Single-cell and population coding of expected reward probability in the orbitofrontal cortex of the rat.

The orbitofrontal cortex (OFC) has been implicated in decision-making under uncertainty, but it is unknown how information about the probability or uncertainty of future reward is coded by single orbitofrontal neurons and ensembles. We recorded neuronal ensembles in rat OFC during an olfactory discrimination task in which different odor stimuli predicted different reward probabilities. Single-unit firing patterns correlated to the expected reward probability primarily within an immobile waiting period before reward delivery but also when the rat executed movements toward the reward site. During these pre-reward periods, a subset of OFC neurons was sensitive to differences in probability but only very rarely discriminated on the basis of reward uncertainty. In the reward period, neurons responded during presentation or omission of reward or during both types of outcome. At the population level, neurons were characterized by a wide divergence in firing-rate variability attributable to expected probability. A population analysis using template matching as reconstruction method indicated that OFC generates a distributed representation of reward probability with a weak dependence on neuronal group size. The analysis furthermore confirmed that predictive information coded by OFC populations was quantitatively related to reward probability, but not to uncertainty.

Population coding of reward magnitude in the orbitofrontal cortex of the rat.

Although single-cell coding of reward-related information in the orbitofrontal cortex (OFC) has been characterized to some extent, much less is known about the coding properties of orbitofrontal ensembles. We examined population coding of reward magnitude by performing ensemble recordings in rat OFC while animals learned an olfactory discrimination task in which various reinforcers were associated with predictive odor stimuli. Ensemble activity was found to represent information about reward magnitude during several trial phases, namely when animals moved to the reward site, anticipated reward during an immobile period, and received it. During the anticipation phase, Bayesian and template-matching reconstruction algorithms decoded reward size correctly from the population activity significantly above chance level (highest value of 43 and 48%, respectively; chance level, 33.3%), whereas decoding performance for the reward delivery phase was 76 and 79%, respectively. In the anticipation phase, the decoding score was only weakly dependent on the size of the neuronal group participating in reconstruction, consistent with a redundant, distributed representation of reward information. In contrast, decoding was specific for temporal segments within the structure of a trial. Decoding performance steeply increased across the first few trials for every rewarded odor, an effect that could not be explained by a nonspecific drift in response strength across trials. Finally, when population responses to a negative reinforcer (quinine) were compared with sucrose reinforcement, coding in the delivery phase appeared to be related to reward quality, and thus was not based on ingested liquid volume.

Neural coding of reward magnitude in the orbitofrontal cortex of the rat during a five-odor olfactory discrimination task.

The orbitofrontal cortex (OBFc) has been suggested to code the motivational value of environmental stimuli and to use this information for the flexible guidance of goal-directed behavior. To examine whether information regarding reward prediction is quantitatively represented in the rat OBFc, neural activity was recorded during an olfactory discrimination "go"/"no-go" task in which five different odor stimuli were predictive for various amounts of reward or an aversive reinforcer. Neural correlates related to both actual and expected reward magnitude were observed. Responses related to reward expectation occurred during the execution of the behavioral response toward the reward site and within a waiting period prior to reinforcement delivery. About one-half of these neurons demonstrated differential firing toward the different reward sizes. These data provide new and strong evidence that reward expectancy, regardless of reward magnitude, is coded by neurons of the rat OBFc, and are indicative for representation of quantitative information concerning expected reward. Moreover, neural correlates of reward expectancy appear to be distributed across both motor and nonmotor phases of the task.