Article

Simple integration of fast excitation and offset, delayed inhibition computes directional selectivity in Drosophila

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Abstract

A neuron that extracts directionally selective motion information from upstream signals lacking this selectivity must compare visual responses from spatially offset inputs. Distinguishing among prevailing algorithmic models for this computation requires measuring fast neuronal activity and inhibition. In the Drosophila melanogaster visual system, a fourth-order neuron—T4—is the first cell type in the ON pathway to exhibit directionally selective signals. Here we use in vivo whole-cell recordings of T4 to show that directional selectivity originates from simple integration of spatially offset fast excitatory and slow inhibitory inputs, resulting in a suppression of responses to the nonpreferred motion direction. We constructed a passive, conductance-based model of a T4 cell that accurately predicts the neuron’s response to moving stimuli. These results connect the known circuit anatomy of the motion pathway to the algorithmic mechanism by which the direction of motion is computed.

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Acknowledgements

We thank A. Nern for providing the driver line and image, K. Shinomiya and Janelia’s FlyEM project team for providing the reconstructed T4 cell morphology, M. Cembrowski for assistance with the NEURON simulations and E. Rogers for help with fly husbandry. We are also grateful to A. Hermundstad, J. Dudman, N. Spruston, B. Mensh and members of the Reiser lab for comments on the manuscript. This project was supported by the Howard Hughes Medical Institute.

Author information

Affiliations

  1. Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA

    • Eyal Gruntman
    • , Sandro Romani
    •  & Michael B. Reiser

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Contributions

E.G. and M.B.R. designed experiments; E.G. performed experiments and analysis. E.G. and S.R. conducted the simulation study. E.G. and M.B.R. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Michael B. Reiser.

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Supplementary information