Synaptic Specializations of Melanopsin-Retinal Ganglion Cells in Multiple Brain Regions Revealed by Genetic Label for Light and Electron Microscopy

Keun-Young Kim; Luis C. Rios; Hiep Le; Alex J. Perez; Sébastien Phan; Eric A. Bushong; Thomas J. Deerinck; Yu Hsin Liu; Maya A. Ellisman; Varda Lev-Ram; Suyeon Ju; Sneha A. Panda; Sanghee Yoon; Masatoshi Hirayama; Ludovic S. Mure; Megumi Hatori; Mark H. Ellisman; Satchidananda Panda

Cell Reports (Oct 2019)

Synaptic Specializations of Melanopsin-Retinal Ganglion Cells in Multiple Brain Regions Revealed by Genetic Label for Light and Electron Microscopy

Keun-Young Kim,
Luis C. Rios,
Hiep Le,
Alex J. Perez,
Sébastien Phan,
Eric A. Bushong,
Thomas J. Deerinck,
Yu Hsin Liu,
Maya A. Ellisman,
Varda Lev-Ram,
Suyeon Ju,
Sneha A. Panda,
Sanghee Yoon,
Masatoshi Hirayama,
Ludovic S. Mure,
Megumi Hatori,
Mark H. Ellisman,
Satchidananda Panda

Affiliations

Keun-Young Kim: Department of Neurosciences, University of California at San Diego School of Medicine, La Jolla, CA, USA; National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, CA, USA
Luis C. Rios: Salk Institute for Biological Studies, La Jolla, CA, USA
Hiep Le: Salk Institute for Biological Studies, La Jolla, CA, USA
Alex J. Perez: National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, CA, USA
Sébastien Phan: Department of Neurosciences, University of California at San Diego School of Medicine, La Jolla, CA, USA; National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, CA, USA
Eric A. Bushong: Department of Neurosciences, University of California at San Diego School of Medicine, La Jolla, CA, USA; National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, CA, USA
Thomas J. Deerinck: Department of Neurosciences, University of California at San Diego School of Medicine, La Jolla, CA, USA; National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, CA, USA
Yu Hsin Liu: Salk Institute for Biological Studies, La Jolla, CA, USA; Medical Scientist Training Program, University of California at San Diego School of Medicine, La Jolla, CA, USA
Maya A. Ellisman: Biological Sciences Graduate Training Program, Division of Biological Sciences, University of California, San Diego, La Jolla, CA, USA
Varda Lev-Ram: Department of Pharmacology, University of California, San Diego, La Jolla, CA, USA
Suyeon Ju: National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, CA, USA
Sneha A. Panda: National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, CA, USA
Sanghee Yoon: National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, CA, USA
Masatoshi Hirayama: Salk Institute for Biological Studies, La Jolla, CA, USA
Ludovic S. Mure: Salk Institute for Biological Studies, La Jolla, CA, USA
Megumi Hatori: Salk Institute for Biological Studies, La Jolla, CA, USA
Mark H. Ellisman: Department of Neurosciences, University of California at San Diego School of Medicine, La Jolla, CA, USA; National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, CA, USA; Department of Pharmacology, University of California, San Diego, La Jolla, CA, USA; Corresponding author
Satchidananda Panda: Salk Institute for Biological Studies, La Jolla, CA, USA; Corresponding author

Journal volume & issue: Vol. 29, no. 3
pp. 628 – 644.e6

Abstract

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Summary: The form and synaptic fine structure of melanopsin-expressing retinal ganglion cells, also called intrinsically photosensitive retinal ganglion cells (ipRGCs), were determined using a new membrane-targeted version of a genetic probe for correlated light and electron microscopy (CLEM). ipRGCs project to multiple brain regions, and because the method labels the entire neuron, it was possible to analyze nerve terminals in multiple retinorecipient brain regions, including the suprachiasmatic nucleus (SCN), olivary pretectal nucleus (OPN), and subregions of the lateral geniculate. Although ipRGCs provide the only direct retinal input to the OPN and SCN, ipRGC terminal arbors and boutons were found to be remarkably different in each target region. A network of dendro-dendritic chemical synapses (DDCSs) was also revealed in the SCN, with ipRGC axon terminals preferentially synapsing on the DDCS-linked cells. The methods developed to enable this analysis should propel other CLEM studies of long-distance brain circuits at high resolution. : Kim et al. express a genetically encoded electron microscopy (EM) tag in mRGCs of the mouse retina and use serial block-face electron microscopy to analyze the optic nerve and synaptic neuropil in five different brain regions. They find that mRGC synaptic terminals show target-specific specializations corresponding to differences in responses to light. Keywords: melanopsin, mRGC, ipRGC, circadian, SCN, OPN, miniSOG, serial blockface electron microscopy, LGN, IGL

Published in Cell Reports

ISSN: 2211-1247 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Science: Biology (General)
Website: http://www.cell.com/cell-reports/home

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