In order to achieve a goal, one procures immediately available rewards, escape from aversive events or endures absence of rewards. The neuronal substrate for these goal-directed actions includes the limbic system and the basal ganglia. In the basal ganglia, classes of projection neurons in the striatum show activity with motivational as well as sensorimotor properties, such as expectation of reward and task schedule for obtaining reward. Tonically active neurons (TANs), presumed cholinergic interneurons in the striatum, respond to reward-associated stimuli, evolve their activity through learning and respond also to aversive event-associated stimuli such as airpuff on the face. A recent study showed that responses to visual cues are less selective to whether the cue instructs reward or no reward. To address this paradox, we asked macaque monkeys to perform a set of visual reaction time tasks while expecting the reward, aversive event or absence of reward. We found that TANs respond to instruction stimuli associated with motivational outcomes but not to unassociated ones, and that they mostly differentiate associated instructions. We also found that the higher percentage of TANs in the caudate nucleus respond to stimuli associated with motivational outcomes than in the putamen, whereas the higher percentage of TANs in the putamen respond to GO signals than in the caudate nucleus especially for an action anticipating a reward. These findings suggest a distinct, pivotal role played by TANs in the caudate nucleus and putamen in encoding instructed motivational contexts for goal-directed action selection and learning in the striatum.