Orbitofrontal Cortex Representations Research Articles

The hippocampus and orbitofrontal cortex jointly represent task structure during memory-guided decision making.

SUMMARYThe hippocampus, well known for its role in episodic memory, might also be an important brain region for extracting structure from our experiences in order to guide future decisions. Recent evidence in rodents suggests that the hippocampus supports decision making by representing task structure in cooperation with the orbitofrontal cortex (OFC). Here, we examine how the human hippocampus and OFC represent task structure during an associative learning task that required learning of both context-determined and context-invariant probabilistic associations. We find that after learning, hippocampal and lateral OFC representations differentiated between context-determined and context-invariant task structures. The degree of this differentiation within the hippocampus and lateral OFC is highly correlated. These results advance our understanding of the hippocampus and suggest that the hippocampus and OFC support goal-directed behavior by representing information that guides the selection of appropriate decision strategies.

Orbitofrontal State Representations Are Related to Choice Adaptations and Reward Predictions.

Animals can categorize the environment into "states," defined by unique sets of available action-outcome contingencies in different contexts. Doing so helps them choose appropriate actions and make accurate outcome predictions when in each given state. State maps have been hypothesized to be held in the orbitofrontal cortex (OFC), an area implicated in decision-making and encoding information about outcome predictions. Here we recorded neural activity in OFC in 6 male rats to test state representations. Rats were trained on an odor-guided choice task consisting of five trial blocks containing distinct sets of action-outcome contingencies, constituting states, with unsignaled transitions between them. OFC neural ensembles were analyzed using decoding algorithms. Results indicate that the vast majority of OFC neurons contributed to representations of the current state at any point in time, independent of odor cues and reward delivery, even at the level of individual neurons. Across state transitions, these representations gradually integrated evidence for the new state; the rate at which this integration happened in the prechoice part of the trial was related to how quickly the rats' choices adapted to the new state. Finally, OFC representations of outcome predictions, often thought to be the primary function of OFC, were dependent on the accuracy of OFC state representations.SIGNIFICANCE STATEMENT A prominent hypothesis proposes that orbitofrontal cortex (OFC) tracks current location in a "cognitive map" of state space. Here we tested this idea in detail by analyzing neural activity recorded in OFC of rats performing a task consisting of a series of states, each defined by a set of available action-outcome contingencies. Results show that most OFC neurons contribute to state representations and that these representations are related to the rats' decision-making and OFC reward predictions. These findings suggest new interpretations of emotional dysregulation in pathologies, such as addiction, which have long been known to be related to OFC dysfunction.

Value and choice as separable and stable representations in orbitofrontal cortex

Value-based decision-making requires different variables—including offer value, choice, expected outcome, and recent history—at different times in the decision process. Orbitofrontal cortex (OFC) is implicated in value-based decision-making, but it is unclear how downstream circuits read out complex OFC responses into separate representations of the relevant variables to support distinct functions at specific times. We recorded from single OFC neurons while macaque monkeys made cost-benefit decisions. Using a novel analysis, we find separable neural dimensions that selectively represent the value, choice, and expected reward of the present and previous offers. The representations are generally stable during periods of behavioral relevance, then transition abruptly at key task events and between trials. Applying new statistical methods, we show that the sensitivity, specificity and stability of the representations are greater than expected from the population’s low-level features—dimensionality and temporal smoothness—alone. The separability and stability suggest a mechanism—linear summation over static synaptic weights—by which downstream circuits can select for specific variables at specific times.

Targeted Stimulation of Human Orbitofrontal Networks Disrupts Outcome-Guided Behavior.

Outcome-guided behavior requires knowledge about the current value of expected outcomes. Such behavior can be isolated in the reinforcer devaluation task, which assesses the ability to infer the current value of specific rewards after devaluation. Animal lesion studies demonstrate that orbitofrontal cortex (OFC) is necessary for normal behavior in this task, but a causal role for human OFC in outcome-guided behavior has not been established. Here, we used sham-controlled, non-invasive, continuous theta-burst stimulation (cTBS) to temporarily disrupt human OFC network activity by stimulating a site in the lateral prefrontal cortex that is strongly connected to OFC prior to devaluation of food odor rewards. Subjects in the sham group appropriately avoided Pavlovian cues associated with devalued food odors. However, subjects in the stimulation group persistently chose those cues, even though devaluation of food odors themselves was unaffected by cTBS. This behavioral impairment was mirrored in changes in resting-state functional magnetic resonance imaging (rs-fMRI) activity such that subjects in the stimulation group exhibited reduced OFC network connectivity after cTBS, and the magnitude of this reduction was correlated with choices after devaluation. These findings demonstrate the feasibility of indirectly targeting the human OFC with non-invasive cTBS and indicate that OFC is specifically required for inferring the value of expected outcomes.

Decision Making: How Is Information Represented in Orbitofrontal Cortex?

Classically, specific orbitofrontal cortex (OFC) neurons are thought to represent attributes of specific decision options. A new model proposes instead that OFC neurons represent whichever option is currently attended. A recent study, however, tests these two models and rules out the 'current-focus-of-attention' model.

Identity-Specific Reward Representations in Orbitofrontal Cortex Are Modulated by Selective Devaluation.

Goal-directed behavior is sensitive to the current value of expected outcomes. This requires independent representations of specific rewards, which have been linked to orbitofrontal cortex (OFC) function. However, the mechanisms by which the human brain updates specific goals on the fly, and translates those updates into choices, have remained unknown. Here we implemented selective devaluation of appetizing food odors in combination with pattern-based neuroimaging and a decision-making task. We found that in a hungry state, participants chose to smell high-intensity versions of two value-matched food odor rewards. After eating a meal corresponding to one of the two odors, participants switched choices toward the low intensity of the sated odor but continued to choose the high intensity of the nonsated odor. This sensory-specific behavioral effect was mirrored by pattern-based changes in fMRI signal in lateral posterior OFC, where specific reward identity representations were altered after the meal for the sated food odor but retained for the nonsated counterpart. In addition, changes in functional connectivity between the OFC and general value coding in ventromedial prefrontal cortex (vmPFC) predicted individual differences in satiety-related choice behavior. These findings demonstrate how flexible representations of specific rewards in the OFC are updated by devaluation, and how functional connections to vmPFC reflect the current value of outcomes and guide goal-directed behavior.SIGNIFICANCE STATEMENT The orbitofrontal cortex (OFC) is critical for goal-directed behavior. A recent proposal is that OFC fulfills this function by representing a variety of state and task variables ("cognitive maps"), including a conjunction of expected reward identity and value. Here we tested how identity-specific representations of food odor reward are updated by satiety. We found that fMRI pattern-based signatures of reward identity in lateral posterior OFC were modulated after selective devaluation, and that connectivity between this region and general value coding ventromedial prefrontal cortex (vmPFC) predicted choice behavior. These results provide evidence for a mechanism by which devaluation modulates a cognitive map of expected reward in OFC and thereby alters general value signals in vmPFC to guide goal-directed behavior.

Identity-specific coding of future rewards in the human orbitofrontal cortex

Nervous systems must encode information about the identity of expected outcomes to make adaptive decisions. However, the neural mechanisms underlying identity-specific value signaling remain poorly understood. By manipulating the value and identity of appetizing food odors in a pattern-based imaging paradigm of human classical conditioning, we were able to identify dissociable predictive representations of identity-specific reward in orbitofrontal cortex (OFC) and identity-general reward in ventromedial prefrontal cortex (vmPFC). Reward-related functional coupling between OFC and olfactory (piriform) cortex and between vmPFC and amygdala revealed parallel pathways that support identity-specific and -general predictive signaling. The demonstration of identity-specific value representations in OFC highlights a role for this region in model-based behavior and reveals mechanisms by which appetitive behavior can go awry.

The Road Not Taken: Neural Correlates of Decision Making in Orbitofrontal Cortex

Empirical research links human orbitofrontal cortex (OFC) to the evaluation of outcomes during decision making and the representation of alternative (better) outcomes after failures. When faced with a difficult decision, rats sometimes pause and turn back-and-forth toward goals, until finally orienting toward the chosen direction. Neural representations of reward in rodent OFC increased immediately following each reorientation, implying a transient representation of the expected outcome following self-initiated decisions. Upon reaching reward locations and finding no reward (having made an error), OFC representations of reward decreased locally indicating a disappointment signal that then switched to represent the unrewarded, non-local, would-have-been rewarded site. These results illustrate that following a decision to act, neural ensembles in OFC represent reward, and upon the realization of an error, represent the reward that could have been.

The value of identity: olfactory notes on orbitofrontal cortex function

Neuroscientific research has emphatically promoted the idea that the key function of the orbitofrontal cortex (OFC) is to encode value. Associative learning studies indicate that OFC representations of stimulus cues reflect the predictive value of expected outcomes. Neuroeconomic studies suggest that the OFC distills abstract representations of value from discrete commodities to optimize choice. Although value-based models provide good explanatory power for many different findings, these models are typically disconnected from the very stimuli and commodities giving rise to those value representations. Little provision is made, either theoretically or empirically, for the necessary cooperative role of object identity, without which value becomes orphaned from its source. As a step toward remediating the value of identity, this review provides a focused olfactory survey of OFC research, including new work from our lab, to highlight the elemental involvement of this region in stimulus-specific predictive coding of both perceptual outcomes and expected values.

The architecture of reward value coding in the human orbitofrontal cortex.

To ensure their survival, animals exhibit a number of reward-directed behaviors, such as foraging for food or searching for mates. This suggests that a core set of brain regions may be shared by many species to process different types of rewards. Conversely, many new brain areas have emerged over the course of evolution, suggesting potential specialization of specific brain regions in the processing of more recent rewards such as money. Here, using functional magnetic resonance imaging in humans, we identified the common and distinct brain systems processing the value of erotic stimuli and monetary gains. First, we provide evidence that a set of neural structures, including the ventral striatum, anterior insula, anterior cingulate cortex, and midbrain, encodes the subjective value of rewards regardless of their type, consistent with a general hedonic representation. More importantly, our results reveal reward-specific representations in the orbitofrontal cortex (OFC): whereas the anterior lateral OFC, a phylogenetically recent structure, processes monetary gains, the posterior lateral OFC, phylogenetically and ontogenetically older, processes more basic erotic stimuli. This dissociation between OFC representations of primary and secondary rewards parallels current views on lateral prefrontal cortex organization in cognitive control, suggesting an increasing trend in complexity along a postero-anterior axis according to more abstract representations. Together, our results support a modular view of reward value coding in the brain and propose that a unifying principle of postero-anterior organization can be applied to the OFC.

The neural code of reward anticipation in human orbitofrontal cortex

An optimal choice among alternative behavioral options requires precise anticipatory representations of their possible outcomes. A fundamental question is how such anticipated outcomes are represented in the brain. Reward coding at the level of single cells in the orbitofrontal cortex (OFC) follows a more heterogeneous coding scheme than suggested by studies using functional MRI (fMRI) in humans. Using a combination of multivariate pattern classification and fMRI we show that the reward value of sensory cues can be decoded from distributed fMRI patterns in the OFC. This distributed representation is compatible with previous reports from animal electrophysiology that show that reward is encoded by different neural populations with opposing coding schemes. Importantly, the fMRI patterns representing specific values during anticipation are similar to those that emerge during the receipt of reward. Furthermore, we show that the degree of this coding similarity is related to subjects' ability to use value information to guide behavior. These findings narrow the gap between reward coding in humans and animals and corroborate the notion that value representations in OFC are independent of whether reward is anticipated or actually received.