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Dendro-somatic synaptic inputs to ganglion cells violate receptive field and connectivity rules in the mammalian retina

Miloslav Sedlacek, William N. Grimes, Morgan Musgrove, View ORCID ProfileAmurta Nath, Hua Tian, View ORCID ProfileMrinalini Hoon, View ORCID ProfileFred Rieke, View ORCID ProfileJoshua H. Singer, View ORCID ProfileJeffrey S. Diamond
doi: https://doi.org/10.1101/2021.07.01.450751
Miloslav Sedlacek
1Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892
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William N. Grimes
1Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892
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Morgan Musgrove
1Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892
2Department of Biology, University of Maryland, College Park, MD 20742
3Program in Neuroscience and Cognitive Science, University of Maryland, College Park, MD 20742
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Amurta Nath
1Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892
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Hua Tian
1Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892
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Mrinalini Hoon
4Department of Ophthalmology and Visual Sciences, University of Wisconsin School of Medicine and Public Health, Madison, WI 53706
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Fred Rieke
5Department of Physiology and Biophysics, University of Washington, Seattle, WA 98195
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Joshua H. Singer
2Department of Biology, University of Maryland, College Park, MD 20742
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Jeffrey S. Diamond
1Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892
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  • For correspondence: diamondj@ninds.nih.gov
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Summary

In retinal neurons, morphology strongly influences visual response features. Ganglion cell (GC) dendrites ramify in distinct strata of the inner plexiform layer (IPL) so that GCs responding to light increments (ON) or decrements (OFF) receive appropriate excitatory inputs. This vertical stratification prescribes response polarity and ensures consistent connectivity between cell types, whereas the lateral extent of GC dendritic arbors typically dictates receptive field (RF) size. Here, we identify circuitry in mouse retina that contradicts these conventions. A2 amacrine cells are interneurons understood to mediate “cross-over” inhibition by relaying excitatory input from the ON layer to inhibitory outputs in the OFF layer. Ultrastructural and physiological analyses show, however, that some A2s deliver powerful inhibition to OFF GC somas and proximal dendrites in the ON layer, rendering their inhibitory RFs smaller than their dendritic arbors. This OFF pathway, avoiding entirely the OFF region of the IPL, challenges several tenets of retinal circuitry.

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. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license.
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Posted July 01, 2021.
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Dendro-somatic synaptic inputs to ganglion cells violate receptive field and connectivity rules in the mammalian retina
Miloslav Sedlacek, William N. Grimes, Morgan Musgrove, Amurta Nath, Hua Tian, Mrinalini Hoon, Fred Rieke, Joshua H. Singer, Jeffrey S. Diamond
bioRxiv 2021.07.01.450751; doi: https://doi.org/10.1101/2021.07.01.450751
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Dendro-somatic synaptic inputs to ganglion cells violate receptive field and connectivity rules in the mammalian retina
Miloslav Sedlacek, William N. Grimes, Morgan Musgrove, Amurta Nath, Hua Tian, Mrinalini Hoon, Fred Rieke, Joshua H. Singer, Jeffrey S. Diamond
bioRxiv 2021.07.01.450751; doi: https://doi.org/10.1101/2021.07.01.450751

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