Dopamine, learning and motivation

REVIEWS

DOPAMINE, LEARNING AND MOTIVATION

Roy A. Wise

The hypothesis that dopamine is important for reward has been proposed in a number of forms, each of which has been challenged. Normally, rewarding stimuli such as food, water, lateral hypothalamic brain stimulation and several drugs of abuse become ineffective as rewards in animals given performance-sparing doses of dopamine antagonists. Dopamine release in the nucleus accumbens has been linked to the efficacy of these unconditioned rewards, but dopamine release in a broader range of structures is implicated in the stamping-in of memory that attaches motivational importance to otherwise neutral environmental stimuli.

The neurotransmitter dopamine particularly nigrostriatal dopamine (BOX 1) has long been identified with motor function1.However, moderate doses of

NEUROLEPTIC drugs (dopamine antagonists) attenuate the motivation to act before they compromise the ability to act. Such drugs do not immediately compromise the initiation of well-learned response habits213 or even

consummatory behaviour14.Rather, initiation of habitual responding declines progressively sometimes over minutes3,4 and sometimes over days5,14 in neuroleptictreated animals12,14. Therefore, dopamine has come

to be identified with motivational1517 as well as motor function.

Different versions of the hypothesis that dopamine is important for the normal effectiveness of rewarding stimuli have been challenged on various grounds. In this review, I first identify several versions of the hypothesis, indicating which have been falsified and which remain viable. I then differentiate between the largely conditioned motivation that precedes and guides an instrumental act, and the REINFORCEMENT of

stimulusREWARD and responsereward associations that follows the receipt of reward. This separation of what comes before and what comes after reward contact leads not only to a better appreciation of the role of dopamine in immediate motivation, but also to an appreciation of its role in the learning and memory consolidation functions that establish the motivational foundation of most goal-directed behaviour.

Multiple dopamine hypotheses

Dopamine was first identified with motivational function on the strength of Ungerstedts18 report that feeding and drinking deficits that are similar to those caused by lesions of the lateral hypothalamus can be induced by selective damage to the dopamine fibres that traverse this region. Damage to the nigrostriatal dopamine fibres causes feeding and drinking deficits19,20,whereas selective damage to the mesolimbic dopamine fibres decreases the forward locomotion21 that is common to most...