Emergence of Reward Coding in the Olfactory System

Abstract

Identifying dangerous or rewarding elements in an animal’s surroundings is an important – if not primary – function of sensory systems. This holds particularly true for the mouse olfactory system since odors convey crucial information about predators, mates, kin and food. Thus, the olfactory system needs to effectively determine which odors are present as well as whether each odor has a positive or negative association, termed valence. Currently, we have little knowledge of how reward influences the processing of odors in the olfactory system of behaving mice. My work focuses on two high-level olfactory areas, the posterior piriform cortex (pPC) and olfactory tubercle (OT), that are situated at the intersection of sensory and reward-related brain regions. The pPC receives direct input from early olfactory areas and makes reciprocal connections to cognitive brain regions such as orbitofrontal cortex, limbic structures and the medial temporal lobe. The OT is a part of the ventral striatum which also receives input from early olfactory areas and is heavily interconnected with the reward system. To examine odor and reward coding in these areas, I developed a novel odor categorization task and recorded individual pPC and OT neurons during task performance. Mice successfully learn multiple, novel odor-response associations after only a few repetitions when the contingencies predict reward. I find that an explicit representation for reward category emerges in the OT within minutes of learning a novel odor-response association, whereas the pPC lacks an explicit representation even after more than one month of overtraining. The explicit representation is visible in the first sniff of an odor on each trial, when the motor decision is made, and is not correlated with the trial-to-trial motor decision. Together, these results suggest that decoding of stimulus information required for reward-driven sensorimotor decision making does not occur within olfactory cortex, rather decoding occurs in circuits involving olfactory striatum.