A common evolutionary origin for the ON- and OFF-edge motion detection pathways of the Drosophila visual system

Synaptic circuits for identified behaviors in the Drosophila brain have typically been considered from either a developmental or functional perspective without reference to how the circuits might have been inherited from ancestral forms. For example, two candidate pathways for ON- and OFF-edge motion detection in the visual system act via circuits that use respectively either T4 or T5, two cell types of the fourth neuropil, or lobula plate, that exhibit narrow-field direction-selective responses and provide input to wide-field tangential neurons. T4 or T5 both have four subtypes that terminate one each in the four strata of the lobula plate. Representatives are reported in a wide range of Diptera, and both cell types exhibit various similarities in: 1) the morphology of their dendritic arbors; 2) their four morphological and functional subtypes; 3) their cholinergic profile in Drosophila; 4) their input from the pathways of L3 cells in the first neuropil, or lamina, and by one of a pair of lamina cells, L1 (to the T4 pathway) and L2 (to the T5 pathway); and 5) their innervation by a single, wide-field contralateral tangential neuron from the central brain. Progenitors of both also express the gene atonal early in their proliferation from the inner anlage of the developing optic lobe, being alone among many other cell type progeny to do so. Yet T4 receives input in the second neuropil, or medulla, and T5 in the third neuropil or lobula. Here we suggest that these two cell types were originally one, that their ancestral cell population duplicated and split to innervate separate medulla and lobula neuropils, and that a fiber crossing – the internal chiasma – arose between the two neuropils. The split most plausibly occurred, we suggest, with the formation of the lobula as a new neuropil that formed when it separated from its ancestral neuropil to leave the medulla, suggesting additionally that medulla input neurons to T4 and T5 may also have had a common origin.