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The Journal of Neuroscience, March 1, 1998, 18(5):1827-1840
Transition of Brain Activation from Frontal to Parietal Areas in
Visuomotor Sequence Learning
Katsuyuki
Sakai1, 2,
Okihide
Hikosaka1,
Satoru
Miyauchi3,
Ryousuke
Takino4,
Yuka
Sasaki3, and
Benno
Pütz5
1 Department of Physiology, Juntendo University School
of Medicine, Tokyo 113, Japan, 2 Department of Neurology,
Division of Neuroscience, Graduate School of Medicine, University of
Tokyo, Tokyo 113, Japan, 3 Human Neurosystem Science
Section, Intelligent Communications Division, Communications Research
Laboratory, Tokyo 184, Japan, 4 Shiraume Gakuen College,
Tokyo 187, Japan, and 5 Exploratory Research for Advanced
Technology, Japan Science and Technology Corporation, Kyoto 619-02, Japan
We studied the neural correlates of visuomotor sequence learning
using functional magnetic resonance imaging (fMRI). In the test
condition, subjects learned, by trial and error, the correct order of
pressing two buttons consecutively for 10 pairs of buttons (2 × 10 task); in the control condition, they pressed buttons in any order.
Comparison between the test condition and the control condition
revealed four brain areas specifically related to learning: the
dorsolateral prefrontal cortex (DLPFC), the presupplementary motor area
(pre-SMA), the precuneus, and the intraparietal sulcus (IPS). We found
that the time course of activation during learning was different
between these areas. To normalize the individual differences in the
speed of learning, we classified the performance of each subject into
three learning stages: early, intermediate, and advanced stages. Both
the relative increase of signal intensity and the number of activated
pixels within the four areas showed significant changes across the
learning stages, with different time courses. The two frontal areas,
DLPFC and pre-SMA, were activated in the earlier stages of learning,
whereas the two parietal areas, precuneus and IPS, were activated in
the later stages. Specifically, DLPFC, pre-SMA, precuneus, and IPS were
most highly activated in the early stage, in both the early and
intermediate stages, in the intermediate stage, and in both the
intermediate and advanced stages, respectively. The results suggest
that the acquisition of visuomotor sequences requires frontal
activation, whereas the retrieval of visuomotor sequences requires
parietal activation, which might reflect the transition from the
declarative stage to the procedural stage.
Key words:
visuomotor sequence; learning; functional magnetic
resonance imaging; procedure; prefrontal cortex; presupplementary motor
area; precuneus; intraparietal sulcus
Copyright © 1998 Society for Neuroscience 0270-6474/98/1851827-14$05.00/0
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[Full Text]
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[Full Text]
[PDF]
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[Abstract]
[Full Text]
[PDF]
|
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|
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|
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[Full Text]
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|
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|

|
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|
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[Abstract]
[Full Text]
[PDF]
|
 |
|
|