Anatomical distribution and functional roles of electrical synapses in Drosophila

• Published in: Current biology Vol. 32; no. 9; pp. 2022 - 2036.e4
• Main Authors: Ammer, Georg, Vieira, Renée M., Fendl, Sandra, Borst, Alexander
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 09-05-2022
• Subjects: electrical synapses, gap junctions, innexins, shakB, Drosophila, lobula plate tangential cells, LPTCs, VS/HS cells, oscillations, visual processing, motion vision; electrical synapses, gap junctions, innexins, shakB, Drosophila, lobula plate tangential cells, LPTCs, VS/HS cells, oscillations, visual processing, motion vision
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2022.03.040

Electrical synapses are present in almost all organisms that have a nervous system. However, their brain-wide expression patterns and the full range of contributions to neural function are unknown in most species. Here, we first provide a light-microscopic, immunohistochemistry-based anatomical map of all innexin gap junction proteins—the building blocks of electrical synapses—in the central nervous system of Drosophila melanogaster. Of those innexin types that are expressed in the nervous system, some localize to glial cells, whereas others are predominantly expressed in neurons, with shakB being the most widely expressed neuronal innexin. We then focus on the function of shakB in VS/HS cells—a class of visual projection neurons—thereby uncovering an unexpected role for electrical synapses. Removing shakB from these neurons leads to spontaneous, cell-autonomous voltage and calcium oscillations, demonstrating that electrical synapses are required for these cells’ intrinsic stability. Furthermore, we investigate the role of shakB-type electrical synapses in early visual processing. We find that the loss of shakB from the visual circuits upstream of VS/HS cells differentially impairs ON and OFF visual motion processing pathways but is not required for the computation of direction selectivity per se. Taken together, our study demonstrates that electrical synapses are widespread across the Drosophila nervous system and that they play essential roles in neuronal function and visual information processing.
•An immunohistochemistry-based map of innexin gap junctions in the Drosophila CNS•VS/HS cells are electrically coupled to large cell networks via shakB gap junctions•Loss of electrical synapses from VS/HS cells induces voltage and calcium oscillations•Electrical synapses play functional roles in both ON and OFF vision pathways
Ammer et al. first map the broad distribution of electrical synapses in the fly nervous system. Next, they find that electrical synapses are required for the intrinsic stability of VS/HS cells. Furthermore, electrical synapses play differential roles in ON and OFF visual pathways but are not necessary for the emergence of direction selectivity.