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Pilot fMRI investigation of representational plasticity associated with motor skill learning and its functional consequences

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Abstract

Complex skill learning at a joint initiates competition between its representation in the primary motor cortex (M1) and that of the neighboring untrained joint. This process of representational plasticity has been mapped by cortically-evoking simple movements. We investigated, following skill learning at a joint, 1) whether comparable processes of representational plasticity are observed when mapping is based on volitionally produced complex movements and 2) the consequence on the skill of the adjacent untrained joint. Twenty-four healthy subjects were assigned to either finger- or elbow-skill training or no-training control group. At pretest and posttest, subjects performed complex skill movements at finger, elbow and ankle concurrent with functional magnetic resonance imaging (fMRI) to define learning and allow mapping of corresponding activation-based representations in M1. Skill following both finger- and elbow- training transferred to the ankle (remote joint) (p = 0.05 and 0.05); however, finger training did not transfer to the elbow and elbow training did not transfer to the finger. Following finger training, location of the trained finger representation showed a trend (p = 0.08) for medial shift towards the representation of adjacent untrained elbow joint; the change in intensity of the latter representation was associated with elbow skill (Spearman’s ρ = −0.71, p = 0.07). Following elbow training, the trained elbow representation and the adjacent untrained finger representation increased their overlap (p = 0.02), which was associated with finger skill (Spearman’s ρ = −0.83, p = 0.04). Thus, our pilot study reveals comparable processes of representational plasticity with fMRI mapping of complex skill movements as have been demonstrated with cortically-evoked methods. Importantly, these processes may limit the degree of transfer of skill between trained and adjacent untrained joints. These pilot findings that await confirmation in large-scale studies have significant implications for neuro-rehabilitation. For instance, techniques, such as motor cortical stimulation, that can potentially modulate processes of representational plasticity between trained and adjacent untrained representations, may optimize transfer of skill.

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Abbreviations

M1:

Primary Motor Cortex

ICMS:

Intra Cortical Micro Stimulation

TMS:

Transcranial Magnetic Stimulation

KR:

Knowledge of Results

KP:

Knowledge of Performance

S-R:

Stimulus–Response

FingerGroup :

Finger Tracking Training Group

ElbowGroup :

Elbow Tracking Training Group

ControlGroup :

No Training Control Group

EMG:

Electromygraphy

MRI:

Magnetic Resonance Imaging

fMRI:

Functional Magnetic Resonance Imaging

BOLD:

Blood Oxygen Level-Dependent

EPI:

Echo Planar Imaging

TE:

Echo Time

TR:

Repetition Time

FA:

Flip Angle

FOV:

Field of View

AI:

Accuracy Index

AIFINGER :

Average Accuracy Index for 4 finger tracking trials during tracking test

AIELBOW :

Average Accuracy Index for 4 elbow tracking trials during tracking test

AIANKLE :

Average Accuracy Index for 4 ankle tracking trials during tracking test

GLM:

General Linear Model

FingerVOLUME :

Finger representation, defined by voxels significantly active during finger tracking trials with fMRI

ElbowVOLUME :

Elbow representation, defined by voxels significantly active during elbow tracking trials with fMRI

AnkleVOLUME :

Ankle representation, defined by voxels significantly active during ankle tracking trials with fMRI

POA:

Peak of Activation

FingerPREPOST :

Voxels within finger representation that are commonly active at pretest and posttest

ElbowPREPOST :

Voxels within elbow representation that are commonly active at pretest and posttest

AnklePREPOST :

Voxels within ankle representation that are commonly active at pretest and posttest

ICC:

Intraclass Correlation Coefficient

COM:

Center of Mass

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Acknowledgements

This work was supported by the University of Minnesota’s Doctoral Dissertation Fellowship to [E. B. P.]; National Center for Research Resources at the National Institutes of Health (grant numbers P41 RR008079, M01-RR00400 to Center for Magnetic Resonance and Research, Minneapolis, MN); National Institutes of Health supporting investigator roles- 1K01HD069504 (E. B. P.) and 1 R01 HD 053153-01A2 and 1 RC1 HD063838-01 (J. R. C) and the Program in Physical Therapy at the University of Minnesota. The authors would like to thank Ms. Pooja Arora, Ms. Megan Pline, Ms. Meagan Binenstock, and Dr. Kathleen Anderson for their assistance in data collection and analysis. Also, the authors would like to thank Drs. Theresa Kimberley, James Ashe and Carl Kukulka for valuable feedback.

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Authors and Affiliations

  1. Department of Biomedical Engineering, Lerner Research Institute, Department of Physical Medicine and Rehabilitation, Neurological Institute, Center for Neurological Restoration, Neurological Institute, Cleveland Clinic, 9500 Euclid Avenue, ND20, Cleveland, OH, 44195, USA

    Ela B. Plow

  2. Program in Rehabilitation Science, University of Minnesota, Minneapolis, MN, 55455, USA

    Ela B. Plow

  3. Program in Physical Therapy, University of Minnesota, University of Minnesota Medical School, University of Minnesota, 388 MMC, 420 Delaware St SE, Minneapolis, MN , 55455, USA

    James R. Carey

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  1. Ela B. Plow
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  2. James R. Carey
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Correspondence to Ela B. Plow.

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Plow, E.B., Carey, J.R. Pilot fMRI investigation of representational plasticity associated with motor skill learning and its functional consequences. Brain Imaging and Behavior 6, 437–453 (2012). https://doi.org/10.1007/s11682-012-9158-3

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  • DOI: https://doi.org/10.1007/s11682-012-9158-3

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