Responding to preconditioned cues is devaluation sensitive and requires orbitofrontal cortex during cue-cue learning

Abstract

The orbitofrontal cortex (OFC) is necessary for inferring value in tests of model-based reasoning, including in sensory preconditioning. This involvement could be accounted for by representation of value or by representation of broader associative structure. We recently reported neural correlates of such broader associative structure in OFC during the initial phase of sensory preconditioning (Sadacca et al., 2018). Here, we used optogenetic inhibition of OFC to test whether these correlates might be necessary for value inference during later probe testing. We found that inhibition of OFC during cue-cue learning abolished value inference during the probe test, inference subsequently shown in control rats to be sensitive to devaluation of the expected reward. These results demonstrate that OFC must be online during cue-cue learning, consistent with the argument that the correlates previously observed are not simply downstream readouts of sensory processing and instead contribute to building the associative model supporting later behavior.

Is the core function of orbitofrontal cortex to signal values or make predictions?

“…After the outcome is paired with an unpleasant experience such as LiCl injection or satiety, normal subjects would update value of the cue through its model-based association with the outcome, which is reflected in reduced responding to the cue during the probe test. Work using this procedure has shown repeatedly that OFC manipulations disrupt normal changes in behavior after devaluation [57][58][59][60][61][62][63][64]. This has recently also been found to be true in instrumental settings, specifically when prior learning of the operanda has occurred [58,65].…”

“…In each of these tasks, the critical role of the OFC is difficult to explain as signaling of scalar value, while being easy to explain as related to representing task structure. This is particularly true in a recent study showing that optogenetically inactivating OFC during the initial cue-cue learning during sensory preconditioning abolishes value inference in the later the probe test [59]. The initial cue-cue learning occurs in the absence of any overt value or reward; there is no behavioral response.…”

“…Though this at first seems far-fetched, it turns out that such evidence is actually relatively abundant. For instance, OFC is required for outcome-specific Pavlovian-to-instrumental transfer [58,70], outcome-identity unblocking [71], facilitated learning caused by differential outcomes [72], and for proper sensory learning in the first phase of sensory preconditioning [59]. In each of these tasks, the critical role of the OFC is difficult to explain as signaling of scalar value, while being easy to explain as related to representing task structure.…”

Value Representations in the Rodent Orbitofrontal Cortex Drive Learning, not Choice

“…Taken together with this literature, our results suggest that OFC activity is necessary when the cognitive map is deployed to guide learning, but not when it is deployed to guide choice. Recent data suggest that this role may not be limited to learning about value, but extend to learning purely sensory associations as well (Hart et al, 2020)…”

The orbitofrontal cortex is necessary for learning to ignore

“…If so, the orbitofrontal cortex (OFC), as a key node in such networks, should be important. 3 Specifically, the OFC has been hypothesized to participate in the recognition of hidden task states, which are not directly signaled by explicit outcomes. 4 Evaluating its involvement in pre-exposure learning during latent inhibition would be an acid test for this hypothesis.…”