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      Birds multiplex spectral and temporal visual information via retinal On- and Off-channels

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          Abstract

          In vertebrate vision, early retinal circuits divide incoming visual information into functionally opposite elementary signals: On and Off, transient and sustained, chromatic and achromatic. Together these signals can yield an efficient representation of the scene for transmission to the brain via the optic nerve. However, this long-standing interpretation of retinal function is based on mammals, and it is unclear whether this functional arrangement is common to all vertebrates. Here we show that male poultry chicks use a fundamentally different strategy to communicate information from the eye to the brain. Rather than using functionally opposite pairs of retinal output channels, chicks encode the polarity, timing, and spectral composition of visual stimuli in a highly correlated manner: fast achromatic information is encoded by Off-circuits, and slow chromatic information overwhelmingly by On-circuits. Moreover, most retinal output channels combine On- and Off-circuits to simultaneously encode, or multiplex, both achromatic and chromatic information. Our results from birds conform to evidence from fish, amphibians, and reptiles which retain the full ancestral complement of four spectral types of cone photoreceptors.

          Abstract

          In mammals, the retina splits visual information into functionally opposite signals, but if this applies to birds is not known. Here, the authors show a different retinal functional organization in poultry chicks, where spectral and temporal information is multiplexed.

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          Some informational aspects of visual perception.

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            Parallel processing in the mammalian retina.

            Our eyes send different 'images' of the outside world to the brain - an image of contours (line drawing), a colour image (watercolour painting) or an image of moving objects (movie). This is commonly referred to as parallel processing, and starts as early as the first synapse of the retina, the cone pedicle. Here, the molecular composition of the transmitter receptors of the postsynaptic neurons defines which images are transferred to the inner retina. Within the second synaptic layer - the inner plexiform layer - circuits that involve complex inhibitory and excitatory interactions represent filters that select 'what the eye tells the brain'.
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              The functional diversity of retinal ganglion cells in the mouse

              SUMMARY In the vertebrate visual system, all output of the retina is carried by retinal ganglion cells. Each type encodes distinct visual features in parallel for transmission to the brain. How many such “output channels” exist and what each encodes is an area of intense debate. In mouse, anatomical estimates range between 15–20 channels, and only a handful are functionally understood. Combining two-photon calcium imaging to obtain dense retinal recordings and unsupervised clustering of the resulting sample of >11,000 cells, we here show that the mouse retina harbours substantially more than 30 functional output channels. These include all known and several new ganglion cell types, as verified by genetic and anatomical criteria. Therefore, information channels from the mouse’s eye to the mouse’s brain are considerably more diverse than shown thus far by anatomical studies, suggesting an encoding strategy resembling that used in state-of-the-art artificial vision systems.
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                Author and article information

                Contributors
                m.seifert@sussex.ac.uk
                d.osorio@sussex.ac.uk
                t.baden@sussex.ac.uk
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                31 August 2023
                31 August 2023
                2023
                : 14
                : 5308
                Affiliations
                [1 ]GRID grid.12082.39, ISNI 0000 0004 1936 7590, School of Life Sciences, , University of Sussex, ; Brighton, UK
                [2 ]GRID grid.10392.39, ISNI 0000 0001 2190 1447, Institute of Ophthalmic Research, , University of Tübingen, ; Tübingen, Germany
                Author information
                http://orcid.org/0000-0001-5293-6431
                http://orcid.org/0000-0002-5856-527X
                http://orcid.org/0000-0003-2808-4210
                Article
                41032
                10.1038/s41467-023-41032-z
                10471707
                37652912
                f547f663-bcc3-4e96-9adb-915fe6f467a2
                © Springer Nature Limited 2023

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 1 December 2022
                : 18 August 2023
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100000268, RCUK | Biotechnology and Biological Sciences Research Council (BBSRC);
                Award ID: BB/R014817/1 and BB/W013509/1
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100000275, Leverhulme Trust;
                Award ID: PLP-2017-005 and RPG-2021-026
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100001255, Lister Institute of Preventive Medicine;
                Award ID: Fellowship (no code)
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100010661, EC | Horizon 2020 Framework Programme (EU Framework Programme for Research and Innovation H2020);
                Award ID: 677687
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100004440, Wellcome Trust (Wellcome);
                Award ID: 220277/Z20/Z
                Award Recipient :
                Categories
                Article
                Custom metadata
                © Springer Nature Limited 2023

                Uncategorized
                retina,colour vision,evolution
                Uncategorized
                retina, colour vision, evolution

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