RESPONSES OF TONICALLY DISCHARGING NEURONS IN THE MONKEY STRIATUM TO PRIMARY REWARDS DELIVERED DURING DIFFERENT BEHAVIORAL STATES

In the primate striatum, the tonically discharging neurons respond to conditioned stimuli associated with reward. We investigated whether th ese neurons respond tcr the reward itself and how changes in the behav ioral context in which the reward is delivered might influence their r esponsiveness. A total of 286 neurons in the caudate nucleus and putam en were studied in two awake macaque monkeys while liquid reward was d elivered in three behavioral situations: (1) an instrumental task, in which reward was delivered upon execution of a visually triggered arm movement; (2) a classically conditioned task, in which reward was deli vered 1 s after a visual signal; (3) a free reward situation, in which reward was delivered at irregular time intervals outside of any condi tioning task. The monkeys' uncertainty about the time at which reward will be delivered was assessed by monitoring their-mouth movements. A larger proportion of neurons responsive to reward was observed in the free reward situation (86%) than in the classically conditioned (57%) and instrumental tasks (37%). Among the neurons tested in all situatio ns (n = 78), 24% responded to reward regardless of the situation and 6 5% in only one or two situations. Responses selective for one particul ar situation occurred exclusively in tile free reward situation. When the reward was delivered immediately after the visual signal in the cl assically conditioned task, most of the neurons reduced or completely lost their responses to reward, and other neurons remained responsive. Conversely, neuronal responses invariably persisted when reward was d elivered later than 1 s after the visual signal. This is the first rep ort that tonic striatal neurons might display responses directly to pr imary rewards. The neuronal responses were strongly influenced by the behavioral context in which the animals received the reward. An import ant factor appears to be the timing of reward. These neurons might the refore contribute to a general aspect of behavioral reactivity of the subject to relevant stimuli.