A Single Pair of Serotonergic Neurons Counteracts Serotonergic Inhibition of Ethanol Attraction in Drosophila

Xu, Li; He, Jianzheng; Kaiser, Andrea; Gräber, Nikolaus; Schläger, Laura; Ritze, Yvonne; Scholz, Henrike

doi:10.1371/journal.pone.0167518

Cited by 32 publications

(40 citation statements)

References 46 publications

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“…Neuromodulation provides a means of functional reconfiguration of circuit activity in a fixed wiring diagram. Bidirectional modulation of behavioral output by serotonin has also been described in adult Drosophila behaviors (Xu et al, 2016).…”

Section: Innate Olfactory Preferences Depend On Feeding Statementioning

confidence: 94%

Internal state configures olfactory behavior and early sensory processing inDrosophilalarvae

Vogt

Zimmerman

Schlichting

et al. 2020

Preprint

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Animals can respond differently to a sensory cue when in different states. Here, we show that certain odors repel well-fed Drosophila larvae but attract food-deprived larvae and how feeding state flexibly alters neural processing in an early olfactory circuit, the antennal lobe, to determine the behavioral valence of a sensory cue. Odor valence is assigned by a neuronal architecture that controls a switch between two separate projection neuron output pathways that mediate opposite behavioral responses. A uniglomerular projection neuron pathway mediates odor attraction whereas a multiglomerular projection neuron pathway mediates odor repulsion. The serotonergic CSD neuron in the antennal lobe is a critical regulator of this neuronal and behavioral switch. CSD selects an appropriate behavior by shifting patterns of serotonergic modulation and glutamatergic inhibition onto each output pathway. The antennal lobe is a decision-making circuit for innate behavioral responses that uses feeding state to determine an odor's valence.

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Section: Innate Olfactory Preferences Depend On Feeding Statementioning

confidence: 94%

Internal state configures olfactory behavior and early sensory processing inDrosophilalarvae

Vogt

Zimmerman

Schlichting

et al. 2020

Preprint

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“…Specifically, we found that PN axons directly excite CSDn terminals in the LH in an odor specific manner while CSDn branches in the AL are inhibited. Previous studies have shown that the CSDn soma is also inhibited by odors and that stimulation of the CSDn has little impact on olfactory circuitry in the AL (30), despite the CSDn being critical for normal olfactory behavior (27,28). Our current study resolves this issue by suggesting instead that the CSDn modulates behavior by affecting odorprocessing in the LH (Fig.…”

Section: Multi-dendritic Processingmentioning

confidence: 50%

“…CSDns can be targeted genetically (26) and are critical for various olfactory behaviors involving appetitive (27) and pheromonal odorants, including cis-vaccenyl acetate (cVA) (28). The modulation of cVA-evoked behavioral responses is especially interesting because the CSDns are thought to participate in top-down modulation and to have their effects mainly in the first olfactory relay, the antennal lobe (AL) (24,28,29).…”

Section: Introductionmentioning

confidence: 99%

Regulation of modulatory cell activity across olfactory structures in Drosophila melanogaster

Zhang

Coates

Dacks

et al. 2019

Preprint

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SignificanceThe centrifugal innervation of neuronal circuits is ubiquitous across centralized nervous systems. Such inputs often arise from modulatory neurons that arborize broadly throughout the brain. How information is integrated in such cells and how release from their distant terminals is regulated remains largely unknown. We show that a serotonergic neuron that innervates multiple stages of odor processing in Drosophila has distinct activity throughout its neurites, including opposite polarity responses in first and second order olfactory neuropils. Disparate activity arises from local interactions within each target region. Our results show that such neurons exhibit dendritic computation rather than somatic integration alone, and that examining local interactions at release sites is critical for understanding centrifugal innervation. AbstractAll centralized nervous systems possess modulatory neurons that arborize broadly across multiple brain regions. Such modulatory systems are critical for proper sensory, motor, and cognitive processing. How single modulatory neurons integrate into circuits within their target destination remains largely unexplored due to difficulties in both labeling individual cells and imaging across distal parts of the CNS. Here, we take advantage of an identified modulatory neuron in Drosophila that arborizes in multiple olfactory neuropils. We demonstrate that this serotonergic neuron has opposing odor responses in its neurites of the antennal lobe and lateral horn, first and second order olfactory neuropils respectively. Specifically, processes of this neuron in the antennal lobe have responses that are inhibitory and odor-independent, while lateral horn responses are excitatory and odor-specific. The results show that widespread modulatory neurons may not function purely as integrate-and-fire cells, but rather their transmitter release is locally regulated based on neuropil. As nearly all vertebrate and invertebrate neurons are subject to synaptic inputs along their dendro-axonic axis, it is likely that our findings generalize across phylogeny and other broadly-projecting modulatory systems.

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“…Serotonin immunolabeling was observed in processes within all optic ganglia as well as 93 a cluster of 8-10 cell bodies in the accessory medulla ( Figure 1D, G). The cell bodies 94 correspond to cluster LP2 (or Cb1), previously shown to project into the medulla (Nässel, 1988;95 Valles et al, 1988;Xu et al, 2016). Many of the neuronal processes expressing serotonin receptor MiMIC-GAL4 driven GFP showed close apposition to serotonergic boutons ( Figure 1D…”

Section: Serotoninergic Circuitry In the Optic Lobe 73mentioning

confidence: 84%

Serotonergic modulation of visual neurons inDrosophila melanogaster

Gschweng

Sampson

Hardcastle

et al. 2019

Preprint

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Sensory systems rely on neuromodulators, such as serotonin, to provide flexibility for information processing in the face of a highly variable stimulus space. Serotonergic neurons broadly innervate the optic ganglia of Drosophila melanogaster, a widely used model for studying vision. The role for serotonergic signaling in the Drosophila optic lobe and the mechanisms by which serotonin regulates visual neurons remain unclear. Here we map the expression patterns of serotonin receptors in the visual system, focusing on a subset of cells with processes in the first optic ganglion, the lamina, and show that serotonin can modulate visual responses. Serotonin receptors are expressed in several types of columnar cells in the lamina including 5-HT2B in lamina monopolar cell L2, required for the initial steps of visual processing, and both 5-HT1A and 5-HT1B in T1 cells, whose function is unknown. Subcellular mapping with GFP-tagged 5-HT2B and 5-HT1A constructs indicates that these receptors localize to layer M2 of the medulla, proximal to serotonergic boutons, suggesting that the medulla is the primary site of serotonergic regulation for these neurons. Serotonin increases intracellular calcium in L2 terminals in layer M2 and alters the kinetics of visually induced calcium transients in L2 neurons following dark flashes. These effects were not observed in flies without a functional 5-HT2B, which displayed severe differences in the amplitude and kinetics of their calcium response to both dark and light flashes. While we did not detect serotonin receptor expression in L1 neurons, they also undergo serotonin-induced calcium changes, presumably via cell non-autonomous signaling pathways. We provide the first functional data showing a role for serotonergic neuromodulation of neurons required for initiating visual processing in Drosophila and establish a new platform for investigating the serotonergic neuromodulation of sensory networks.Author SummarySerotonergic neurons innervate the Drosophila melanogaster eye, but the function of serotonergic signaling is not known. We found that serotonin receptors are expressed in all neuropils of the optic lobe and identify specific neurons involved in visual information processing that express serotonin receptors. We then demonstrate that activation of these receptors can alter how visual information is processed. These are the first data suggesting a functional role for serotonergic signaling in Drosophila vision. This study contributes to the understanding of serotonin biology and modulation of sensory circuits.

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A Single Pair of Serotonergic Neurons Counteracts Serotonergic Inhibition of Ethanol Attraction in Drosophila

Cited by 32 publications

References 46 publications

Internal state configures olfactory behavior and early sensory processing inDrosophilalarvae

Internal state configures olfactory behavior and early sensory processing inDrosophilalarvae

Regulation of modulatory cell activity across olfactory structures in Drosophila melanogaster

Serotonergic modulation of visual neurons inDrosophila melanogaster

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