Abstract
In both vertebrates and invertebrates, photoreceptors’ output is regulated by feedback signals from interneurons that contribute to several important visual functions. Although synaptic feedback regulation of photoreceptors is known to occur in Drosophila, many questions about the underlying molecular mechanisms and physiological implementation remain unclear. Here, we systematically investigated these questions using a broad range of experimental methods. We isolated two Ih mutant fly lines that exhibit rhythmic photoreceptor depolarization without light stimulation. We discovered that Ih channels regulate glutamate release from amacrine cells by modulating calcium channel activity. Moreover, we showed that the eye-enriched kainate receptor (EKAR) is expressed in photoreceptors and receives the glutamate signal released from amacrine cells. Finally, we presented evidence that amacrine cell feedback regulation helps maintain light sensitivity in ambient light. Our findings suggest plausible molecular underpinnings and physiological effects of feedback regulation from amacrine cells to photoreceptors. These results provide new mechanistic insight into how synaptic feedback regulation can participate in network processing by modulating neural information transfer and circuit excitability.
Highlights
Feedback regulation is common in neural circuit information processing
Feedback regulation is a common feature of neural circuits during the process of acquiring information
Using the primary visual system of the fruit fly Drosophila melanogaster as a model, we systematically investigated the molecular mechanisms and the physiological implementation of feedback regulation from amacrine cells to photoreceptors
Summary
Feedback regulation is common in neural circuit information processing. In both vertebrate and invertebrate visual systems, photoreceptor output is feedback-regulated by interneurons, which is an important mechanism for shaping the transmission of light information [1,2]. Serial electron-micrograph (EM) studies have revealed that outer photoreceptor (R1–R6) axons project their outputs to L1–L3 monopolar cells and amacrine cells (AC) and receive synaptic inputs from L2, L4, AC, Lawf, and C3 cells [6,7,8]. Because connectivity in the Drosophila lamina has been elucidated to the level of individual synapses, this system provides a good model to study how the feedback neural circuit works and facilitates network information processing [6,7,9,10]
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