Synaptic circuits and their variations within different columns in the visual system of Drosophila

Significance Circuit diagrams of brains are generally reported only as absolute or consensus networks; these diagrams fail to identify the accuracy of connections, however, for which multiple circuits of the same neurons must be documented. For this reason, the modular composition of the Drosophila visual system, with many identified neuron classes, is ideal. Using EM, we identified synaptic connections in the fly’s second visual relay neuropil, or medulla, in the 20 neuron classes in a so-called “core connectome,” those neurons present in seven neighboring columns. These connections identify circuits for motion. Their error rates for wiring reveal that <1% of contacts overall are not part of a consensus circuit but incorporate errors of either omission or commission. Autapses are occasionally seen. We reconstructed the synaptic circuits of seven columns in the second neuropil or medulla behind the fly’s compound eye. These neurons embody some of the most stereotyped circuits in one of the most miniaturized of animal brains. The reconstructions allow us, for the first time to our knowledge, to study variations between circuits in the medulla’s neighboring columns. This variation in the number of synapses and the types of their synaptic partners has previously been little addressed because methods that visualize multiple circuits have not resolved detailed connections, and existing connectomic studies, which can see such connections, have not so far examined multiple reconstructions of the same circuit. Here, we address the omission by comparing the circuits common to all seven columns to assess variation in their connection strengths and the resultant rates of several different and distinct types of connection error. Error rates reveal that, overall, <1% of contacts are not part of a consensus circuit, and we classify those contacts that supplement (E+) or are missing from it (E−). Autapses, in which the same cell is both presynaptic and postsynaptic at the same synapse, are occasionally seen; two cells in particular, Dm9 and Mi1, form ≥20-fold more autapses than do other neurons. These results delimit the accuracy of developmental events that establish and normally maintain synaptic circuits with such precision, and thereby address the operation of such circuits. They also establish a precedent for error rates that will be required in the new science of connectomics.