SUMMARY
Mapping neural circuits across defined synapses is essential for understanding brain function. Here we describe trans-Tango, a technique for anterograde transsynaptic circuit tracing and manipulation. At the core of trans-Tango is a synthetic signaling pathway that is introduced into all neurons in the animal. This pathway converts receptor activation at the cell-surface into reporter expression through site-specific proteolysis. Specific labeling is achieved by presenting a tethered ligand at the synapses of genetically defined neurons, thereby activating the pathway in their postsynaptic partners and providing genetic access to these neurons. We first validated trans-Tango in the Drosophila olfactory system and then implemented it in the gustatory system, where projections beyond the first-order receptor neurons are not fully characterized. We identified putative second-order neurons within the sweet circuit that include projection neurons targeting known neuromodulation centers in the brain. These experiments establish trans-Tango as a flexible platform for transsynaptic circuit analysis.
SUMMARYSweet and bitter compounds excite different sensory cells and drive opposing behaviors. It is commonly thought that the neural circuits linking taste sensation to behavior conform to a labeled-line architecture, but in Drosophila, evidence for labeled lines beyond first-order neurons is lacking. To address this, we devised trans-Tango(activity), a strategy for calcium imaging of second-order gustatory projection neurons based on trans-Tango, a genetic transsynaptic tracing technique. We found distinct projection neuron populations that respond to sweet and bitter tastants. However, the bitter-responsive population was also activated by water alone. We further discovered that bitter tastants evoke activity upon both stimulus onset and offset. Bitter offset responses are exhibited by both first- and second-order gustatory neurons, but these responses are distributed among multiple types of projection neurons in the second order. These findings suggest a more complex coding scheme for gustatory information than can be explained by a labeled line model.
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