Functional diversity of dopamine axons in prefrontal cortex during classical conditioning

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  • Kenta Abe
    Department of Neuroscience, Medical University of South Carolina
  • Yuki Kambe
    Department of Pharmacology, Kagoshima University
  • Kei Majima
    Institute for Quantum Life Science, National Institutes for Quantum Science and Technology
  • Zijing Hu
    Department of Physiology, Monash University
  • Makoto Ohtake
    Department of Neuroscience, Medical University of South Carolina
  • Ali Momennezhad
    Department of Pharmacology, Kagoshima University
  • Hideki Izumi
    Faculty of Data Science, Shiga University
  • Takuma Tanaka
    Faculty of Data Science, Shiga University
  • Ashley Matunis
    Department of Neuroscience, Medical University of South Carolina
  • Emma Stacy
    Department of Neuroscience, Medical University of South Carolina
  • Takahide Itokazu
    Department of Neuro-Medical Science, Osaka University
  • Takashi R Sato
    Department of Neuroscience, Medical University of South Carolina
  • Tatsuo Sato
    Department of Pharmacology, Kagoshima University

Description

<jats:p>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) during reward and aversive processing. By optimizing microprism-mediated two-photon calcium imaging of dopamine axon terminals, we found diverse activity in dopamine axons responsive to both reward and aversive stimuli. Some axons exhibited a preference for reward, while others favored aversive stimuli, and there was a strong bias for the latter at the population level. Long-term longitudinal imaging revealed that the preference was maintained in reward- and aversive-preferring axons throughout classical conditioning in which rewarding and aversive stimuli were paired with preceding auditory cues. However, as mice learned to discriminate reward or aversive cues, a cue activity preference gradually developed only in aversive-preferring axons. We inferred the trial-by-trial cue discrimination based on machine learning using anticipatory licking or facial expressions, and found that successful discrimination was accompanied by sharper selectivity for the aversive cue in aversive-preferring axons. Our findings indicate that a group of mesocortical dopamine axons encodes aversive-related signals, which are modulated by both classical conditioning across days and trial-by-trial discrimination within a day.</jats:p>

Journal

  • eLife

    eLife 12 2024-05-15

    eLife Sciences Publications, Ltd

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