Serotonergic modulation of visual neurons inDrosophila melanogaster

Abstract

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.

Internal state configures olfactory behavior and early sensory processing in Drosophila larvae

“…Because of the broad similarities in the antennal lobe circuitry of the larva and adult, we speculate that the adult antennal lobe may also be a locus of state-dependent modulation. Recent findings in the adult fly suggest that neuromodulatory feedback also conveys internal-state information from the higher brain to early visual processing layers (40)(41)(42). Thus, the mechanism that we have uncovered may reflect a general principle in the organization of diverse sensory processing systems.…”

Seasonal variations of serotonin in the visual system of an ant revealed by immunofluorescence and a machine learning approach

“…There, 5HT is involved in setting the day state [71] and can affect even the physical size of lamina monopolar cells [72]. In Drosophila melanogaster , direct modulation of calcium signals in lamina interneurons by serotonin has been demonstrated [70]. We have observed significant differences in SI between laminae of hibernating and active L. niger workers.…”

“…5HT is known to modulate neuronal responses of neurons in all three visual ganglia (lamina, medulla, lobula), but since in most studies serotonin had been bath-applied, the exact site of 5HT action is not clear. Indirect information about the sites of 5HT action can be derived from the distribution of serotonin receptors in all three optic lobe neuropils [70]. In the visual system of many insects, 5HT is involved in circadian rhythmicity, most conspicuously observed in the lamina.…”