Neural substrates of motor memory consolidation depend on practice structure

Journal name:
Nature Neuroscience
Volume:
13,
Pages:
923–925
Year published:
DOI:
doi:10.1038/nn.2596
Received
Accepted
Published online

Motor-skill practice drives subsequent offline activity in functionally related resting human brain networks. We investigated the manner in which offline neural networks are modulated by practice structures that affect motor-skill retention. Interference to dorsolateral-prefrontal cortex (DLPFC), but not to primary motor cortex (M1), after variable practice attenuated motor-skill retention, whereas interference to M1, but not to DLPFC, after constant practice attenuated motor-skill retention. We conclude that neural substrates of motor-memory consolidation are modulated by practice structure.

At a glance

Figures

  1. Experimental design.
    Figure 1: Experimental design.

    Participants practiced the task on day 1 either under a constant practice condition or variable practice condition. Immediately following practice, they were tested for EoA performance. Participants were re-tested on a retention test (R) to infer learning of target A3 (criterion task) 1 d later. Participants from each practice condition (constant and variable) were randomized to a control no-rTMS group (constant practice (CP), variable practice (VP)), an M1-interference group (CP-M1, VP-M1) and a DLPFC-interference group (CP-DLPFC, VP-DLPFC). The M1-interference groups received 1-Hz rTMS over M1 and the DLPFC-interference groups received 1-Hz rTMS over DLPFC, immediately after EoA. The black dots represent measurement of corticospinal excitability.

  2. Practice structure and offline motor-memory stabilization.
    Figure 2: Practice structure and offline motor-memory stabilization.

    EoA and retention error (RMSE) of participants in the control, M1 interference, DLPFC interference, and delayed interference (VP-DLPFC 4 h and CP-M1 4 h) groups. Left, rTMS interference to DLPFC (gray-filled circle), but not to M1 (black-filled circle), after variable practice attenuated offline motor skill stabilization between EoA and retention compared with the control group (open circle). Performance stabilization between EoA and retention was attenuated only when rTMS was applied over DLPFC immediately after variable practice (gray-filled circle), but not when applied 4 h post-practice (blue-filled square). Right, immediately after constant practice, rTMS to M1 (black-filled circle), but not to DLPFC (gray-filled circle), attenuated offline stabilization of the motor skill compared with the no-rTMS group (open circle). Performance from EoA to retention was significantly attenuated when rTMS was applied over M1 immediately after constant practice (black-filled circle), but not when applied 4 h post-practice (green-filled square). Error bars represent the s.e.m.

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Author information

Affiliations

  1. Motor Behavior and Neurorehabilitation Laboratory, Division of Biokinesiology and Physical Therapy at the Herman Ostrow School of Dentistry, University of Southern California, Los Angeles, California, USA.

    • Shailesh S Kantak,
    • Katherine J Sullivan,
    • Beth E Fisher &
    • Carolee J Winstein
  2. Neuroplasticity and Imaging Laboratory, Division of Biokinesiology and Physical Therapy at the Herman Ostrow School of Dentistry, University of Southern California, Los Angeles, California, USA.

    • Shailesh S Kantak &
    • Beth E Fisher
  3. Department of Psychology, University of California, Los Angeles, California, USA.

    • Barbara J Knowlton
  4. Department of Neurology, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.

    • Carolee J Winstein

Contributions

S.S.K. provided the theoretical framework, designed the study, conducted experiments, analyzed the data and wrote the manuscript. K.J.S., B.E.F. and B.J.K. helped with the experimental design, data analyses and manuscript writing. C.J.W. provided the theoretical framework and helped with experimental design, data analysis and manuscript writing. K.J.S., B.E.F. and C.J.W. supervised the project.

Competing financial interests

The authors declare no competing financial interests.

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Supplementary information

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    Supplementary Figure 1, Supplementary Results, Supplementary Methods and Supplementary Discussion

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