Hierarchical partner selection shapes rod-cone pathway specificity in the inner retina

Summary: Neurons form stereotyped microcircuits that underlie specific functions. In the vertebrate retina, the primary rod and cone pathways that convey dim and bright light signals, respectively, exhibit distinct wiring patterns. Rod and cone pathways are thought to be assembled separately during...

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Main Authors: Chi Zhang, Ayana Hellevik, Shunsuke Takeuchi, Rachel O. Wong
Format: Article
Language:English
Published: Elsevier 2022-09-01
Series:iScience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2589004222013049
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author Chi Zhang
Ayana Hellevik
Shunsuke Takeuchi
Rachel O. Wong
author_facet Chi Zhang
Ayana Hellevik
Shunsuke Takeuchi
Rachel O. Wong
author_sort Chi Zhang
collection DOAJ
description Summary: Neurons form stereotyped microcircuits that underlie specific functions. In the vertebrate retina, the primary rod and cone pathways that convey dim and bright light signals, respectively, exhibit distinct wiring patterns. Rod and cone pathways are thought to be assembled separately during development. However, using correlative fluorescence imaging and serial electron microscopy, we show here that cross-pathway interactions are involved to achieve pathway-specific connectivity within the inner retina. We found that A17 amacrine cells, a rod pathway-specific cellular component, heavily bias their synaptogenesis with rod bipolar cells (RBCs) but increase their connectivity with cone bipolar cells (CBCs) when RBCs are largely ablated. This cross-pathway synaptic plasticity occurs during synaptogenesis and is triggered even on partial loss of RBCs. Thus, A17 cells adopt a hierarchical approach in selecting postsynaptic partners from functionally distinct pathways (RBC>CBC), in which contact and/or synaptogenesis with preferred partners (RBCs) influences connectivity with less-preferred partners (CBCs).
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spelling doaj.art-7427e952087e4b70802b4abccaafb73d2022-12-22T03:12:29ZengElsevieriScience2589-00422022-09-01259105032Hierarchical partner selection shapes rod-cone pathway specificity in the inner retinaChi Zhang0Ayana Hellevik1Shunsuke Takeuchi2Rachel O. Wong3Department of Biological Structure, University of Washington, Seattle, WA 98195, USADepartment of Biological Structure, University of Washington, Seattle, WA 98195, USADepartment of Biological Sciences, University of Tokyo, Tokyo 113-0033, JapanDepartment of Biological Structure, University of Washington, Seattle, WA 98195, USA; Corresponding authorSummary: Neurons form stereotyped microcircuits that underlie specific functions. In the vertebrate retina, the primary rod and cone pathways that convey dim and bright light signals, respectively, exhibit distinct wiring patterns. Rod and cone pathways are thought to be assembled separately during development. However, using correlative fluorescence imaging and serial electron microscopy, we show here that cross-pathway interactions are involved to achieve pathway-specific connectivity within the inner retina. We found that A17 amacrine cells, a rod pathway-specific cellular component, heavily bias their synaptogenesis with rod bipolar cells (RBCs) but increase their connectivity with cone bipolar cells (CBCs) when RBCs are largely ablated. This cross-pathway synaptic plasticity occurs during synaptogenesis and is triggered even on partial loss of RBCs. Thus, A17 cells adopt a hierarchical approach in selecting postsynaptic partners from functionally distinct pathways (RBC>CBC), in which contact and/or synaptogenesis with preferred partners (RBCs) influences connectivity with less-preferred partners (CBCs).http://www.sciencedirect.com/science/article/pii/S2589004222013049Sensory neurosciencecell biologyexperimental systems for structural biology
spellingShingle Chi Zhang
Ayana Hellevik
Shunsuke Takeuchi
Rachel O. Wong
Hierarchical partner selection shapes rod-cone pathway specificity in the inner retina
iScience
Sensory neuroscience
cell biology
experimental systems for structural biology
title Hierarchical partner selection shapes rod-cone pathway specificity in the inner retina
title_full Hierarchical partner selection shapes rod-cone pathway specificity in the inner retina
title_fullStr Hierarchical partner selection shapes rod-cone pathway specificity in the inner retina
title_full_unstemmed Hierarchical partner selection shapes rod-cone pathway specificity in the inner retina
title_short Hierarchical partner selection shapes rod-cone pathway specificity in the inner retina
title_sort hierarchical partner selection shapes rod cone pathway specificity in the inner retina
topic Sensory neuroscience
cell biology
experimental systems for structural biology
url http://www.sciencedirect.com/science/article/pii/S2589004222013049
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AT shunsuketakeuchi hierarchicalpartnerselectionshapesrodconepathwayspecificityintheinnerretina
AT rachelowong hierarchicalpartnerselectionshapesrodconepathwayspecificityintheinnerretina