Elsevier

Neuroscience

Volume 171, Issue 1, 24 November 2010, Pages 227-234
Neuroscience

Cognitive, Behavioral, and Systems Neuroscience
Research Paper
Sleep consolidates the effector-independent representation of a motor skill

https://doi.org/10.1016/j.neuroscience.2010.07.062Get rights and content

Abstract

During off-line consolidation a motor skill becomes less vulnerable to interference (stabilisation) and improves in performance (enhancement). Here we examined whether off-line consolidation contributes to the process of generalisation in the extrinsic and intrinsic coordinate frame in the motor domain. Participants trained with the left hand a sequential finger tapping task that has proved sensitive to off-line consolidation. Generalisation was tested by the ability to transfer the original sequence (extrinsic transformation) or the mirror sequence (intrinsic transformation) to the right hand, and this was compared with performance on a new sequence not learned before. To determine acute effects on generalisation, transfer was assessed immediately after training of the left hand. To study the effects of off-line consolidation participants were tested after an interval of daytime (training at 8 am and retrieval test on the transfer sequences at 8 pm) or after an interval of night-time sleep (training at 8 pm and retrieval test on the transfer sequences at 8 am). Acutely, training of the left hand induced significant transfer effects to the right hand for the extrinsic transformation of the sequence, but there was no advantage for the intrinsic transformation. After a period of daytime wakefulness the transfer from the left to the right hand for the extrinsic sequence transformation had vanished and, again, there was no transfer effect for the intrinsic transformation of the sequence. By contrast, nocturnal sleep saved the initial transfer effect for the extrinsic sequence transformation. The intrinsic sequence transformation was not affected by sleep. Our results show that an effector-independent representation in an extrinsic co-ordinate frame of a skill develops soon after initial training. Sleep has the capacity to consolidate this transfer and, in this way, contributes to the generalisation of a motor skill.

Section snippets

Participants

Seventy-two healthy subjects aged between 18 and 28 years (mean 23.1 years, SD 2.5 years, 39 females, 33 males) participated in the study. All participants were right-handed as defined by the Edinburgh Handedness Questionnaire (Oldfield, 1971). Exclusion criteria were any neurological, psychiatric or sleep disorder, a history of any impairment to the central nervous system like trauma, infections, tumours, surgical procedures, substance dependency. Musicians, professional typists, shift-working

Finger sequence tapping during training

The six experimental groups did not show significant differences in finger sequence tapping performance in the training phase. Sequence tapping speed significantly improved across the 15 training trails starting with a mean (±SEM) of 10.62±0.60 sequences per 30 s on the 1st trail to 18.14±0.57 sequences per 30 s on the 15th trail (F=56.52, P<0.0001, for ANOVA main effect of “trial”; P>0.7, for main and interaction effects of the “group” factor). In parallel, accuracy improved across the 15

Discussion

We found significant transfer effects after training with the left hand to performance with the right hand for extrinsic transformations of a sequence which were evident already shortly after training. These extrinsic transfer effects were maintained after a 12-h period covering nocturnal sleep, but decayed after a 12-h period of wakefulness. We did not see any transfer effects for an intrinsic transformation of the sequence acutely after training or after 12-h periods of sleep or wakefulness.

Acknowledgments

This work was supported by a grant from the Deutsche ForschungsgemeinschaftSFB 654 “Plasticity and Sleep.”

References (38)

  • M.P. Walker et al.

    Sleep-dependent learning and memory consolidation

    Neuron

    (2004)
  • R.S. Bapi et al.

    Evidence for effector independent and dependent representations and their differential time course of acquisition during motor sequence learning

    Exp Brain Res

    (2000)
  • J. Born et al.

    Sleep to remember

    Neuroscientist

    (2006)
  • A. Cohen et al.

    Attention and structure in sequence learning

    J Exp Psychol Learn Mem Cogn

    (1990)
  • D.A. Cohen et al.

    Off-line learning of motor skill memory: a double dissociation of goal and movement

    Proc Natl Acad Sci U S A

    (2005)
  • S.E. Criscimagna-Hemminger et al.

    Learned dynamics of reaching movements generalize from dominant to nondominant arm

    J Neurophysiol

    (2003)
  • S.E. Criscimagna-Hemminger et al.

    Consolidation patterns of human motor memory

    J Neurosci

    (2008)
  • S. Fischer et al.

    Sleep forms memory for finger skills

    Proc Natl Acad Sci U S A

    (2002)
  • S.M. Fogel et al.

    Learning-dependent changes in sleep spindles and stage 2 sleep

    J Sleep Res

    (2006)
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    Contribution of authors:

    The following authors are responsible for the concept and the design of the study: KW, NM, CB, GD and JB.

    The following authors acquired the data: CB and NM.

    The following authors analysed and interpreted the data: KW, CB, NM, GD, JB.

    The following authors drafted all or part of the paper: KW, NM, JB.

    The following authors critically reviewed the paper: CB, GD.

    The following authors contributed their statistical expertise: KW, NM.

    GD and JB obtained funding and held supervision.

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