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Hierarchical architecture of dopaminergic circuits enables second-order conditioning in Drosophila.


ABSTRACT: Dopaminergic neurons with distinct projection patterns and physiological properties compose memory subsystems in a brain. However, it is poorly understood whether or how they interact during complex learning. Here, we identify a feedforward circuit formed between dopamine subsystems and show that it is essential for second-order conditioning, an ethologically important form of higher-order associative learning. The Drosophila mushroom body comprises a series of dopaminergic compartments, each of which exhibits distinct memory dynamics. We find that a slow and stable memory compartment can serve as an effective 'teacher' by instructing other faster and transient memory compartments via a single key interneuron, which we identify by connectome analysis and neurotransmitter prediction. This excitatory interneuron acquires enhanced response to reward-predicting odor after first-order conditioning and, upon activation, evokes dopamine release in the 'student' compartments. These hierarchical connections between dopamine subsystems explain distinct properties of first- and second-order memory long known by behavioral psychologists.

SUBMITTER: Yamada D 

PROVIDER: S-EPMC9937650 | biostudies-literature | 2023 Jan

REPOSITORIES: biostudies-literature

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Hierarchical architecture of dopaminergic circuits enables second-order conditioning in <i>Drosophila</i>.

Yamada Daichi D   Bushey Daniel D   Li Feng F   Hibbard Karen L KL   Sammons Megan M   Funke Jan J   Litwin-Kumar Ashok A   Hige Toshihide T   Aso Yoshinori Y  

eLife 20230124


Dopaminergic neurons with distinct projection patterns and physiological properties compose memory subsystems in a brain. However, it is poorly understood whether or how they interact during complex learning. Here, we identify a feedforward circuit formed between dopamine subsystems and show that it is essential for second-order conditioning, an ethologically important form of higher-order associative learning. The <i>Drosophila</i> mushroom body comprises a series of dopaminergic compartments,  ...[more]

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