Journal article
Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments
eLife, Vol.11, e76712
03/14/2022
DOI: 10.7554/eLife.76712
PMCID: PMC8956283
PMID: 35285796
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
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
2.1 calcium channel subunit
. 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 γ3 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.
Details
- Title: Subtitle
- Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments
- Creators
- Aaron Stahl - Scripps Research InstituteNathaniel C Noyes - Scripps Research InstituteTamara Boto - Scripps Research InstituteValentina Botero - Scripps Research InstituteConnor N Broyles - Scripps Research InstituteMiao Jing - Chinese Institute for Brain ResearchJianzhi Zeng - King CenterLanikea B King - Scripps Research InstituteYulong Li - King UniversityRonald L Davis - Scripps Research InstituteSeth M Tomchik - Scripps Research Institute
- Resource Type
- Journal article
- Publication Details
- eLife, Vol.11, e76712
- DOI
- 10.7554/eLife.76712
- PMID
- 35285796
- PMCID
- PMC8956283
- NLM abbreviation
- Elife
- ISSN
- 2050-084X
- eISSN
- 2050-084X
- Grant note
- R00 MH092294 / NIMH NIH HHS P40 OD018537 / NIH HHS R01 NS114403 / NINDS NIH HHS R01 NS097237 / NINDS NIH HHS U01 NS103558 / NINDS NIH HHS R35 NS097224 / NINDS NIH HHS
- Language
- English
- Date published
- 03/14/2022
- Academic Unit
- Iowa Neuroscience Institute; Neuroscience and Pharmacology
- Record Identifier
- 9984303854402771
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