IMPORTANCE OF UNPREDICTABILITY FOR REWARD RESPONSES IN PRIMATE DOPAMINE NEURONS

1. We used single neuron recording techniques in two behaving monkeys to investigate the conditions in which dopamine neurons respond to pri mary rewarding or potentially rewarding stimuli. Animals received drop s of liquid either outside behavioral tasks or as rewards during learn ing or established performance of an auditory reaction time task. 2. T hree quarters of dopamine neurons showed a short-latency, phasic respo nse to liquid that was delivered outside the task without being predic ted by phasic stimuli. The same neurons responded to liquid reward dur ing learning but not when task performance was established, at which t ime the neuronal response occurred to the conditioned, reward-predicti ng, movement-triggering stimulus. 3. These data suggest that the respo nses of dopamine neurons to rewarding or potentially rewarding liquid are due to the temporally unpredicted stimulus occurrence. A known, re ward-predicting, tonic context does not prevent dopamine neurons from responding to the rewarding liquid. The responses during learning appa rently occur because reward is not yet reliably predicted by a conditi oned phasic stimulus. Because the unpredicted occurrence of reward is of central importance for learning, these responses allow dopamine neu rons to play an important role in reward-driven learning.