Neuronal activity in monkey ventral striatum related to the expectation of reward

Abstract

Projections from cortical and subcortical limbic structures to the basal ganglia are predominantly directed to the ventral striatum. The present study investigated how the expectation of external events with behavioral significance is reflected in the activity of ventral striatal neurons. A total of 420 neurons were studied in macaque monkeys performing in a delayed go-no-go task. Lights of different colors instructed the animal to do an arm-reaching movement or refrain from moving, respectively, when a trigger light was illuminated a few seconds later. Task performance was reinforced by liquid reward in both situations. A total of 60 ventral striatal neurons showed sustained increases of activity before the occurrence of individual task events. In 43 of these neurons, activations specifically preceded the delivery of reward, independent of the movement or no-movement reaction. In a series of additional tests, these activations were time locked to the subsequent reward, disappeared within a few trials when reward was omitted, and were temporally unrelated to mouth movements. Changes in the appetitive value of the reward liquid modified the magnitude of activations, suggesting a possible relationship to the hedonic properties of the expected event. Activations also occurred when reward was delivered in a predictable manner outside of any behavioral task. These data suggest that neurons in the ventral striatum are activated during states of expectation of individual environmental events that are predictable to the subject through its past experience. The prevalence of activations related to the expectation of reward suggests that ventral striatal neurons have access to central representations of reward and thereby participate in the processing of information underlying the motivational control of goal-directed behavior.

Nucleus accumbens lesions decrease sensitivity to rapid changes in the delay to reinforcement

“…Numerous electrophysiological and imaging studies on rodents, humans and non-human primates have implicated the NACas part of a neural circuit responsible for predicting delayed rewards [14][15][16][17][18][19][20][21][22][23][24][25][26]. The results of the present study provide strong behavioral evidence that the NAC is an essential part of this reward prediction circuit.…”

“…However, these findings were complicated by the observation that lesioned rats had a low preference for the "large" reward even when there was no delay, suggesting that the lesions generally impaired choice behavior rather than directly affecting delay discounting. Because the NAC is part of a circuit involved in predicting the occurrence of delayed rewards [14][15][16][17][18][19][20][21][22][23][24][25][26], it is possible that the lesioned rats in the Cardinal study were less able to track the within session changes in the delay associated with the large reinforcer and generally avoided this option without affecting delay discounting.…”

Differential Brain Activity in Alcoholics and Social Drinkers to Alcohol Cues: Relationship to Craving

“…Both regions have been implicated in the rewarding properties of reinforcing behaviors and substances, and have extensive cortical and subcortical connections. In animals, dopaminergic projections from the ventral tegmental area to the nucleus accumbens fire in response to presentation of reward cues and reward anticipation (Berridge and Robinson, 1998;Ikemoto and Panksepp, 1999;Schultz et al, 1992). A recent fMRI study in humans found that anticipation of increasing monetary rewards in healthy volunteers yielded increasing nucleus accumbens activation (Knutson et al, 2001).…”

Dopamine gating of glutamatergic sensorimotor and incentive motivational input signals to the striatum

“…Reward-related neurons are found in both the dorsal and ventral striatum, but they are more frequently found in the ventral striatum [7]. These cells respond to both the anticipation [55,104] and presentation of reward stimuli [7,16,55], and show activity levels that reflects the appetitive value of the reward [7,104]. The striatum also contains cells responsive to aversive stimuli [122,126].…”