OFC neurons do not represent the negative value of a conditioned inhibitor

Abstract

The orbitofrontal cortex (OFC) is often proposed to function as a value integrator; however, alternative accounts focus on its role in representing associative structures that specify the probability and sensory identity of future outcomes. These two accounts make different predictions about how this area should respond to conditioned inhibitors of reward, since in the former, neural activity should reflect the negative value of the inhibitor, whereas in the latter, it should track the estimated probability of a future reward based on all cues present. Here, we assessed these predictions by recording from small groups of neurons in the lateral OFC of rats during training in a conditioned inhibition design. Rats showed negative summation when the inhibitor was compounded with a novel excitor, suggesting that they learned to respond to the conditioned inhibitor appropriately. Against this backdrop, we found unit and population responses that scaled with expected reward value on excitor + inhibitor compound trials. However, the responses of these neurons did not differentiate between the conditioned inhibitor and a neutral cue when both were presented in isolation. Further, when the ensemble patterns were analyzed, activity to the conditioned inhibitor did not classify according to putative negative value. Instead, it classified with a same-modality neutral cue when presented alone and as a unique item when presented in compound with a novel excitor. This pattern of results supports the notion that OFC encodes a model of the causal structure of the environment rather than either the modality or the value of cues.