The physiological basis for contrast opponency in motion computation in Drosophila

Giordano Ramos-Traslosheros,Marion Silies

doi:10.1038/s41467-021-24986-w

Giordano Ramos-Traslosheros, Marion Silies

Open Access

https://doi.org/10.1038/s41467-021-24986-w

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Abstract

In Drosophila, direction-selective neurons implement a mechanism of motion computation similar to cortical neurons, using contrast-opponent receptive fields with ON and OFF subfields. It is not clear how the presynaptic circuitry of direction-selective neurons in the OFF pathway supports this computation if all major inputs are OFF-rectified neurons. Here, we reveal the biological substrate for motion computation in the OFF pathway. Three interneurons, Tm2, Tm9 and CT1, provide information about ON stimuli to the OFF direction-selective neuron T5 across its receptive field, supporting a contrast-opponent receptive field organization. Consistent with its prominent role in motion detection, variability in Tm9 receptive field properties transfers to T5, and calcium decrements in Tm9 in response to ON stimuli persist across behavioral states, while spatial tuning is sharpened by active behavior. Together, our work shows how a key neuronal computation is implemented by its constituent neuronal circuit elements to ensure direction selectivity.

Highlights

In Drosophila, direction-selective neurons implement a mechanism of motion computation similar to cortical neurons, using contrast-opponent receptive fields with ON and OFF subfields
To test whether direction selectivity in T5 would benefit from yet uncharacterized ON inputs, we modeled responses to sine gratings moving in different directions by simulating the T5 dendrite as a passive cable that integrates inputs from the main presynaptic neuron types, Tm9, Tm1, Tm2, Tm4, and CT1
We sketched a minimal model that exposed the benefit of ON information to T5 and identified the ON inputs that provide the cellular basis to implement a mechanism for direction selectivity in the fly OFF motion pathway

Summary

Introduction

In Drosophila, direction-selective neurons implement a mechanism of motion computation similar to cortical neurons, using contrast-opponent receptive fields with ON and OFF subfields. It is not clear how the presynaptic circuitry of direction-selective neurons in the OFF pathway supports this computation if all major inputs are OFF-rectified neurons. These neurons are at least three synapses away from photoreceptors and receive inputs from distinct lamina and medulla interneurons of the ON and OFF pathways[10,11,12,13] Two models, and their variants, have been used to describe direction-selective calcium signals in T4/T510,14,15–17. Cortical simple-cell receptive fields have a push-pull structure, meaning that at each receptive field location, inversion of the contrast polarity evokes a response of the opposite polarity, e.g., where ON stimuli provide excitation, OFF stimuli provide inhibition[27,29]

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