Linear Summation Underlies Direction Selectivity in Drosophila

Abstract

While linear mechanisms lay the foundations of feature selectivity in many brain areas, direction selectivity in the elementary motion detector (EMD) of the fly has become a paradigm of nonlinear neuronal computation. We have bridged this divide by demonstrating that linear spatial summation can generate direction selectivity in the fruit fly Drosophila. Using linear systems analysis and two-photon imaging of a genetically encoded voltage indicator, we measure the emergence of direction-selective (DS) voltage signals in the Drosophila OFF pathway. Our study is a direct, quantitative investigation of the algorithm underlying directional signals, with the striking finding that linear spatial summation is sufficient for the emergence of direction selectivity. A linear stage of the fly EMD strongly resembles similar computations in vertebrate visual cortex, demands a reappraisal of the role of upstream nonlinearities, and implicates the voltage-to-calcium transformation in the refinement of feature selectivity in this system. VIDEO ABSTRACT.

Keywords: Drosophila; direction selectivity; feature selectivity; linear filtering; motion processing; neural computation; sensory processing; two-photon imaging; vision; voltage imaging.