Origins of direction selectivity in the primate retina

Yeon Jin Kim, Beth B. Peterson, Joanna D. Crook, Hannah R. Joo, Jiajia Wu, Christian Puller, Farrel R. Robinson, Paul D. Gamlin, King-Wai Yau, Felix Viana, John B. Troy, Robert G. Smith, Orin S. Packer, Peter B. Detwiler and Dennis M. Dacey ()
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Yeon Jin Kim: University of Washington
Beth B. Peterson: University of Washington
Joanna D. Crook: University of Washington
Hannah R. Joo: University of Washington
Jiajia Wu: Northwestern University
Christian Puller: University of Washington
Farrel R. Robinson: University of Washington
Paul D. Gamlin: University of Alabama at Birmingham
King-Wai Yau: Johns Hopkins University School of Medicine
Felix Viana: Institute of Neuroscience, UMH-CSIC
John B. Troy: Northwestern University
Robert G. Smith: University of Pennsylvania
Orin S. Packer: University of Washington
Peter B. Detwiler: University of Washington
Dennis M. Dacey: University of Washington

Nature Communications, 2022, vol. 13, issue 1, 1-20

Abstract: Abstract From mouse to primate, there is a striking discontinuity in our current understanding of the neural coding of motion direction. In non-primate mammals, directionally selective cell types and circuits are a signature feature of the retina, situated at the earliest stage of the visual process. In primates, by contrast, direction selectivity is a hallmark of motion processing areas in visual cortex, but has not been found in the retina, despite significant effort. Here we combined functional recordings of light-evoked responses and connectomic reconstruction to identify diverse direction-selective cell types in the macaque monkey retina with distinctive physiological properties and synaptic motifs. This circuitry includes an ON-OFF ganglion cell type, a spiking, ON-OFF polyaxonal amacrine cell and the starburst amacrine cell, all of which show direction selectivity. Moreover, we discovered that macaque starburst cells possess a strong, non-GABAergic, antagonistic surround mediated by input from excitatory bipolar cells that is critical for the generation of radial motion sensitivity in these cells. Our findings open a door to investigation of a precortical circuitry that computes motion direction in the primate visual system.

Date: 2022
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DOI: 10.1038/s41467-022-30405-5

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