A Population of Interneurons Signals Changes in the Basal Concentration of Serotonin and Mediates Gain Control in the Drosophila Antennal Lobe

Schenk, Jonathan E.; Tan, Hua; Gaudry, Quentin

doi:10.1016/j.cub.2020.01.018

Cited by 19 publications

(24 citation statements)

References 51 publications

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“…These neurons form connections on the presynaptic bouton of ORN synapses to cause lateral excitation or inhibition across glomeruli (Olsen et al, 2007;Wang et al, 2003;Wilson, 2013). These connections are required for fine tuning of signaling at synapses as a way of rapid modulation of neuronal function (Dacks et al, 2009;Johnson et al, 2009;Mohamed et al, 2019;Olsen et al, 2007;Sizemore and Dacks, 2016;Sudhakaran et al, 2012;Suzuki et al, 2020;Wang et al, 2003;Wong et al, 2002;Zhang et al, 2019). We found a high expression of choline acetyltransferase (ChAT) that catalyzes acetylcholine biosynthesis and VAChT that packages acetylcholine into synaptic vesicles, coinciding with their reported cholinergic roles.…”

Section: Regulators Of Neurotransmissionsupporting

confidence: 52%

“…Moreover, we also found relatively high expression of several genes encoding receptors of various neurotransmitters, such as choline, serotonin (5-HT), GABA, and glutamate (Figure 6C-F’). Many of these genes, such as nAChRalpha4 / 5 , 5-HT2A , 5-HT7 , GABA-B-R2 , and GluRIIA , have previously been found to regulate courtship behavior in flies through signaling in the antennal lobe (Becnel et al, 2011; Clowney et al, 2015; Johnson et al, 2011; Suzuki et al, 2020). Interestingly, GABA-B-R2 was shown to be specifically involved in presynaptic gain control of Or47b ORNs (Root et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

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Social experience and pheromone receptor activity reprogram behavioral switch and neuromodulatory gene expression in sensory neurons

Volkan

Deanhardt

Duan

et al. 2021

Preprint

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Social experience and pheromone signaling in ORNs affect pheromone responses and male courtship behaviors in Drosophila, however, the molecular mechanisms underlying this circuit-level neuromodulation remain less clear. Previous studies identified social experience and pheromone signaling-dependent modulation of chromatin around behavioral switch gene fruitless, which encodes a transcription factor necessary and sufficient for male behaviors. To identify the molecular mechanisms driving social experience-dependent neuromodulation, we performed RNA-seq from antennal samples of mutant fruit flies in pheromone receptors and fruitless, as well as grouped or isolated wild-type males. We found that loss of pheromone detection differentially alters the levels of fruitless exons suggesting changes in splicing patterns. In addition, many Fruitless target neuromodulatory genes, such as neurotransmitter receptors, ion channels, and ion transporters, are differentially regulated by social context and pheromone signaling. Our results suggest that modulation of circuit activity and behaviors in response to social experience and pheromone signaling arise due to changes in transcriptional programs for neuromodulators downstream of behavioral switch gene function.

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Section: Regulators Of Neurotransmissionsupporting

confidence: 52%

Section: Introductionmentioning

confidence: 99%

Social experience and pheromone receptor activity reprogram behavioral switch and neuromodulatory gene expression in sensory neurons

Volkan

Deanhardt

Duan

et al. 2021

Preprint

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“…The effects of 5-HT on mosquito olfaction and vision could be reflected in the processing of this sensory information. In D. melanogaster , 5-HT plays an important role in gain control in the fly antennal lobe, and serotonergic neurons are predominantly located and innervate the fly optic lobe suggesting important functional effects ( Bao et al, 2010 ; Suzuki et al, 2020 ). It remains unclear whether the ingestion of the 5-HT in the blood meal could mediate similar functional effects in the A. stephensi brain, but passage of ingested 5-HT into the body with circulation to the brain or a neuromodulatory link suggested by our immunohistochemistry data could mediate gut-to-brain and brain-to-gut 5-HT signaling in A. stephensi .…”

Section: Discussionmentioning

confidence: 99%

Anopheles stephensi Feeding, Flight Behavior, and Infection With Malaria Parasites are Altered by Ingestion of Serotonin

et al. 2022

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Approximately 3.4 billion people are at risk of malaria, a disease caused by infection with Plasmodium spp. parasites, which are transmitted by Anopheles mosquitoes. Individuals with severe falciparum malaria often exhibit changes in circulating blood levels of biogenic amines, including reduced serotonin or 5-hydroxytryptamine (5-HT), and these changes are associated with disease pathology. In insects, 5-HT functions as an important neurotransmitter for many behaviors and biological functions. In Anopheles stephensi, we show that 5-HT is localized to innervation in the head, thorax, and midgut, suggesting a gut-to-brain signaling axis that could support the effects of ingested 5-HT on mosquito biology and behavioral responses. Given the changes in blood levels of 5-HT associated with severe malaria and the key roles that 5-HT plays in insect neurophysiology, we investigated the impact of ingesting blood with healthy levels of 5-HT (1.5 µM) or malaria-associated levels of 5-HT (0.15 µM) on various aspects of A. stephensi biology. In these studies, we provisioned 5-HT and monitored fecundity, lifespan, flight behavior, and blood feeding of A. stephensi. We also assessed the impact of 5-HT ingestion on infection of A. stephensi with the mouse malaria parasite Plasmodium yoelii yoelii 17XNL and the human malaria parasite Plasmodium falciparum. Our data show that ingestion of 5-HT associated with severe malaria increased mosquito flight velocity and investigation of visual objects in response to host odor (CO2). 5-HT ingestion in blood at levels associated with severe malaria also increased the tendency to take a second blood meal 4 days later in uninfected A. stephensi. In mosquitoes infected with P. y. yoelii 17XNL, feeding tendency was decreased when midgut oocysts were present but increased when sporozoites were present. In addition to these effects, treatment of A. stephensi with 5-HT associated with severe malaria increased infection success with P. y. yoelii 17XNL compared to control, while treatment with healthy levels of 5-HT decreased infection success with P. falciparum. These changes in mosquito behavior and infection success could be used as a basis to manipulate 5-HT signaling in vector mosquitoes for improved control of malaria parasite transmission.

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“…Using our 5-HT1.0 sensor, we measured 5-HT release in specific compartments in the MB γ lobe in response to odor application (CS) and electric shock (US), which is regulated by local ACh release from KCs. Each hemisphere contains at least three serotonergic neurons that project to the MB, the DPM neuron innervates all lobes and the peduncle, the serotonergic projection neuron (SPN) innervates only the peduncle (Scheunemann et al, 2018), and the contralaterally-projecting serotonin-immunoreactive deuterocerebral interneuron (CSDn) innervates the calyx (Coates et al, 2020; Coates et al, 2017; Dacks et al, 2006; Suzuki et al, 2020; Zhang et al, 2019a). However, our finding that the physiological stimulation-evoked increase in 5-HT1.0 fluorescence in the γ lobe disappeared when the DPM neuron was silenced suggests that the DPM neuron is the principal source of 5-HT release in the γ lobe.…”

Section: Discussionmentioning

confidence: 99%

“…Both receptor subtypes are coupled to the inhibitory Gαi pathway (Saudou et al, 1992). Therefore, to determine which 5-HT receptor subtype mediated inhibitory 5-HT signaling to KCs, we applied 5-HT receptor subtype specific antagonists (Suzuki et al, 2020) and found that blocking the 5-HT1a receptor with WAY100635 prevented the optogenetically induced decrease of tonic ACh signaling. In contrast, blocking the 5-HT1b, 5-HT2a, or 5-HT2b receptor had no such effects (Figures 4J-4L).…”

Section: The Dpm Neuron Provides Inhibitory Feedback To the Kcsmentioning

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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A Population of Interneurons Signals Changes in the Basal Concentration of Serotonin and Mediates Gain Control in the Drosophila Antennal Lobe

Cited by 19 publications

References 51 publications

Social experience and pheromone receptor activity reprogram behavioral switch and neuromodulatory gene expression in sensory neurons

Social experience and pheromone receptor activity reprogram behavioral switch and neuromodulatory gene expression in sensory neurons

Anopheles stephensi Feeding, Flight Behavior, and Infection With Malaria Parasites are Altered by Ingestion of Serotonin

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

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