Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments
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...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-03-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/76712 |
| _version_ | 1811235822886715392 |
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| author | Aaron Stahl Nathaniel C Noyes Tamara Boto Valentina Botero Connor N Broyles Miao Jing Jianzhi Zeng Lanikea B King Yulong Li Ronald L Davis Seth M Tomchik |
| author_facet | Aaron Stahl Nathaniel C Noyes Tamara Boto Valentina Botero Connor N Broyles Miao Jing Jianzhi Zeng Lanikea B King Yulong Li Ronald L Davis Seth M Tomchik |
| author_sort | Aaron Stahl |
| collection | DOAJ |
| description | 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 CaV2.1 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 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. |
| first_indexed | 2024-04-12T11:58:36Z |
| format | Article |
| id | doaj.art-dec195defa834890b9033a0c335f44a0 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T11:58:36Z |
| publishDate | 2022-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-dec195defa834890b9033a0c335f44a02022-12-22T03:33:56ZengeLife Sciences Publications LtdeLife2050-084X2022-03-011110.7554/eLife.76712Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartmentsAaron Stahl0https://orcid.org/0000-0003-3170-1101Nathaniel C Noyes1Tamara Boto2https://orcid.org/0000-0002-9974-3714Valentina Botero3https://orcid.org/0000-0002-9744-3929Connor N Broyles4https://orcid.org/0000-0002-2930-7343Miao Jing5Jianzhi Zeng6https://orcid.org/0000-0002-5380-6281Lanikea B King7Yulong Li8Ronald L Davis9Seth M Tomchik10https://orcid.org/0000-0001-5686-0833Department of Neuroscience, The Scripps Research Institute, Jupiter, United StatesDepartment of Neuroscience, The Scripps Research Institute, Jupiter, United StatesDepartment of Neuroscience, The Scripps Research Institute, Jupiter, United StatesDepartment of Neuroscience, The Scripps Research Institute, Jupiter, United StatesDepartment of Neuroscience, The Scripps Research Institute, Jupiter, United StatesChinese Institute for Brain Research, Beijing, ChinaPeking-Tsinghua Center for Life Sciences, Peking University, Beijing, China; State Key Laboratory of Membrane Biology, Peking University School of Life Sciences, Beijing, China; PKU IDG/McGovern Institute for Brain Research, Beijing, ChinaDepartment of Neuroscience, The Scripps Research Institute, Jupiter, United StatesChinese Institute for Brain Research, Beijing, China; Peking-Tsinghua Center for Life Sciences, Peking University, Beijing, China; State Key Laboratory of Membrane Biology, Peking University School of Life Sciences, Beijing, China; PKU IDG/McGovern Institute for Brain Research, Beijing, ChinaDepartment of Neuroscience, The Scripps Research Institute, Jupiter, United StatesDepartment of Neuroscience, The Scripps Research Institute, Jupiter, United StatesAnatomical 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 CaV2.1 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 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.https://elifesciences.org/articles/76712synapticpotentiationIP3Rhabituationdepressioncav2 |
| spellingShingle | Aaron Stahl Nathaniel C Noyes Tamara Boto Valentina Botero Connor N Broyles Miao Jing Jianzhi Zeng Lanikea B King Yulong Li Ronald L Davis Seth M Tomchik Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments eLife synaptic potentiation IP3R habituation depression cav2 |
| title | Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments |
| title_full | Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments |
| title_fullStr | Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments |
| title_full_unstemmed | Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments |
| title_short | Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments |
| title_sort | associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments |
| topic | synaptic potentiation IP3R habituation depression cav2 |
| url | https://elifesciences.org/articles/76712 |
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