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Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila
Memory consolidation is a time-dependent process through which an unstable learned experience is transformed into a stable long-term memory; however, the circuit and molecular mechanisms underlying this process are poorly understood. The Drosophila mushroom body (MB) is a huge brain neuropil that pl...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8631865/ https://www.ncbi.nlm.nih.gov/pubmed/34858982 http://dx.doi.org/10.3389/fcell.2021.755574 |
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author | Lee, Wang-Pao Chiang, Meng-Hsuan Chang, Li-Yun Shyu, Wei-Huan Chiu, Tai-Hsiang Fu, Tsai-Feng Wu, Tony Wu, Chia-Lin |
author_facet | Lee, Wang-Pao Chiang, Meng-Hsuan Chang, Li-Yun Shyu, Wei-Huan Chiu, Tai-Hsiang Fu, Tsai-Feng Wu, Tony Wu, Chia-Lin |
author_sort | Lee, Wang-Pao |
collection | PubMed |
description | Memory consolidation is a time-dependent process through which an unstable learned experience is transformed into a stable long-term memory; however, the circuit and molecular mechanisms underlying this process are poorly understood. The Drosophila mushroom body (MB) is a huge brain neuropil that plays a crucial role in olfactory memory. The MB neurons can be generally classified into three subsets: γ, αβ, and α′β′. Here, we report that water-reward long-term memory (wLTM) consolidation requires activity from α′β′-related mushroom body output neurons (MBONs) in a specific time window. wLTM consolidation requires neurotransmission in MBON-γ3β′1 during the 0–2 h period after training, and neurotransmission in MBON-α′2 is required during the 2–4 h period after training. Moreover, neurotransmission in MBON-α′1α′3 is required during the 0–4 h period after training. Intriguingly, blocking neurotransmission during consolidation or inhibiting serotonin biosynthesis in serotoninergic dorsal paired medial (DPM) neurons also disrupted the wLTM, suggesting that wLTM consolidation requires serotonin signals from DPM neurons. The GFP Reconstitution Across Synaptic Partners (GRASP) data showed the connectivity between DPM neurons and MBON-γ3β′1, MBON-α′2, and MBON-α′1α′3, and RNAi-mediated silencing of serotonin receptors in MBON-γ3β′1, MBON-α′2, or MBON-α′1α′3 disrupted wLTM. Taken together, our results suggest that serotonin released from DPM neurons modulates neuronal activity in MBON-γ3β′1, MBON-α′2, and MBON-α′1α′3 at specific time windows, which is critical for the consolidation of wLTM in Drosophila. |
format | Online Article Text |
id | pubmed-8631865 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-86318652021-12-01 Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila Lee, Wang-Pao Chiang, Meng-Hsuan Chang, Li-Yun Shyu, Wei-Huan Chiu, Tai-Hsiang Fu, Tsai-Feng Wu, Tony Wu, Chia-Lin Front Cell Dev Biol Cell and Developmental Biology Memory consolidation is a time-dependent process through which an unstable learned experience is transformed into a stable long-term memory; however, the circuit and molecular mechanisms underlying this process are poorly understood. The Drosophila mushroom body (MB) is a huge brain neuropil that plays a crucial role in olfactory memory. The MB neurons can be generally classified into three subsets: γ, αβ, and α′β′. Here, we report that water-reward long-term memory (wLTM) consolidation requires activity from α′β′-related mushroom body output neurons (MBONs) in a specific time window. wLTM consolidation requires neurotransmission in MBON-γ3β′1 during the 0–2 h period after training, and neurotransmission in MBON-α′2 is required during the 2–4 h period after training. Moreover, neurotransmission in MBON-α′1α′3 is required during the 0–4 h period after training. Intriguingly, blocking neurotransmission during consolidation or inhibiting serotonin biosynthesis in serotoninergic dorsal paired medial (DPM) neurons also disrupted the wLTM, suggesting that wLTM consolidation requires serotonin signals from DPM neurons. The GFP Reconstitution Across Synaptic Partners (GRASP) data showed the connectivity between DPM neurons and MBON-γ3β′1, MBON-α′2, and MBON-α′1α′3, and RNAi-mediated silencing of serotonin receptors in MBON-γ3β′1, MBON-α′2, or MBON-α′1α′3 disrupted wLTM. Taken together, our results suggest that serotonin released from DPM neurons modulates neuronal activity in MBON-γ3β′1, MBON-α′2, and MBON-α′1α′3 at specific time windows, which is critical for the consolidation of wLTM in Drosophila. Frontiers Media S.A. 2021-11-11 /pmc/articles/PMC8631865/ /pubmed/34858982 http://dx.doi.org/10.3389/fcell.2021.755574 Text en Copyright © 2021 Lee, Chiang, Chang, Shyu, Chiu, Fu, Wu and Wu. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Cell and Developmental Biology Lee, Wang-Pao Chiang, Meng-Hsuan Chang, Li-Yun Shyu, Wei-Huan Chiu, Tai-Hsiang Fu, Tsai-Feng Wu, Tony Wu, Chia-Lin Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila |
title | Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila
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title_full | Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila
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title_fullStr | Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila
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title_full_unstemmed | Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila
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title_short | Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila
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title_sort | serotonin signals modulate mushroom body output neurons for sustaining water-reward long-term memory in drosophila |
topic | Cell and Developmental Biology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8631865/ https://www.ncbi.nlm.nih.gov/pubmed/34858982 http://dx.doi.org/10.3389/fcell.2021.755574 |
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