Sniffing Shapes Dopamine Signals for Reward Prediction

Adaptive behaviors depend on predicting outcomes from sensory evidence. Dopamine neurons in the ventral tegmental area (VTA) broadcast reward-prediction signals that guide learning. Yet the principles functionally coordinating information flow from input regions to VTA are incompletely understood. In the olfactory system, the sniff cycle structures sampling and odor encoding. We therefore asked whether this rhythm also entrains the ventral striatum to VTA communication and if so, how this shapes the implementation of predictive coding in dopamine neurons. We recorded identified dopamine neurons throughout olfactory conditioning and found that their firing shifted systematically to the post-inspiratory phase of the sniff cycle with learning. This temporal realignment predicted a neuron’s engagement in value encoding along the optimism-pessimism-spectrum of distributional reinforcement learning. This is associated with an enhanced phase-gated communication channel from the striatal olfactory tubercle to dopamine neurons, the strength of which predicts task performance. Thus, the sniffing rhythm provides a scaffold for information flow, revealing a phase-gating mechanism for the integration of outcome predicting sensory evidence to dopamine neurons during reinforcement learning.