A neural system that represents the association of odors with rewarded outcomes and promotes behavioral engagement

Learning strengthens the strong emotional and behavioral responses odors are well known for eliciting. Presumably subserving this, several brain regions display experience-dependent plasticity during odor learning, yet the specific cellular systems involved and the actual influence of these systems on odor-directed behavior are less understood. Here we investigated the transformation of odor information throughout the association of odors with rewards and also sought to link those neural systems with displays of reinforcement-based task engagement. First, we investigated the representation of odor-reward associations within two areas recipient of dense olfactory bulb input, the posterior piriform cortex (pPCX) and olfactory tubercle (OT), using simultaneous multi-site electrophysiological recordings from mice engaged in a reward-based olfactory learning task. As expected, neurons in both regions represented conditioned odors and did so with similar information content, yet both the proportion of neurons recruited by conditioned rewarded odors and the magnitudes and durations of their responses were greater in the OT. Using fiber photometry, we found that OT D1-type dopamine receptor expressing neurons flexibly represent odors based upon reward associations. In both the recordings and imaging, statistically meaningful changes in activity occurred soon after odor onset. Finally, using optogenetics we show that OT D1-receptor expressing neurons strongly influence behavior to promote task engagement. Together our results contribute to a model whereby OT D1 neurons support odor-guided motivated behaviors.