Motivationally attractive cues can draw in behavior in a phenomenon termed incentive salience. Incentive cue attraction is an important model for animal models of drug seeking and relapse. One question of interest is the extent to which the pursuit of motivationally attractive cues is related to the value of the paired outcome or can become unrelated and habitual. We studied this question using a sign-tracking (ST) paradigm in rats, in which a lever stimulus preceding food reward comes to elicit conditioned lever-interaction behavior. We asked whether reinforcer devaluation by means of conditioned taste aversion, a classic test of habitual behavior, can modify ST to incentive cues, and whether this depends upon the manner in which reinforcer devaluation takes place. In contrast to several recent reports, we conclude that ST is indeed sensitive to reinforcer devaluation. However, this effect depends critically upon the congruence between the context in which taste aversion is learned and the context in which it is tested. When the taste aversion successfully transfers to the testing context, outcome value strongly influences ST behavior, both when the outcome is withheld (in extinction) and when animals can learn from outcome feedback (reacquisition). When taste aversion does not transfer to the testing context, ST remains high. In total, the extent to which ST persists after outcome devaluation is closely related to the extent to which that outcome is truly devalued in the task context. We believe this effect of context on devaluation can reconcile contradictory findings about the flexibility/inflexibility of ST. We discuss this literature and relate our findings to the study of habits generally.
When pursuing desirable outcomes, one must make the decision between exploring possible actions to obtain those outcomes and exploiting known strategies to maximize efficiency. The dorsolateral striatum (DLS) has been extensively studied with respect to how actions can develop into habits and has also been implicated as an area involved in governing exploitative behavior. Surprisingly, prior work has shown that DLS cholinergic interneurons (ChIs) are not involved in the canonical habit formation function ascribed to the DLS but are instead modulators of behavioral flexibility after initial learning. To further probe this, we evaluated the role of DLS ChIs in behavioral exploration during a brief instrumental training experiment. Through designer receptors exclusively activated by designer drugs (DREADDs) in ChAT‐Cre rats, ChIs in the DLS were inhibited during specific phases of the experiment: instrumental training, free‐reward delivery, at both times, or never. Without ChI activity during instrumental training, animals biased their responding toward an “optimal” strategy while continuing to work efficiently. This effect was observed again when contingencies were removed as animals with ChIs offline during that phase, regardless of ChI inhibition previously, decreased responding more than animals with ChIs intact. These findings build upon a growing body of literature implicating ChIs in the striatum as gate‐keepers of behavioral flexibility and exploration.
The basolateral amygdala (BLA) has been implicated in mediating both fear and reward learning. Parvalbumin interneurons (PVs) in the BLA have previously been shown to contribute to BLA oscillatory states integral to fear expression, but whether BLA oscillatory states and PV interneurons also contribute to reward learning is unknown and critical to our understanding of reward processing. Local field potentials in the BLA were collected as animals consumed a sucrose reward, where prominent changes in the beta band (15-30 Hz) emerged with reward experience. Rhythmic optogenetic stimulation of PV interneurons to entrain the BLA network to 20Hz during consumption of one bottle during a two bottle choice test produced a robust bottle preference. Finally, to demonstrate that PV activity is necessary for reward value use, PVs were chemogenetically targeted and inhibited following outcome devaluation, rendering those animals incapable of using updated reward value information to guide their behavior. Taken together, these experiments provide novel information regarding the physiological signatures of reward learning while highlighting the importance of PV interneurons in reward learning. This work builds upon the established knowledge in the field of PV involvement in fear expression and provides evidence that PV orchestration of unique BLA network states is involved in both learning types.
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