Abstract
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.
Highlights
Serotonin acts as a neuromodulator [1,2,3,4,5] in a variety of networks including the sensory systems required for olfaction, hearing, and vision [6,7,8,9,10,11,12,13,14,15,16,17]
Five genes encoding serotonin receptors have been identified in the Drosophila genome: 5-HT1A, 5-HT1B, 5-HT2A, 5-HT2B and 5-HT7 [72,73,74,75,76]
The GAL4 sequence is inserted into receptor-encoding genes where it acts as an artificial exon and is expected to “mimic” the endogenous gene expression patterns [78]
Summary
Serotonin acts as a neuromodulator [1,2,3,4,5] in a variety of networks including the sensory systems required for olfaction, hearing, and vision [6,7,8,9,10,11,12,13,14,15,16,17]. In the mammalian visual cortex, serotonin regulates the balance of excitation and inhibition [6], cellular plasticity [18,19,20,21], and response gain [8, 22]. For most sensory circuits, the manner in which serotonin receptor activation is integrated to regulate their activity and drive adaptive changes remains poorly understood. In Drosophila, early visual processing occurs in the lamina where intrinsic monopolar neurons receive direct input from photoreceptors [27]. Significant progress has been made in mapping the synaptic connectivity and function of visual processing neurons, including those required for motion detection [27,35,36,37,38,39,40]
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