Responses of tonically discharging neurons in the monkey striatum to primary rewards delivered during different behavioral states

Abstract

In the primate striatum, the tonically discharging neurons respond to conditioned stimuli associated with reward. We investigated whether these neurons respond to the reward itself and how changes in the behavioral context in which the reward is delivered might influence their responsiveness. A total of 286 neurons in the caudate nucleus and putamen were studied in two awake macaque monkeys while liquid reward was delivered 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 delivered 1 s after a visual signal; (3) a free reward situation, in which reward was delivered at irregular time intervals outside of any conditioning 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 situations (n = 78), 24% responded to reward regardless of the situation and 65% in only one or two situations. Responses selective for one particular situation occurred exclusively in the free reward situation. When the reward was delivered immediately after the visual signal in the classically 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 delivered later than 1 s after the visual signal. This is the first report that tonic striatal neurons might display responses directly to primary rewards. The neuronal responses were strongly influenced by the behavioral context in which the animals received the reward. An important factor appears to be the timing of reward. These neurons might therefore contribute to a general aspect of behavioral reactivity of the subject to relevant stimuli.

Differential involvement of M1-type and M4-type muscarinic cholinergic receptors in the dorsomedial striatum in task switching

“…Moreover, Apicella and colleagues (1991) found that the activity of TANs within the striatum changed during a delayed go/no-go task that demands flexible responding for goal-directed behavior. TANs also exhibited changes in activity when either the timing of a predictive cue is changed or the timing of reward delivery (Apicella, Legallet & Trouche, 1997;Ravel et al, 2001). This change in TANs activity with a switch in conditions may facilitate one's ability to adapt to changing environmental conditions in order to achieve a goal.…”

The Role of Striatal Tonically Active Neurons in Reward Prediction Error Signaling during Instrumental Task Performance

“…The task relationships of neuronal discharges were assessed on-line in the form of rasters aligned on each task event. We used well established criteria to identify TANs (Aosaki et al, 1994;Apicella et al, 1997). Every TAN isolated was examined while the monkey performed the task with reward at p ϭ 1.0.…”

“…We evaluated TAN responsiveness to task events in terms of changes in firing detected on the basis of a Wilcoxon signed-rank test (Apicella et al, 1997) and only neurons with statistically significant changes against control activity were considered responsive. The baseline activity was calculated during the 0.5 s before the presentation of the trigger stimulus.…”

The Role of Acetylcholine in Cocaine Addiction

“…Specifically, these interneurons appear highly responsive to stimulus detection, movement control, and context recognition. Thus, while TANs are somewhat responsive to the experience of rewards, they exhibit a significantly greater response to contextual features (cues) associated with the reward (Aosaki et al, 1994;Apicella et al, 1997;Kimura et al, 2003). This feature distinguishes the TANs from mesostriatal DANs, which are equally responsive to both rewards and their associated cues.…”