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...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Wang-Pao Lee, Meng-Hsuan Chiang, Li-Yun Chang, Wei-Huan Shyu, Tai-Hsiang Chiu, Tsai-Feng Fu, Tony Wu, Chia-Lin Wu
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	mushroom body serotonin 5HT receptor long-term memory neuronal circuits of the brain Drosophila melanogaster Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/4206f49720724846ad22444c8488478f
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:4206f49720724846ad22444c8488478f
record_format	dspace
spelling	oai:doaj.org-article:4206f49720724846ad22444c8488478f2021-11-11T05:40:36ZSerotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila2296-634X10.3389/fcell.2021.755574https://doaj.org/article/4206f49720724846ad22444c8488478f2021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fcell.2021.755574/fullhttps://doaj.org/toc/2296-634XMemory 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.Wang-Pao LeeMeng-Hsuan ChiangLi-Yun ChangWei-Huan ShyuTai-Hsiang ChiuTsai-Feng FuTony WuTony WuTony WuChia-Lin WuChia-Lin WuChia-Lin WuChia-Lin WuFrontiers Media S.A.articlemushroom bodyserotonin5HT receptorlong-term memoryneuronal circuits of the brainDrosophila melanogasterBiology (General)QH301-705.5ENFrontiers in Cell and Developmental Biology, Vol 9 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	mushroom body serotonin 5HT receptor long-term memory neuronal circuits of the brain Drosophila melanogaster Biology (General) QH301-705.5
spellingShingle	mushroom body serotonin 5HT receptor long-term memory neuronal circuits of the brain Drosophila melanogaster Biology (General) QH301-705.5 Wang-Pao Lee Meng-Hsuan Chiang Li-Yun Chang Wei-Huan Shyu Tai-Hsiang Chiu Tsai-Feng Fu Tony Wu Tony Wu Tony Wu Chia-Lin Wu Chia-Lin Wu Chia-Lin Wu Chia-Lin Wu Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila
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	article
author	Wang-Pao Lee Meng-Hsuan Chiang Li-Yun Chang Wei-Huan Shyu Tai-Hsiang Chiu Tsai-Feng Fu Tony Wu Tony Wu Tony Wu Chia-Lin Wu Chia-Lin Wu Chia-Lin Wu Chia-Lin Wu
author_facet	Wang-Pao Lee Meng-Hsuan Chiang Li-Yun Chang Wei-Huan Shyu Tai-Hsiang Chiu Tsai-Feng Fu Tony Wu Tony Wu Tony Wu Chia-Lin Wu Chia-Lin Wu Chia-Lin Wu Chia-Lin Wu
author_sort	Wang-Pao Lee
title	Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila
title_short	Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila
title_full	Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila
title_fullStr	Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila
title_full_unstemmed	Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila
title_sort	serotonin signals modulate mushroom body output neurons for sustaining water-reward long-term memory in drosophila
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/4206f49720724846ad22444c8488478f
work_keys_str_mv	AT wangpaolee serotoninsignalsmodulatemushroombodyoutputneuronsforsustainingwaterrewardlongtermmemoryindrosophila AT menghsuanchiang serotoninsignalsmodulatemushroombodyoutputneuronsforsustainingwaterrewardlongtermmemoryindrosophila AT liyunchang serotoninsignalsmodulatemushroombodyoutputneuronsforsustainingwaterrewardlongtermmemoryindrosophila AT weihuanshyu serotoninsignalsmodulatemushroombodyoutputneuronsforsustainingwaterrewardlongtermmemoryindrosophila AT taihsiangchiu serotoninsignalsmodulatemushroombodyoutputneuronsforsustainingwaterrewardlongtermmemoryindrosophila AT tsaifengfu serotoninsignalsmodulatemushroombodyoutputneuronsforsustainingwaterrewardlongtermmemoryindrosophila AT tonywu serotoninsignalsmodulatemushroombodyoutputneuronsforsustainingwaterrewardlongtermmemoryindrosophila AT tonywu serotoninsignalsmodulatemushroombodyoutputneuronsforsustainingwaterrewardlongtermmemoryindrosophila AT tonywu serotoninsignalsmodulatemushroombodyoutputneuronsforsustainingwaterrewardlongtermmemoryindrosophila AT chialinwu serotoninsignalsmodulatemushroombodyoutputneuronsforsustainingwaterrewardlongtermmemoryindrosophila AT chialinwu serotoninsignalsmodulatemushroombodyoutputneuronsforsustainingwaterrewardlongtermmemoryindrosophila AT chialinwu serotoninsignalsmodulatemushroombodyoutputneuronsforsustainingwaterrewardlongtermmemoryindrosophila AT chialinwu serotoninsignalsmodulatemushroombodyoutputneuronsforsustainingwaterrewardlongtermmemoryindrosophila
_version_	1718439478919430144

Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila

Ejemplares similares