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The Retinal Basis of Light Aversion in Neonatal Mice

View ORCID ProfileFranklin S. Caval-Holme, View ORCID ProfileMarcos L. Aranda, Andy Quaen Chen, View ORCID ProfileAlexandre Tiriac, Yizhen Zhang, Benjamin Smith, View ORCID ProfileLutz Birnbaumer, View ORCID ProfileTiffany M. Schmidt, View ORCID ProfileMarla B. Feller
doi: https://doi.org/10.1101/2022.01.20.477130
Franklin S. Caval-Holme
1Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA 94720, USA
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  • ORCID record for Franklin S. Caval-Holme
Marcos L. Aranda
2Department of Neurobiology, Northwestern University, Evanston, IL, USA
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Andy Quaen Chen
3Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA
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Alexandre Tiriac
3Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA
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Yizhen Zhang
3Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA
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Benjamin Smith
4School of Optometry, University of California, Berkeley, Berkeley, CA 94720, USA
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Lutz Birnbaumer
5Signal Transduction Laboratory, National Institute of Environmental Health Sciences, National Institutes of Health, Durham, NC, USA; Institute of Biomedical Research (BIOMED), School of Medical Sciences, Catholic University of Argentina, Buenos Aires, Argentina
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Tiffany M. Schmidt
2Department of Neurobiology, Northwestern University, Evanston, IL, USA
6Department of Ophthalmology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA
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Marla B. Feller
1Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA 94720, USA
3Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA
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  • For correspondence: mfeller@berkeley.edu
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SUMMARY

Aversive responses to bright light (photoaversion) require signaling from the eye to the brain. Melanopsin-expressing intrinsically photosensitive retinal ganglion cells (ipRGCs) encode absolute light intensity and are thought to provide the light signals for photoaversion. Consistent with this, neonatal mice exhibit photoaversion prior to the developmental onset of image vision, and melanopsin deletion abolishes photoaversion in neonates. It is not well understood how the population of ipRGCs, which constitutes multiple physiologically distinct types (denoted M1-M6 in mouse) encodes light stimuli to produce an aversive response. Here, we provide several lines of evidence that M1 ipRGCs that lack the Brn3b transcription factor drive photoaversion in neonatal mice. First, neonatal mice lacking TRPC6 and TRPC7 ion channels failed to turn away from bright light, while two photon Ca2+ imaging of their acutely isolated retinas revealed reduced photosensitivity in M1 ipRGCs, but not other ipRGC types. Second, mice in which all ipRGC types except for Brn3b-negative M1 ipRGCs are ablated, exhibited normal photoaversion. Third, pharmacological blockade or genetic knockout of gap junction channels expressed by ipRGCs, which reduces the light sensitivity of M2-M6 ipRGCs in the neonatal retina, had small effects on photoaversion only at the brightest light intensities. Finally, M1s were not strongly depolarized by spontaneous retinal waves, a robust source of activity in the developing retina that depolarizes all other ipRGC types. M1s therefore constitute a separate information channel between the neonatal retina and brain that could ensure behavioral responses to light but not spontaneous retinal waves.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted January 22, 2022.
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The Retinal Basis of Light Aversion in Neonatal Mice
Franklin S. Caval-Holme, Marcos L. Aranda, Andy Quaen Chen, Alexandre Tiriac, Yizhen Zhang, Benjamin Smith, Lutz Birnbaumer, Tiffany M. Schmidt, Marla B. Feller
bioRxiv 2022.01.20.477130; doi: https://doi.org/10.1101/2022.01.20.477130
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The Retinal Basis of Light Aversion in Neonatal Mice
Franklin S. Caval-Holme, Marcos L. Aranda, Andy Quaen Chen, Alexandre Tiriac, Yizhen Zhang, Benjamin Smith, Lutz Birnbaumer, Tiffany M. Schmidt, Marla B. Feller
bioRxiv 2022.01.20.477130; doi: https://doi.org/10.1101/2022.01.20.477130

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