Journal Article

Serotonergic modulation of visual neurons in Drosophila melanogaster

Hardcastle, Ben J., Sizemore, Tyler R., Dacks, Andrew M., Myers Gschweng, Katherine M., Arnold, Rebecca C., Frye, Mark A., Gao, Fuying, Sampson, Maureen M., Krantz, David E., Bonanno, Shivan L.

2020

Overview

Sensory systems rely on neuromodulators, such as serotonin, to provide flexibility for information processing as stimuli vary, such as light intensity throughout the day. Serotonergic neurons broadly innervate the optic ganglia of Drosophila melanogaster, a widely used model for studying vision. It remains unclear whether serotonin modulates the physiology of interneurons in the optic ganglia. To address this question, we first mapped 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. Serotonin receptor expression was found in several types of columnar cells in the lamina including 5-HT2B in lamina monopolar cell L2, required for spatiotemporal luminance contrast, 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 indicated that these receptors localize to layer M2 of the medulla, proximal to serotonergic boutons, suggesting that the medulla neuropil is the primary site of serotonergic regulation for these neurons. Exogenous serotonin increased basal intracellular calcium in L2 terminals in layer M2 and modestly decreased the duration of visually induced calcium transients in L2 neurons following repeated dark flashes, but otherwise did not alter the calcium transients. Flies without functional 5-HT2B failed to show an increase in basal calcium in response to serotonin. 5-HT2B mutants also failed to show a change in amplitude in their response to repeated light flashes but other calcium transient parameters were relatively unaffected. While we did not detect serotonin receptor expression in L1 neurons, they, like L2, underwent serotonin-induced changes in basal calcium, presumably via interactions with other cells. These data demonstrate that serotonin modulates the physiology of interneurons involved in early visual processing in Drosophila.

• Publisher: Public Library of Science,Public Library of Science (PLoS)
• Subject: Adaptation / Animals / Behavior / Biology / Biology and Life Sciences / Calcium (intracellular) / Circadian Rhythm - genetics / Drosophila / Drosophila melanogaster / Drosophila melanogaster - genetics / Drosophila Proteins - genetics / Funding / Ganglia / Geffen, David / Gene expression / Gene Expression Regulation - genetics / Genetic aspects / Information processing / Insects / Interneurons / Interneurons - metabolism / Light intensity / Medicine / Medicine and Health Sciences / Medulla / Medulla oblongata / Membrane Proteins - genetics / Morphology / Nerve Tissue Proteins - genetics / Neuromodulation / Neurons / Neuropil / Neurosciences / Neurotransmitter Agents - genetics / Photoreceptors / Physiological aspects / Physiology / Presynapse / Psychiatry / Receptor, Serotonin, 5-HT1B - genetics / Receptors, Serotonin - genetics / Receptors, Serotonin, 5-HT1 - genetics / Receptors, Serotonin, 5-HT2 - genetics / Research and Analysis Methods / Sensory neurons / Sensory systems / Serotonergic Neurons - metabolism / Serotonin / Serotonin - genetics / Serotonin - metabolism / Serotonin receptors / Serotonin S1 receptors / Serotonin S2 receptors / Serotoninergic mechanisms / Social Sciences / Supervision / Visual pathway / Visual Perception - genetics / Visual system