Synaptic placement reflects shared input in Drosophila descending neurons

Abstract

Network topology describes connections between neurons, whereas synaptic placement specifies how those connections are arranged within individual cells. How these levels of organization correspond remains incompletely understood. Here we show that connectivity between presynaptic neurons is reflected in relative input placement within Drosophila descending neurons (DNs). Across thousands of one-way DN connections in the independently reconstructed MaleCNS and FlyWire brains, inputs from sources also contacting the partner DN lay on average 9.4 and 8.0 μm nearer that partner's inputs along the receiver's neurites than other non-DN inputs. The same ordering held when source-input positions were fixed and partners with and without recorded source input were compared after standardizing reference-set size. In BANC and MaleCNS, shared input and measured spatial overlap provided complementary predictive information about DN interconnection. Two interconnected DNs sharing an ascending source differed in their identified cord outputs. Together, these findings link a three-neuron topological relationship to relative input placement, revealing a correspondence between network connectivity and the internal spatial organization of a receiving neuron.