Title Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments
Authors Stahl, Aaron
Noyes, Nathaniel C.
Boto, Tamara
Botero, Valentina
Broyles, Connor N.
Jing, Miao
Zeng, Jianzhi
King, Lanikea B.
Li, Yulong
Davis, Ronald L.
Tomchik, Seth M.
Affiliation Scripps Res Inst, Dept Neurosci, Jupiter, FL USA
Chinese Inst Brain Res, Beijing, Peoples R China
Peking Univ, Peking Tsinghua Ctr Life Sci, Beijing, Peoples R China
Peking Univ Sch Life Sci, State Key Lab Membrane Biol, Beijing, Peoples R China
PKU IDG McGovern Inst Brain Res, Beijing, Peoples R China
Keywords DROSOPHILA MUSHROOM BODY
MEMORY RETRIEVAL
EFFERENT NEURONS
OUTPUT NEURONS
N-TYPE
DOPAMINE
CALCIUM
REINFORCEMENT
EXPRESSION
CHANNELS
Issue Date 14-Mar-2022
Publisher ELIFE
Abstract Anatomical and physiological compartmentalization of neurons is a mechanism to increase the computational capacity of a circuit, and a major question is what role axonal compartmentalization plays. Axonal compartmentalization may enable localized, presynaptic plasticity to alter neuronal output in a flexible, experience-dependent manner. Here, we show that olfactory learning generates compartmentalized, bidirectional plasticity of acetylcholine release that varies across the longitudinal compartments of Drosophila mushroom body (MB) axons. The directionality of the learning-induced plasticity depends on the valence of the learning event (aversive vs. appetitive), varies linearly across proximal to distal compartments following appetitive conditioning, and correlates with learning-induced changes in downstream mushroom body output neurons (MBONs) that modulate behavioral action selection. Potentiation of acetylcholine release was dependent on the Ca(V)2.1 calcium channel subunit cacophony. In addition, contrast between the positive conditioned stimulus and other odors required the inositol triphosphate receptor, which maintained responsivity to odors upon repeated presentations, preventing adaptation. Downstream from the MB, a set of MBONs that receive their input from the gamma 3 MB compartment were required for normal appetitive learning, suggesting that they represent a key node through which reward learning influences decision-making. These data demonstrate that learning drives valence-correlated, compartmentalized, bidirectional potentiation, and depression of synaptic neurotransmitter release, which rely on distinct mechanisms and are distributed across axonal compartments in a learning circuit.
URI http://hdl.handle.net/20.500.11897/643016
ISSN 2050-084X
DOI 10.7554/eLife.76712
Indexed SCI(E)
Appears in Collections: 生命科学学院
膜生物学国家重点实验室

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