Direction Selectivity in Drosophila Emerges from Preferred-Direction Enhancement and Null-Direction Suppression

Abstract

Across animal phyla, motion vision relies on neurons that respond preferentially to stimuli moving in one, preferred direction over the opposite, null direction. In the elementary motion detector of Drosophila, direction selectivity emerges in two neuron types, T4 and T5, but the computational algorithm underlying this selectivity remains unknown. We find that the receptive fields of both T4 and T5 exhibit spatiotemporally offset light-preferring and dark-preferring subfields, each obliquely oriented in spacetime. In a linear-nonlinear modeling framework, the spatiotemporal organization of the T5 receptive field predicts the activity of T5 in response to motion stimuli. These findings demonstrate that direction selectivity emerges from the enhancement of responses to motion in the preferred direction, as well as the suppression of responses to motion in the null direction. Thus, remarkably, T5 incorporates the essential algorithmic strategies used by the Hassenstein-Reichardt correlator and the Barlow-Levick detector. Our model for T5 also provides an algorithmic explanation for the selectivity of T5 for moving dark edges: our model captures all two-and three-point spacetime correlations relevant to motion in this stimulus class. More broadly, our findings reveal the contribution of input pathway visual processing, specifically centersurround, temporally biphasic receptive fields, to the generation of direction selectivity in T5. As the spatiotemporal receptive field of T5 in Drosophila is common to the simple cell in vertebrate visual cortex, our stimulus-response model of T5 will inform efforts in an experimentally tractable context to identify more detailed, mechanistic models of a prevalent computation.

The Neuronal Basis of an Illusory Motion Percept Is Explained by Decorrelation of Parallel Motion Pathways

“…T5 responses showed OFF-selective responses of similar width (Figure S2). These were narrower than the receptive fields previously found for T4 and T5 using stochastic noise stimuli [13, 30], possibly because the stronger stimulus used here recruited more inhibitory elements that sharpened the response. The time traces of the single bar responses at the receptive field center clearly segregated T4 and T5 (Figure 2B): T4 cells responded to single ON-contrast bars, whereas T5 cells responded to single OFF-contrast bars.…”

“…This provided us with functional access to 4 distinct cell types: T4 and T5 cells that responded to progressive or regressive motion [30]. We isolated neuropil signals (ROIs) corresponding to each T4 or T5 cell type based on the selectivity of these neurons for light or dark edges moving in progressive or regressive directions [13, 19, 30] (Figure S1, see STAR Methods). …”

“…In these stimuli, repeated every 30 degrees in space, a 5-degree-wide vertical bar flickered stochastically while flanked by white, black, or mean luminance bars (Figure 3A, stimulus plots ). Linear receptive fields previously extracted from T4 and T5 indicate that these cells respond to flicker [13, 30]. By flanking a flickering bar with a second bar of a specific contrast, the flicker becomes similar to apparent motion stimuli, but on a fast timescale.…”

“…This 1-dimensional natural scene eliminated spatial variation in the dimension perpendicular to the motion. While the lack of variation may have affected response amplitudes [48], these cells are relatively insensitive to spatial structure in the orientation perpendicular to the motion dimension [13]. Nonetheless, this stimulus retained edge-structure in the orientation preferred by these cells [49].…”

“…Likewise, the OFF-edge T5 neuron has been shown to hyperpolarize to ON-contrasts, indicating that it receives ON-contrast information [29]. Furthermore, linear receptive fields of T4 and T5 have both positive and negative lobes [13, 30], which are consistent with a functional integration of ON- and OFF-contrasts, but could also result from rectified inputs of a single polarity [30, 31]. Moreover, the responses to the four reverse-phi motion stimuli in Figure 1B appear to differentially associate with the ON- and OFF-edge selective motion pathways [11, 18].…”