Evolution of neuronal cell classes and types in the vertebrate retina

Hahn, Joshua; Monavarfeshani, Aboozar; Qiao, Mu; Kao, Allison H.; Kölsch, Yvonne; Kumar, Ayush; Kunze, Vincent P.; Rasys, Ashley M.; Richardson, Rose; Wekselblatt, Joseph B.; Baier, Herwig; Lucas, Robert J.; Li, Wei; Meister, Markus; Trachtenberg, Joshua T.; Yan, Wenjun; Peng, Yi-Rong; Sanes, Joshua R.; Shekhar, Karthik

doi:10.1038/s41586-023-06638-9

Evolution of neuronal cell classes and types in the vertebrate retina

Journal Article · Wed Dec 13 00:00:00 EST 2023 · Nature (London)

DOI:https://doi.org/10.1038/s41586-023-06638-9· OSTI ID:2470883

^[1]; Monavarfeshani, Aboozar ^[2]; Qiao, Mu ^[3]; Kao, Allison H. ^[2]; Kölsch, Yvonne ^[4]; Kumar, Ayush ^[1]; ^[5]; Rasys, Ashley M. ^[6]; Richardson, Rose ^[7]; Wekselblatt, Joseph B. ^[3]; ^[4]; ^[7]; ^[5]; ^[3]; Trachtenberg, Joshua T. ^[8]; ^[2]; Peng, Yi-Rong ^[9]; ^[2]; ^[10]

University of California, Berkeley, CA (United States)
Harvard University, Cambridge, MA (United States)
California Institute of Technology, Pasadena, CA (United States)
Max Planck Institute for Biological Intelligence, Martinsried (Germany)
National Institutes of Health, Bethesda, MD (United States)
University of Georgia, Athens, GA (United States)
University of Manchester (United Kingdom)
David Geffen School of Medicine at UCLA, Los Angeles, CA (United States)
UCLA David Geffen School of Medicine, Los Angeles, CA (United States)
University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

The basic plan of the retina is conserved across vertebrates, yet species differ profoundly in their visual needs1. Retinal cell types may have evolved to accommodate these varied needs, but this has not been systematically studied. Here we generated and integrated single-cell transcriptomic atlases of the retina from 17 species: humans, two non-human primates, four rodents, three ungulates, opossum, ferret, tree shrew, a bird, a reptile, a teleost fish and a lamprey. We found high molecular conservation of the six retinal cell classes (photoreceptors, horizontal cells, bipolar cells, amacrine cells, retinal ganglion cells (RGCs) and Müller glia), with transcriptomic variation across species related to evolutionary distance. Major subclasses were also conserved, whereas variation among cell types within classes or subclasses was more pronounced. However, an integrative analysis revealed that numerous cell types are shared across species, based on conserved gene expression programmes that are likely to trace back to an early ancestral vertebrate. The degree of variation among cell types increased from the outer retina (photoreceptors) to the inner retina (RGCs), suggesting that evolution acts preferentially to shape the retinal output. Finally, we identified rodent orthologues of midget RGCs, which comprise more than 80% of RGCs in the human retina, subserve high-acuity vision, and were previously believed to be restricted to primates. By contrast, the mouse orthologues have large receptive fields and comprise around 2% of mouse RGCs. Projections of both primate and mouse orthologous types are overrepresented in the thalamus, which supplies the primary visual cortex. We suggest that midget RGCs are not primate innovations, but are descendants of evolutionarily ancient types that decreased in size and increased in number as primates evolved, thereby facilitating high visual acuity and increased cortical processing of visual information.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2470883

Journal Information:: Nature (London), Journal Name: Nature (London) Journal Issue: 7991 Vol. 624; ISSN 0028-0836

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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