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Takashi Sato: Learning enhances aversive signals in dopamine axons in medial prefrontal cortex

Midbrain dopamine neurons impact neural processing in the prefrontal cortex (PFC) through mesocortical projections. However, the signals conveyed by dopamine projections to the PFC remain unclear, particularly at the single-axon level. Here, we investigated dopaminergic axonal activity in the medial PFC (mPFC) in reward and aversive processing. Using microprism-mediated two-photon calcium imaging of dopamine axon terminals, we found that the axons showed increased activity for both reward and aversive stimuli, with a strong preference for the latter. Long-term longitudinal imaging revealed that the preference was maintained throughout Pavlovian conditioning in which reward and aversive stimuli were paired with preceding auditory cues. However, an activity preference at the conditioned cue gradually developed for aversive processing, in which mice learned to discriminate rewarding or aversive cues. We inferred the trial-by-trial cue discrimination based on machine learning using anticipatory licking or facial expressions, and found that the successful discrimination was accompanied by a sharper selectivity for aversive processing in the cue activity. Our findings demonstrate that dopamine neurons projecting to the mPFC do not code the reward prediction error; instead, they might code saliency signals that can become further biased to aversive processing through learning.


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