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The Journal of Neuroscience, September 17, 2003, 23(24):8489-8497

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Responses of Tonically Active Neurons in the Monkey Striatum Discriminate between Motivationally Opposing Stimuli

Sabrina Ravel, Eric Legallet, and Paul Apicella

Institut de Neurosciences Physiologiques et Cognitives, Centre National de la Recherche Scientifique, 13402 Marseille cedex 20, France

The striatum is involved in the control of appetitively motivated behavior. We found previously that tonically active neurons (TANs) in the monkey striatum show discriminative responses to different stimuli that are appetitive or aversive. However, these differential responses may reflect the sensory qualities of the stimulus rather than its motivational value. In the present study, we sought to define more precisely the relationship between the particular aspect of the response of TANs and the motivational value of stimuli. For this purpose, three monkeys were presented with two types of aversive stimuli (loud sound and air puff) and one appetitive stimulus (fruit juice). In most instances, the TAN responses to the loud sound and the air puff were similar, in terms of response pattern and duration, whereas responses to the liquid reward showed distinct features. Using classical appetitive conditioning, we reversed the motivational value of a stimulus so that a previously aversive stimulus was now associatively paired with a reward and found that this manipulation selectively modifies the expression of TAN responses to the stimulus. These data indicate that the characteristics of neuronal responses undergo modifications when the valence of the stimulus is changed from aversive to appetitive during associative learning, suggesting that TANs may contribute to a form of stimulus encoding that is dependent on motivational attributes. The adaptation of TAN responses such as observed in the present study likewise reflects a neuronal system that adjusts to the motivational information about environmental events.

Key words: striatum; basal ganglia; TANs; motivation; learning; monkey

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Received May 9, 2003; revised July 15, 2003; accepted July 18, 2003.

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