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SummaryDetecting the direction of visual movement is fundamental for every sighted animal in order to navigate, avoid predators, or detect conspecifics. Algorithmic models of correlation-type motion detectors describe the underlying computation remarkably well [1–3]. They consist of two spatially separated input lines that are asymmetrically filtered in time and then interact in a nonlinear way. However, the cellular implementation of this computation remains elusive. Recent connectomic data of the Drosophila optic lobe has suggested a neural circuit for the detection of moving bright edges (ON motion) with medulla cells Mi1 and Tm3 providing spatially offset input to direction-selective T4 cells, thereby forming the two input lines of a motion detector [4]. Electrophysiological characterization of Mi1 and Tm3 revealed different temporal filtering properties and proposed them to correspond to the delayed and direct input, respectively [5]. Here, we test this hypothesis by silencing either Mi1 or Tm3 cells and using electrophysiological recordings and behavioral responses of flies as a readout. We show that Mi1 is a necessary element of the ON pathway under all stimulus conditions. In contrast, Tm3 is specifically required only for the detection of fast ON motion in the preferred direction. We thereby provide first functional evidence that Mi1 and Tm3 are key elements of the ON pathway and uncover an unexpected functional specialization of these two cell types. Our results thus require an elaboration of the currently prevailing model for ON motion detection [6, 7] and highlight the importance of functional studies for neural circuit breaking.