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Journal of Neuroscience, Vol 13, 900-913, Copyright © 1993 by Society for Neuroscience
Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task
W Schultz, P Apicella and T Ljungberg
Institut de Physiologie, Universite de Fribourg, Switzerland.
The present investigation had two aims: (1) to study responses of dopamine
neurons to stimuli with attentional and motivational significance during
several steps of learning a behavioral task, and (2) to study the activity
of dopamine neurons during the performance of cognitive tasks known to be
impaired after lesions of these neurons. Monkeys that had previously
learned a simple reaction time task were trained to perform a spatial
delayed response task via two intermediate tasks. During the learning of
each new task, a total of 25% of 76 dopamine neurons showed phasic
responses to the delivery of primary liquid reward, whereas only 9% of 163
neurons responded to this event once task performance was established. This
produced an average population response during but not after learning of
each task. Reward responses during learning were significantly more
numerous and pronounced in area A10, as compared to areas A8 and A9.
Dopamine neurons also showed phasic responses to the two conditioned
stimuli. These were the instruction cue, which was the first stimulus in
each trial and indicated the target of the upcoming arm movement (58% of 76
neurons during and 44% of 163 neurons after learning), and the trigger
stimulus, which was a conditioned incentive stimulus predicting reward and
eliciting a saccadic eye movement and an arm reaching movement (38% of
neurons during and 40% after learning). None of the dopamine neurons showed
sustained activity in the delay between the instruction and trigger stimuli
that would resemble the activity of neurons in dopamine terminal areas,
such as the striatum and frontal cortex. Thus, dopamine neurons respond
phasically to alerting external stimuli with behavioral significance whose
detection is crucial for learning and performing delayed response tasks.
The lack of sustained activity suggests that dopamine neurons do not encode
representational processes, such as working memory, expectation of external
stimuli or reward, or preparation of movement. Rather, dopamine neurons are
involved with transient changes of impulse activity in basic attentional
and motivational processes underlying learning and cognitive behavior.
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|
|
|
|
|
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|
|
|
|
|
|
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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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|
|
|
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[Full Text]
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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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2793 - 2798.
[Abstract]
[Full Text]
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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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[Abstract]
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|
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80(3):
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3874 - 3883.
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[PDF]
|
|
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|
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83(5):
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[Full Text]
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|
|
|
|
|
|
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83(4):
1864 - 1876.
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[Full Text]
[PDF]
|
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