Synaptic gradients transform object location to action

Mark Dombrovski, Martin Y. Peek, Jin-Yong Park, Andrea Vaccari, Marissa Sumathipala, Carmen Morrow, Patrick Breads, Arthur Zhao, Yerbol Z. Kurmangaliyev, Piero Sanfilippo, Aadil Rehan, Jason Polsky, Shada Alghailani, Emily Tenshaw, Shigehiro Namiki, S. Lawrence Zipursky () and Gwyneth M. Card ()
Additional contact information
Mark Dombrovski: University of California, Los Angeles
Martin Y. Peek: Howard Hughes Medical Institute
Jin-Yong Park: Howard Hughes Medical Institute
Andrea Vaccari: Middlebury College
Marissa Sumathipala: Howard Hughes Medical Institute
Carmen Morrow: Howard Hughes Medical Institute
Patrick Breads: Howard Hughes Medical Institute
Arthur Zhao: Howard Hughes Medical Institute
Yerbol Z. Kurmangaliyev: University of California, Los Angeles
Piero Sanfilippo: University of California, Los Angeles
Aadil Rehan: University of California, Los Angeles
Jason Polsky: Howard Hughes Medical Institute
Shada Alghailani: Howard Hughes Medical Institute
Emily Tenshaw: Howard Hughes Medical Institute
Shigehiro Namiki: Howard Hughes Medical Institute
S. Lawrence Zipursky: University of California, Los Angeles
Gwyneth M. Card: Howard Hughes Medical Institute

Nature, 2023, vol. 613, issue 7944, 534-542

Abstract: Abstract To survive, animals must convert sensory information into appropriate behaviours1,2. Vision is a common sense for locating ethologically relevant stimuli and guiding motor responses3–5. How circuitry converts object location in retinal coordinates to movement direction in body coordinates remains largely unknown. Here we show through behaviour, physiology, anatomy and connectomics in Drosophila that visuomotor transformation occurs by conversion of topographic maps formed by the dendrites of feature-detecting visual projection neurons (VPNs)6,7 into synaptic weight gradients of VPN outputs onto central brain neurons. We demonstrate how this gradient motif transforms the anteroposterior location of a visual looming stimulus into the fly’s directional escape. Specifically, we discover that two neurons postsynaptic to a looming-responsive VPN type promote opposite takeoff directions. Opposite synaptic weight gradients onto these neurons from looming VPNs in different visual field regions convert localized looming threats into correctly oriented escapes. For a second looming-responsive VPN type, we demonstrate graded responses along the dorsoventral axis. We show that this synaptic gradient motif generalizes across all 20 primary VPN cell types and most often arises without VPN axon topography. Synaptic gradients may thus be a general mechanism for conveying spatial features of sensory information into directed motor outputs.

Date: 2023
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DOI: 10.1038/s41586-022-05562-8

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