Taste-odor association learning alters the dynamics of intra-oral odor responses in the posterior piriform cortex of awake rats

Abstract

How an odor is perceived is to a large extent dependent on the context in which that odor is (or has been) experienced. For example, experiencing an odor in mixture with taste during consumption can instill taste qualities in the percept of that odor (e.g., vanilla—an odor—has a gustatory quality: sweet). How associative features of odors are encoded in the brain remains unknown, but previous work suggests an important role for ongoing interactions between piriform cortex and extra-olfactory systems. Here we tested the hypothesis that piriform cortex dynamically encodes taste associations of odors. Rats were trained to associate one of two odors with saccharin; the other odor remained neutral. Before and after training, we tested preferences for the saccharin-associated odor versus the neutral odor, and recorded spiking responses from ensembles of neurons in posterior piriform cortex (pPC) to intra-oral delivery of small drops of the same odor solutions. The results show that animals successfully learned taste-odor associations. At the neural level, single pPC neuron responses to the saccharin-paired odor were selectively altered following conditioning. Altered response patterns appeared after 1 second following stimulus delivery, and successfully discriminated between the two odors. However, firing rate patterns in the late epoch appeared different from firing rates early in the early epoch (<1 second following stimulus delivery). That is, in different response epoch, neurons used different codes to represent the difference between the two odors. The same dynamic coding scheme was observed at the ensemble level.

Significance Statement

Odors carry important meaning beyond their chemical identity. One particularly salient example of this are food odors, which play an important role in determining flavor preferences and food choice behavior. How these extra-olfactory aspects of odor are represented is unknown. Using extracellular recordings in awake rats in the context of a flavor preference learning task, we show that learned taste associations of odor stimuli are represented in the dynamic firing patterns of posterior piriform cortex neurons. The results suggest that associative odor coding results from ongoing interactions between olfactory and extra-olfactory systems.