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Journal of Neuroscience, Vol 14, 3775-3790, Copyright © 1994 by Society for Neuroscience
Motor sequence learning: a study with positron emission tomography
IH Jenkins, DJ Brooks, PD Nixon, RS Frackowiak and RE Passingham
MRC Cyclotron Unit, Hammersmith Hospital, London, United Kingdom.
We have used positron emission tomography to study the functional anatomy
of motor sequence learning. Subjects learned sequences of keypresses by
trial and error using auditory feedback. They were scanned with eyes closed
under three conditions: at rest, while performing a sequence that was
practiced before scanning until overlearned, and while learning new
sequences at the same rate of performance. Compared with rest, both
sequence tasks activated the contralateral sensorimotor cortex to the same
extent. Comparing new learning with performance of the prelearned sequence,
differences in activation were identified in other areas. (1) Prefrontal
cortex was only activated during new sequence learning. (2) Lateral
premotor cortex was significantly more activated during new learning,
whereas the supplementary motor area was more activated during performance
of the prelearned sequence. (3) Activation of parietal association cortex
was present during both motor tasks, but was significantly greater during
new learning. (4) The putamen was equally activated by both conditions. (5)
The cerebellum was activated by both conditions, but the activation was
more extensive and greater in degree during new learning. There was an
extensive decrease in the activity of prestriate cortex, inferotemporal
cortex, and the hippocampus in both active conditions, when compared with
rest. These decreases were significantly greater during new learning. We
draw three main conclusions. (1) The cerebellum is involved in the process
by which motor tasks become automatic, whereas the putamen is equally
activated by sequence learning and retrieval, and may play a similar role
in both. (2) When subjects learn new sequences of motor actions, prefrontal
cortex is activated. This may reflect the need to generate new responses.
(3) Reduced activity of areas concerned with visual processing,
particularly during new learning, suggests that selective attention may
involve depressing the activity of cells in modalities that are not engaged
by the task.
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|
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|
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|
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|
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|
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|
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|
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|
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|
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|
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[Abstract]
[Full Text]
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|
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|

|
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|
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|
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|
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|
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[Abstract]
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|
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|
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|
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[PDF]
|
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|
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[Abstract]
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|
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|
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|
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|
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|
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|
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|
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|
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|
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|
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|
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