A minimal synaptic model for direction selective neurons in Drosophila

Visual motion estimation is a canonical neural computation. In Drosophila, recent advances have identified anatomic and functional circuitry underlying direction-selective computations. Models with varying levels of abstraction have been proposed to explain specific experimental results but have rarely been compared across experiments. Here we use the wealth of available anatomical and physiological data to construct a minimal, biophysically inspired synaptic model for Drosophila’s first-order direction-selective T4 cells. We show how this model relates mathematically to classical models of motion detection, including the Hassenstein-Reichardt correlator model. We used numerical simulation to test how well this synaptic model could reproduce measurements of T4 cells across many datasets and stimulus modalities. These comparisons include responses to sinusoid gratings, to apparent motion stimuli, to stochastic stimuli, and to natural scenes. Without fine-tuning this model, it sufficed to reproduce many, but not all, response properties of T4 cells. Since this model is flexible and based on straightforward biophysical properties, it provides an extensible framework for developing a mechanistic understanding of T4 neural response properties. Moreover, it can be used to assess the sufficiency of simple biophysical mechanisms to describe features of the direction-selective computation and identify where our understanding must be improved.