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Connectomic Identification and Three-Dimensional Color Tuning of S-OFF Midget Ganglion Cells in the Primate Retina

Wool, LE; Packer, OS; Zaidi, Q; Dacey, DM; (2019) Connectomic Identification and Three-Dimensional Color Tuning of S-OFF Midget Ganglion Cells in the Primate Retina. Journal of Neuroscience , 39 (40) pp. 7893-7909. 10.1523/JNEUROSCI.0778-19.2019. Green open access

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Abstract

In the trichromatic primate retina, the “midget” retinal ganglion cell is the classical substrate for red–green color signaling, with a circuitry that enables antagonistic responses between long (L)- and medium (M)-wavelength-sensitive cone inputs. Previous physiological studies showed that some OFF midget ganglion cells may receive sparse input from short (S)-wavelength-sensitive cones, but the effect of S-cone inputs on the chromatic tuning properties of such cells has not been explored. Moreover, anatomical evidence for a synaptic pathway from S cones to OFF midget ganglion cells through OFF midget bipolar cells remains ambiguous. In this study, we address both questions for the macaque monkey retina. First, we used serial block-face electron microscopy to show that every S cone in the parafoveal retina synapses principally with a single OFF midget bipolar cell, which in turn forms a private-line connection with an OFF midget ganglion cell. Second, we used patch electrophysiology to characterize the chromatic tuning of OFF midget ganglion cells in the near peripheral retina that receive combined input from L, M, and S cones. These “S-OFF” midget cells have a characteristic S-cone spatial signature, but demonstrate heterogeneous color properties due to the variable strength of L, M, and S cone input across the receptive field. Together, these findings strongly support the hypothesis that the OFF midget pathway is the major conduit for S-OFF signals in primate retina and redefines the pathway as a chromatically complex substrate that encodes color signals beyond the classically recognized L versus M and S versus L+M cardinal mechanisms.

Type: Article
Title: Connectomic Identification and Three-Dimensional Color Tuning of S-OFF Midget Ganglion Cells in the Primate Retina
Location: United States
Open access status: An open access version is available from UCL Discovery
DOI: 10.1523/JNEUROSCI.0778-19.2019
Publisher version: https://doi.org/10.1523/JNEUROSCI.0778-19.2019
Language: English
Additional information: From six months after publication this work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
Keywords: color; connectome; midget pathway; primate; retina; vision
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology > Department of Neuromuscular Diseases
URI: https://discovery-pp.ucl.ac.uk/id/eprint/10084367
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