Summary How do we choose between goods that have different subjective values, like apples and oranges? Neuroeconomics proposes that this is done by reducing complex goods to a single unitary value to allow comparison. This value is computed ‘on the fly’ from the underlying model of the goods space, allowing decisions to meet current needs. Such behavior is termed ‘model-based’ to distinguish it from pre-determined, habitual or ‘model-free’ behavior. The lateral orbitofrontal cortex (OFC) supports model-based behavior in rats and primates, but it is less clear whether it is necessary for economic choice. Here we tested this question by optogenetically inactivating lateral OFC in rats in a classic model-based task and also during economic choice. Contrary to predictions, inactivation disrupted model-based behavior without affecting economic choice.

The lateral orbitofrontal cortex (lOFC) has been described as signaling either outcome expectancies or value. Previously, we used unblocking to show that lOFC neurons respond to a predictive cue signaling a ‘valueless’ change in outcome features (McDannald, 2014). However, many lOFC neurons also fired to a cue that simply signaled more reward. Here, we recorded lOFC neurons in a variant of this task in which rats learned about cues that signaled either more (upshift), less (downshift) or the same (blocked) amount of reward. We found that neurons acquired responses specifically to one of the three cues and did not fire to the other two. These results show that, at least early in learning, lOFC neurons fire to valued cues in a way that is more consistent with signaling of the predicted outcome’s features than with signaling of a general, abstract or cached value that is independent of the outcome.DOI: http://dx.doi.org/10.7554/eLife.11299.001

How are decisions made between different goods? One theory spanning several fields of neuroscience proposes that their values are distilled to a single common neural currency, the calculation of which allows for rational decisions. The orbitofrontal cortex (OFC) is thought to play a critical role in this process, based on the presence of neural correlates of economic value in lateral OFC in monkeys and medial OFC in humans. We previously inactivated lateral OFC in rats without affecting economic choice behavior. Here we inactivated medial OFC in the same task, again without effect. Behavior in the same rats was disrupted by inactivation during progressive ratio responding previously shown to depend on medial OFC, demonstrating the efficacy of the inactivation. These results indicate that medial OFC is not necessary for economic choice, bolstering the proposal that classic economic choice is likely mediated by multiple, overlapping neural circuits.

The orbitofrontal cortex (OFC) has long been implicated in the ability to use the current value of expected outcomes to guide behavior. More recently this specific role has been conceptualized as a special case of a more general function that OFC plays in constructing a “cognitive map” of the behavioral task space by labeling the current task state and learning relationships among task states. Here, we have used single unit recording data from two prior studies to examine whether and how information relating different states within and across trials is represented in medial versus lateral OFC in rats. Using a hierarchical clustering analysis, we examined how neurons from each area represented information about differently valued trial types, defined by the cue-outcome pairings, versus how those same neurons represented information about similar epochs between these different trial types, such as the stimulus sample, delay, and reward consumption epochs. This analysis revealed that ensembles in lOFC group states according to trial epoch, whereas those in mOFC organize the same states by trial type. These results suggest that lOFC and mOFC construct cognitive maps that emphasize different features of the behavioral landscape, with lOFC tracking events based on local similarities, irrespective of their values, and mOFC tracking more distal or higher order relationships relevant to value.

The orbitofrontal cortex (OFC) has been broadly implicated in the ability to use the current value of expected outcomes to guide behavior. Although value correlates have been prominently reported in lateral OFC, they are more often associated with more medial areas. Further, recent studies in primates have suggested a dissociation in which the lateral OFC is involved in credit assignment and representation of reward identity and more medial areas are critical to representing value. Previously, we used unblocking to test more specifically what information about outcomes is represented by OFC neurons in rats; consistent with the proposed dichotomy between the lateral and medial OFC, we found relatively little linear value coding in the lateral OFC (Lopatina et al., 2015). Here we have repeated this experiment, recording in the medial OFC, to test whether such value signals might be found there. Neurons were recorded in an unblocking task as rats learned about cues that signaled either more, less, or the same amount of reward. We found that medial OFC neurons acquired responses to these cues; however, these responses did not signal different reward values across cues. Surprisingly, we found that cells developed responses to cues predicting a change, particularly a decrease, in reward value. This is consistent with a special role for medial OFC in representing current value to support devaluation/revaluation sensitive changes in behavior.