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The Journal of Neurophysiology Vol. 82 No. 2 August 1999, pp. 978-998
Copyright ©1999 by the American Physiological Society
1Faculty of Health and Sport Sciences, Osaka University, Toyonaka, Osaka 560-0043, Japan; and 2Department of Brain and Cognitive Sciences, MIT, Cambridge, Massachusetts 02139
Matsumoto, Naoyuki,
Toru Hanakawa,
Shinichiro Maki,
Ann M. Graybiel, and
Minoru Kimura.
Nigrostriatal Dopamine System in Learning to Perform Sequential
Motor Tasks in a Predictive Manner. J. Neurophysiol. 82: 978-998, 1999. Neurons in the primate
striatum and the substantia nigra pars compacta change their firing
patterns during sensory-motor learning. To study the
consequences of nigrostriatal dopamine depletion for learning and
memory of motor sequences, we used a neurotoxin, 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP), to deplete dopamine unilaterally in the striatum of macaque monkeys either before
or after training them on sequential push-button motor tasks. We
compared the monkeys' performance with the arms ipsilateral and
contralateral to dopamine depletion. During training and retraining on
the tasks, we measured initial and serial movement times and reaction
times for the push button movements, electromyographic patterns of arm
and orofacial muscle activity during button pushing and reward licking,
and saccadic eye movements during the button push sequences. With the
arm ipsilateral to the side of dopamine depletion, each monkey showed
progressive shortening of movement times and initial and serial
reaction times, and each developed consistent strategies of
hand-orofacial and hand-eye coordination in which single button push
movements were linked efficiently to succeeding movements so that
performance of the whole sequence became predictive. These patterns did
not develop for contralateral arm performance in this monkey treated
with MPTP before training. With the arm contralateral to dopamine
depletion, the monkey showed significant quantitative deficits in all
parameters measured except initial reaction times. Movement times and
serial reaction times were longer than those for the ipsilateral arm;
anticipatory saccadic eye movements were not well time-locked to
individual button pushes made with the contralateral hand; and push and
licking movements were not smoothly coordinated. This monkey further
showed striking differences in performance when using the ipsilateral
and contralateral arms in switch trial tests in which reward was
delivered unexpectedly one button early. He continued to make movements
to the previously rewarded button with the ipsilateral arm but showed
no such automatic movements when he used his contralateral arm. For the
monkey treated with MPTP after training, performance on the push-button
task was skilled for both arms before dopamine depletion, but the
unilateral dopamine depletion produced deficits in contralateral arm
performance for all parameters measured, again excepting initial
reaction times. With retraining, however, his performance with the
contralateral arm improved. We conclude that the striatum and its
nigrostriatal afferents function in the initial learning underlying
performance of sequences of movements as single motor programs. The
nigrostriatal system also operates during the retrieval of these
programs once learning is accomplished, but lesions of the
nigrostriatal system spare the ability to relearn the previously
acquired programs.
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