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Divergence of visual channels in the inner retina

Nature Neuroscience volume 15, pages 1581–1589 (2012)Cite this article

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Abstract

Bipolar cells form parallel channels that carry visual signals from the outer to the inner retina. Each type of bipolar cell is thought to carry a distinct visual message to select types of amacrine cells and ganglion cells. However, the number of ganglion cell types exceeds that of the bipolar cells providing their input, suggesting that bipolar cell signals diversify on transmission to ganglion cells. We explored in the salamander retina how signals from individual bipolar cells feed into multiple ganglion cells and found that each bipolar cell was able to evoke distinct responses among ganglion cells, differing in kinetics, adaptation and rectification properties. This signal divergence resulted primarily from interactions with amacrine cells that allowed each bipolar cell to send distinct signals to its target ganglion cells. Our findings indicate that individual bipolar cell–ganglion cell connections have distinct transfer functions. This expands the number of visual channels in the inner retina and enhances the computational power and feature selectivity of early visual processing.

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Figure 1: Many ganglion cells respond to input from a single bipolar cell.
Figure 2: Individual pairs of bipolar and ganglion cells have distinct transmission properties.
Figure 3: Dynamics of bipolar cell signals are diversified by amacrine circuits.
Figure 4: Interactions with amacrine cells can control the kinetics of connections between bipolar and ganglion cells.
Figure 5: Adaptation of bipolar cell signals depends on interaction with amacrine cells.
Figure 6: Adaptation is specific to individual pairs of bipolar and ganglion cells.
Figure 7: Rectifying and nonrectifying transmission from bipolar cells.
Figure 8: Amacrine cells can gate individual bipolar cell signals.

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Acknowledgements

We gratefully acknowledge E. Soucy for his extensive help with the experiments, as well as all of the members of the Meister laboratory for many useful discussions. This work was supported by a Postdoctoral Fellowship for Research Abroad from the Japan Society for the Promotion of Science (H.A.) and grants from the US National Institutes of Health (M.M.).

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  1. Hiroki Asari & Markus Meister

    Present address: Present address: Division of Biology, California Institute of Technology, Pasadena, California, USA.,

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  1. Department of Molecular and Cellular Biology and Center for Brain Science, Harvard University, Cambridge, Massachusetts, USA

    Hiroki Asari & Markus Meister

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H.A. and M.M. designed the study and wrote the manuscript. H.A. performed the experiments and analysis.

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Correspondence to Markus Meister.

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Asari, H., Meister, M. Divergence of visual channels in the inner retina. Nat Neurosci 15, 1581–1589 (2012). https://doi.org/10.1038/nn.3241

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