relative to a corresponding time interval awake. These changes cannot be explained either by 1) differences in initial training, since subjects received the same amount of initial practice, and achieved similar post-training skill levels, or 2) circadian influences on performance-related brain activation, since a separate comparison of task-related

Conclusions

In summary, these findings describe a systems-level change in the neural representation of a learned motor-sequence following a night of sleep. This pattern of overnight plasticity, associated with sleep-dependent memory processing, holds important implications for the learning of countless real-life motor skills, and also suggests its potential impairment or complete absence in psychiatric disorders expressing a failure of normal sleep-dependent motor learning (Manoach et al., 2004). It also

Acknowledgments

The authors wish to thank Drs. Christian Gaiser, Seung-Schik Yoo, Edward Pace-Schott and Edwin Robertson for their guidance and helpful comments regarding these findings, and Alex Morgan for technical assistance. This work was supported in part by grants from the National Institutes of Health (MH 48,832; MH 65,292; MH 67,754; MH 69,935 and NS 45,049) and the Dana Foundation.

References (44)

  • E.M. Robertson et al.

    Awareness modifies the skill-learning benefits of sleep

    Curr Biol

    (2004)
  • H.E. Schendan et al.

    An FMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning

    Neuron

    (2003)
  • J.D. Schmahmann et al.

    Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space

    Neuroimage

    (1999)
  • I. Toni et al.

    The time course of changes during motor sequence learninga whole-brain fMRI study

    Neuroimage

    (1998)
  • L.G. Ungerleider et al.

    Imaging brain plasticity during motor skill learning

    Neurobiol Learn Mem

    (2002)
  • M.P. Walker et al.

    Practice with sleep makes perfectsleep dependent motor skill learning

    Neuron

    (2002)
  • M.P. Walker et al.

    Sleep-dependent learning and memory consolidation

    Neuron

    (2004)
  • M. Atienza et al.

    Posttraining sleep enhances automaticity in perceptual discrimination

    J Cogn Neurosci

    (2004)
  • V.B. Brooks

    How does the limbic system assist motor learning? A limbic comparator hypothesis

    Brain Behav Evol

    (1986)
  • K.M. Fenn et al.

    Consolidation during sleep of perceptual learning of spoken language

    Nature

    (2003)
  • S. Fischer et al.

    Sleep forms memory for finger skills

    Proc Natl Acad Sci U S A

    (2002)
  • K. Friston et al.

    Statistical parametric maps in functional imaginga general linear approach

    Hum Brain Mapp

    (1995)
  • Cited by (235)

    View all citing articles on Scopus
    View full text