Abstract
An impressive array of neural processing appears to be dedicated to the extraction of reward-related information from environmental stimuli and use of this information in the generation of goal-directed behaviors. While other structures are certainly involved in these processes, the characteristics of activations seen in mesencephalic dopamine neurons, striatal neurons and neurons of the orbitofrontal cortex provide distinct examples of the different ways in which reward-related information is processed. In addition, the differences in activations seen in these three regions demonstrate the different roles they may play in goal-directed behavior. A principal role played by dopamine neurons is that of a detector of an error in reward prediction. The homogeneity of responsiveness across the population of dopamine neurons indicates that this error signal is widely broadcast to dopamine terminal regions where it could provide a teaching signal for synaptic modifications underlying the learning of goal-directed appetitive behaviors. The responses of these same neurons to conditioned stimuli associated with reward could also serve as a signal of prediction error useful for the learning of sequences of environmental stimuli leading to reward. Dopamine neuron responses to both rewards and conditioned stimuli are not contingent on the behavior executed to obtain the reward and thus appear to reflect a relatively pure signal of a reward prediction error. It is not yet clear whether these activations, and responses to novel stimuli, have an additional function in engaging neural systems involved in the representation and execution of goal-directed behaviors. This representation of goal-directed behaviors may involve the striatal regions studied, where processing of reward-related information appears to be much more heterogeneous. Different subpopulations of striatal neurons are activated at different stages in the course of goal-directed behaviors, with largely separate populations activated following presentation of conditioned stimuli, preceding reinforcers, and following reinforcers. Neurons exhibiting each of these types of activation appear to differentiate between rewarding and non-rewarding outcomes of behavioral acts and, as a population, appear to be biased towards processing reward vs. non-reward. These activations observed in the striatum were often contingent on the behavioral act associated with obtaining reward, reflecting an integration of information not observed in dopamine neurons. Another difference between reward processing in striatal neurons and dopamine neurons is the influence of predictability on neuronal responsiveness. Unlike dopamine neurons, many striatal neurons respond to predicted rewards, although at least some may reflect the relative degree of predictability in the magnitude of the responses to reward. Thus, striatal processing of reward-related information is in some ways more complex than that observed in dopamine neurons, incorporating information on behavior and potentially providing more detailed information regarding predictability. These activations could serve as a component of the neural representation of the goal, and/or the behavioral aspects of goal-directed behaviors. As such they would be of use for the execution of appropriate goal-directed behaviors in response to known environmental stimuli, as well as for generating behaviors in response to novel stimuli that may be associated with desirable goals. Neuronal activations in the orbitofrontal cortex appear to involve less integration of behavioral and reward-related information, but rather incorporate another aspect of reward, the relative motivational significance of different rewards. These activations would serve a function similar to those striatal neurons that encode exclusively reward-related information in situations in which only a single outcome is obtainable. (ABSTRACT TRUNCATED)
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