Orbitofrontal cortex as a cognitive map of task states

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Project summary: The orbitofrontal cortex as a cognitive map of task states The orbitofrontal cortex (OFC) has remained one of the most mysterious areas in the prefrontal cortex, with suggested functions ranging from inhibition of prepotent actions to valuation in economic decision making. OFC dysfunction is implicated in a wide range of decision-related disorders, chief among them compulsive disorders such as addiction and OCD. Recently, we hypothesized that the OFC represents the current state of the task within a “cognitive map” of task space, providing a summary of task-relevant information to decision-making and learning areas elsewhere in the brain (Wilson et al., 2014, Neuron). In particular, theoretical considerations and previous empirical data suggest that the OFC is especially important for representing task states that are “partially observable”—states that include information that is not directly available in the environment, such as internal information from working memory. This hypothesis offers a unifying theoretical framework for interpreting a wide variety of existing findings, and has already gained considerable traction in the field (e.g., the paper has been cited over 50 times and was mentioned in over half the talks in a recent conference on the OFC). However, the theory has not yet been tested directly, as previous data can also be explained by alternative interpretations. Here we propose to test the hypothesis that the OFC represents task states, and to contrast and differentiate this function from the dominant competing hypothesis according to which the OFC represents reward expectancies. In Aim1, we will test whether the OFC codes the states of an age-judgment task that requires encoding of unobservable information as a critical part of the task state, and that does not involve rewards. We will use fMRI to measure OFC activity in humans, and utilize multivariate analysis methods to test whether the task states can be decoded in OFC, and whether this state representation correlates with and predicts task performance. In Aim 2, we will differentiate the state coding and value coding functions of the OFC by adding rewards to the age-judgment task and testing whether rewards are decodable in OFC when they are instrumental to task performance versus incidental to task performance. Our theory predicts that rewards will be represented in OFC only if they are required as part of the task state. Throughout, we will also analyze representations in related brain areas such as the dorsolateral prefrontal cortex, the hippocampus and high-level visual cortices, to determine the unique function of the OFC, and to establish the relationship between task states in the OFC and task-relevant information encoded elsewhere in the brain. Our findings will impact on the current understanding of the role of OFC in both normal and aberrant learning and decision making, and will help explain why the OFC is important for some tasks but not others. Moreover, our work will establish the utility of decoding internal task states from non-invasive brain imaging data for predicting behavior and for analyzing individual differences in task representations. This is especially relevant to understanding the precise nature of decision-making deficiencies in disorders such as substance abuse and other compulsive disorders where the OFC is strongly implicated.