Rapid Learning of Odor–Value Association in the Olfactory Striatum

Abstract

Rodents can successfully learn multiple novel stimulus-response associations after only a few repetitions when the contingencies predict reward. The circuits modified during such reinforcement learning to support decision-making are not known, but the olfactory tubercle (OT) and posterior piriform cortex (pPC) are candidates for decoding reward category from olfactory sensory input and relaying this information to cognitive and motor areas. Through single-cell recordings in behaving male and female C57BL/6 mice, we show here that an explicit representation for reward category emerges in the OT within minutes of learning a novel odor-reward association, whereas the pPC lacks an explicit representation even after weeks of overtraining. The explicit reward category representation in OT is visible in the first sniff (50-100 ms) of an odor on each trial, and precedes the motor action. Together, these results suggest that the coding of stimulus information required for reward prediction does not occur within olfactory cortex, but rather in circuits involving the olfactory striatum.

Phasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction

“…Such modifications were selective to the odor paired with phasic DA; hence, leaving the responses to other non-paired odors unchanged. Compatible with the concept that VS encodes the value of stimuli 13 , 24 , 39 – 41 , the decoding of stimulus representations increased after pairing with phasic DA. This increased distinctness of stimulus representation was also reflected in the perceived salience of the stimulus paired with phasic DA.…”

Rapid Bayesian learning in the mammalian olfactory system

“…7 h). Olfactory tubercle could be the site for this odor–reward association 5 , 34 , but it could be other regions, such as layer 3 of piriform cortex, as well. To test performance of this circuit, we implemented a go/no go task in which one odor is associated with a reward ( R = 1.0), while another odor is associated with no reward ( R = 0.0), regardless of concentrations.…”

“…Learning, however, is particularly difficult, especially in natural environments where odors are rarely presented in isolation, most odors are presented a small number of times, and odor identities are rarely supervised. Nevertheless, animals can learn to associate an odor with a reward in a few trials 3 – 5 . Our goal here is to elucidate the local plasticity mechanisms that orchestrate this rapid learning.…”

Hierarchical cross-scale analysis identifies parallel ventral striatal networks coding for dynamic and stabilized olfactory reward predictions

“…Recent studies have revealed that Tu neurons are recruited by stimuli that predict rewards upon conditioning (Gadziola et al, 2020, Millman and Murthy, 2020, Murata et al, 2015, Oettl et al, 2020, Zhang et al, 2017). In these studies, the duration of the conditioned stimulus partially overlaps with US.…”