The orbitofrontal cortex (OFC) has long been implicated in associative learning. Early work by Mishkin and Rolls showed that the OFC was critical for rapid changes in learned behavior, a role that was reflected in the encoding of associative information by orbitofrontal neurons. Over the years, new data—particularly neurophysiological data—have increasingly emphasized the OFC in signaling actual value. These signals have been reported to vary according to internal preferences and judgments and to even be completely independent of the sensory qualities of predictive cues, the actual rewards, and the responses required to obtain them. At the same time, increasingly sophisticated behavioral studies have shown that the OFC is often unnecessary for simple value-based behavior and instead seems critical when information about specific outcomes must be used to guide behavior and learning. Here, we review these data and suggest a theory that potentially reconciles these two ideas, value versus specific outcomes, and bodies of work on the OFC.

The best way to respond flexibly to changes in the environment is to anticipate them. Such anticipation often benefits us if we can infer that a change has occurred, before we have actually experienced the effects of that change. Here we test for neural correlates of this process by recording single-unit activity in the orbitofrontal cortex in rats performing a choice task in which the available rewards changed across blocks of trials. Consistent with the proposal that orbitofrontal cortex signals inferred information, firing changes at the start of each new block as if predicting the not-yet-experienced reward. This change occurs whether the new reward is different in number of drops, requiring signaling of a new value, or in flavor, requiring signaling of a new sensory feature. These results show that orbitofrontal neurons provide a behaviorally relevant signal that reflects inferences about both value-relevant and value-neutral information about impending outcomes.

Neurons in the orbitofrontal cortex (OFC) fire in anticipation of and during rewards. Such firing has been suggested to encode reward predictions and to account in some way for the role of this area in adaptive behavior and learning. However, it has also been reported that neural activity in OFC reflects reward prediction errors, which might drive learning directly. Here we tested this question by analyzing the firing of OFC neurons recorded in an odor discrimination task in which rats were trained to sample odor cues and respond left or right on each trial for reward. Neurons were recorded across blocks of trials in which we switched either the number or the flavor of the reward delivered in each well. Previously we have described how neurons in this dataset fired to the predictive cues (Stalnaker et al., 2014); here we focused on the firing in anticipation of and just after delivery of each drop of reward, looking specifically for differences in firing based on whether the reward number or flavor was unexpected or expected. Unlike dopamine neurons recorded in this setting, which exhibited phasic error-like responses after surprising changes in either reward number or reward flavor (Takahashi et al., 2017), OFC neurons showed no such error correlates and instead fired in a way that reflected reward predictions.

The ventral striatum has long been proposed as an integrator of biologically significant associative information to drive actions. While inputs from the amygdala and hippocampus have been much studied, the role of prominent inputs from orbitofrontal cortex (OFC) are less well understood. Here we recorded single unit activity from ventral striatum core in rats with sham or ipsilateral neurotoxic lesions of lateral OFC, as they performed an odor-guided spatial choice task. Consistent with prior reports, we found that spiking activity recorded in sham rats during cue sampling was related to both reward magnitude and reward identity, with higher firing rates observed for cues that predicted more reward. Lesioned rats also showed differential activity to the cues, but this activity was unbiased towards larger rewards. These data support a role for OFC in shaping activity in the ventral striatum to represent the biological significance of associative information in the environment.