Serotonin receptor 5-HT7 in Drosophila mushroom body neurons mediates larval appetitive olfactory learning

Ganguly, Archan; Cheng, Qi; Bajaj, Jeevisha; Lee, Daewoo

doi:10.1038/s41598-020-77910-5

Cited by 19 publications

(14 citation statements)

References 72 publications

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“…The lack of serotonergic neuron in the larval mushroom body, however, does not suggest that serotonin plays no role in learning and memory at larval stage. Recently, a serotonin receptor, 5-HT7, was found expressing in the mushroom body of Drosophila larvae, which was shown to mediate the associative olfactory appetitive learning and memory ( Huser et al, 2017 ; Ganguly et al, 2020 ). Whether serotonin mediates the associative learning and memory for S. frugiperda in the same manner could be investigated by using molecular methods in future study.…”

Section: Discussionmentioning

confidence: 99%

Serotonergic Neurons in the Brain and Gnathal Ganglion of Larval Spodoptera frugiperda

et al. 2022

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The fall armyworm Spodoptera frugiperda (S. frugiperda) (Lepidoptera: Noctuidae) is a worldwide, disruptive, agricultural pest species. The larvae of S. frugiperda feed on seedling, leave, and kernel of crops with chewing mouthparts, resulting in reduced crop yields. Serotonin is an important biogenic amine acting as a neural circuit modulator known to mediate lots of behaviors including feeding in insects. In order to explore the serotonergic neural network in the nervous system of larval S. frugiperda, we performed immunohistochemical experiments to examine the neuropil structure of the brain and the gnathal ganglion with antisynapsin and to examine their serotonergic neurons with antiserotonin serum. Our data show that the brain of larval S. frugiperda contains three neuromeres: the tritocerebrum, the deutocerebrum, and the protocerebrum. The gnathal ganglion also contains three neuromeres: the mandibular neuromere, the maxillary neuromere, and the labial neuromere. There are about 40 serotonergic neurons in the brain and about 24 serotonergic neurons in the gnathal ganglion. Most of these neurons are wide-field neurons giving off processes in several neuropils of the brain and the gnathal ganglion. Serotonergic neuron processes are mainly present in the protocerebrum. A pair of serotonergic neurons associated with the deutocerebrum has arborizations in the contralateral antennal lobe and bilateral superior lateral protocerebra. In the gnathal ganglion, the serotonergic neuron processes are also widespread throughout the neuropil and some process projections extend to the tritocerebrum. These findings on the serotonergic neuron network in larval S. frugiperda allow us to explore the important roles of serotonin in feeding and find a potential approach to modulate the feeding behavior of the gluttonous pest and reduce its damage.

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Section: Discussionmentioning

confidence: 99%

Serotonergic Neurons in the Brain and Gnathal Ganglion of Larval Spodoptera frugiperda

et al. 2022

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“…Despite the known importance of serotonergic signaling in olfactory learning in Drosophila (Ganguly et al, 2020; Johnson et al, 2011; Keene et al, 2006; Keene et al, 2004; Krashes et al, 2007; Lee et al, 2011; Sitaraman et al, 2008; Waddell et al, 2000; Wu et al, 2011; Yu et al, 2005), the dynamics of 5-HT signaling in vivo and the mechanisms that regulate this signaling processes are largely unknown. Previously, addressing these fundamental biological questions has been difficult due to the absence of suitable tools for monitoring 5-HT dynamics in vivo with high spatiotemporal resolution.…”

Section: Discussionmentioning

confidence: 99%

“…In each hemisphere of the MB, the serotonergic DPM neuron innervates all three lobes, which has been reported to be involved in olfactory learning in both adults and larvae. (Ganguly et al, 2020; Johnson et al, 2011; Keene et al, 2006; Keene et al, 2004; Krashes et al, 2007; Lee et al, 2011; Waddell et al, 2000; Wu et al, 2011; Yu et al, 2005). However, the in vivo dynamics of 5-HT release from the DPM neuron, in responses to physiological stimuli and its regulation, are poorly understood.…”

Section: Mainmentioning

confidence: 99%

Local 5-HT signal bi-directionally regulates the coincidence time window of associative learning

Zeng

Zhangren

et al. 2022

Preprint

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Temporal coincidence between the conditioned stimulus (CS) and unconditioned stimulus (US) is essential for associative learning across species. Despite its ubiquitous presence, the mechanism that may regulate this time window duration remains unclear yet. Using olfactory associative learning in Drosophila as a model, we find that suppressing or promoting serotonin (5-HT) signal could respectively shorten or prolong the coincidence time window of odor-shock associative learning and synaptic plasticity in mushroom body (MB) Kenyon cells (KCs). Capitalizing on GPCR-activation based (GRAB) sensors for 5-HT and acetylcholine (ACh), we characterized the in vivo 5-HT dynamics in MB lobes during odor and shock stimulations and further dissected this microcircuit. Interestingly, local KC-released ACh activates nicotinic receptors on the dorsal paired medial (DPM) neuron, and in turn the DPM neuron releases 5-HT to inhibit the ACh signal via the 5-HT1a receptor. Finally, we demonstrated that the DPM-mediated serotonergic feedback circuit is sufficient and necessary to regulate the coincidence time window. This work provides a model for studying the temporal contingency of environmental events and their causal relationship

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“…In fruit flies, the 5HT system participates in olfactory learning and memory ( Johnson et al, 2011 ; Sitaraman et al, 2012 ; Scheunemann et al, 2018 ; Ganguly et al, 2020 ), and a previous study suggested that 5HT signals from DPM neurons modulate the activity of the MB αβ neurons, which play a crucial role in olfactory aversive anesthesia-resistant memory formation ( Lee et al, 2011 ). The axons of DPM neurons innervate the MB lobe, in which the MBON dendrites are distributed.…”

Section: Discussionmentioning

confidence: 99%

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

Lee

Chiang

Chang

et al. 2021

Front. Cell Dev. Biol.

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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.

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Serotonin receptor 5-HT7 in Drosophila mushroom body neurons mediates larval appetitive olfactory learning

Cited by 19 publications

References 72 publications

Serotonergic Neurons in the Brain and Gnathal Ganglion of Larval Spodoptera frugiperda

Serotonergic Neurons in the Brain and Gnathal Ganglion of Larval Spodoptera frugiperda

Local 5-HT signal bi-directionally regulates the coincidence time window of associative learning

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

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