A quantitative description of macaque ganglion cell responses to natural scenes: the interplay of time and space
Key points Responses to natural scenes are the business of the retina. We find primate ganglion cell responses to such scenes consistent with those to simpler stimuli. A biophysical model confirmed this and predicted ganglion cell responses with close to retinal reliability. Primate ganglion cell re...
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Veröffentlicht in: | The Journal of physiology 2021-06, Vol.599 (12), p.3169-3193 |
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description | Key points
Responses to natural scenes are the business of the retina. We find primate ganglion cell responses to such scenes consistent with those to simpler stimuli. A biophysical model confirmed this and predicted ganglion cell responses with close to retinal reliability.
Primate ganglion cell responses to natural scenes were driven by temporal variations in colour and luminance over the receptive field centre caused by eye movements, and little influenced by interaction of centre and surround with structure in the scene.
We discuss implications in the context of efficient coding of the visual environment. Much information in a higher spatiotemporal frequency band is concentrated in the magnocellular pathway.
Responses of visual neurons to natural scenes provide a link between classical descriptions of receptive field structure and visual perception of the natural environment. A natural scene video with a movement pattern resembling that of primate eye movements was used to evoke responses from macaque ganglion cells. Cell responses were well described through known properties of cell receptive fields. Different analyses converge to show that responses primarily derive from the temporal pattern of stimulation derived from eye movements, rather than spatial receptive field structure beyond centre size and position. This was confirmed using a model that predicted ganglion cell responses close to retinal reliability, with only a small contribution of the surround relative to the centre. We also found that the spatiotemporal spectrum of the stimulus is modified in ganglion cell responses, and this can reduce redundancy in the retinal signal. This is more pronounced in the magnocellular pathway, which is much better suited to transmit the detailed structure of natural scenes than the parvocellular pathway. Whitening is less important for chromatic channels. Taken together, this shows how a complex interplay across space, time and spectral content sculpts ganglion cell responses.
Key points
Responses to natural scenes are the business of the retina. We find primate ganglion cell responses to such scenes consistent with those to simpler stimuli. A biophysical model confirmed this and predicted ganglion cell responses with close to retinal reliability.
Primate ganglion cell responses to natural scenes were driven by temporal variations in colour and luminance over the receptive field centre caused by eye movements, and little influenced by interaction of centre |
doi_str_mv | 10.1113/JP281200 |
format | Article |
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Responses to natural scenes are the business of the retina. We find primate ganglion cell responses to such scenes consistent with those to simpler stimuli. A biophysical model confirmed this and predicted ganglion cell responses with close to retinal reliability.
Primate ganglion cell responses to natural scenes were driven by temporal variations in colour and luminance over the receptive field centre caused by eye movements, and little influenced by interaction of centre and surround with structure in the scene.
We discuss implications in the context of efficient coding of the visual environment. Much information in a higher spatiotemporal frequency band is concentrated in the magnocellular pathway.
Responses of visual neurons to natural scenes provide a link between classical descriptions of receptive field structure and visual perception of the natural environment. A natural scene video with a movement pattern resembling that of primate eye movements was used to evoke responses from macaque ganglion cells. Cell responses were well described through known properties of cell receptive fields. Different analyses converge to show that responses primarily derive from the temporal pattern of stimulation derived from eye movements, rather than spatial receptive field structure beyond centre size and position. This was confirmed using a model that predicted ganglion cell responses close to retinal reliability, with only a small contribution of the surround relative to the centre. We also found that the spatiotemporal spectrum of the stimulus is modified in ganglion cell responses, and this can reduce redundancy in the retinal signal. This is more pronounced in the magnocellular pathway, which is much better suited to transmit the detailed structure of natural scenes than the parvocellular pathway. Whitening is less important for chromatic channels. Taken together, this shows how a complex interplay across space, time and spectral content sculpts ganglion cell responses.
Key points
Responses to natural scenes are the business of the retina. We find primate ganglion cell responses to such scenes consistent with those to simpler stimuli. A biophysical model confirmed this and predicted ganglion cell responses with close to retinal reliability.
Primate ganglion cell responses to natural scenes were driven by temporal variations in colour and luminance over the receptive field centre caused by eye movements, and little influenced by interaction of centre and surround with structure in the scene.
We discuss implications in the context of efficient coding of the visual environment. Much information in a higher spatiotemporal frequency band is concentrated in the magnocellular pathway.</description><identifier>ISSN: 0022-3751</identifier><identifier>EISSN: 1469-7793</identifier><identifier>DOI: 10.1113/JP281200</identifier><identifier>PMID: 33913164</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Animals ; Eye movements ; Ganglion cells ; Macaca ; natural scenes ; Neurons ; Photic Stimulation ; primate vision ; Receptive field ; Reproducibility of Results ; Retina ; retinal ganglion cells ; Visual Fields ; Visual perception</subject><ispartof>The Journal of physiology, 2021-06, Vol.599 (12), p.3169-3193</ispartof><rights>2021 The Authors. The Journal of Physiology © 2021 The Physiological Society</rights><rights>2021 The Authors. The Journal of Physiology © 2021 The Physiological Society.</rights><rights>Journal compilation © 2021 The Physiological Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4396-41b0772f6033da03179492012af098d9f35f5cccada2e39db33d060ace299dbf3</citedby><cites>FETCH-LOGICAL-c4396-41b0772f6033da03179492012af098d9f35f5cccada2e39db33d060ace299dbf3</cites><orcidid>0000-0002-5468-4255 ; 0000-0002-0100-5351</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8998785/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8998785/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,1411,1427,27903,27904,45553,45554,46387,46811,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33913164$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Schottdorf, Manuel</creatorcontrib><creatorcontrib>Lee, Barry B.</creatorcontrib><title>A quantitative description of macaque ganglion cell responses to natural scenes: the interplay of time and space</title><title>The Journal of physiology</title><addtitle>J Physiol</addtitle><description>Key points
Responses to natural scenes are the business of the retina. We find primate ganglion cell responses to such scenes consistent with those to simpler stimuli. A biophysical model confirmed this and predicted ganglion cell responses with close to retinal reliability.
Primate ganglion cell responses to natural scenes were driven by temporal variations in colour and luminance over the receptive field centre caused by eye movements, and little influenced by interaction of centre and surround with structure in the scene.
We discuss implications in the context of efficient coding of the visual environment. Much information in a higher spatiotemporal frequency band is concentrated in the magnocellular pathway.
Responses of visual neurons to natural scenes provide a link between classical descriptions of receptive field structure and visual perception of the natural environment. A natural scene video with a movement pattern resembling that of primate eye movements was used to evoke responses from macaque ganglion cells. Cell responses were well described through known properties of cell receptive fields. Different analyses converge to show that responses primarily derive from the temporal pattern of stimulation derived from eye movements, rather than spatial receptive field structure beyond centre size and position. This was confirmed using a model that predicted ganglion cell responses close to retinal reliability, with only a small contribution of the surround relative to the centre. We also found that the spatiotemporal spectrum of the stimulus is modified in ganglion cell responses, and this can reduce redundancy in the retinal signal. This is more pronounced in the magnocellular pathway, which is much better suited to transmit the detailed structure of natural scenes than the parvocellular pathway. Whitening is less important for chromatic channels. Taken together, this shows how a complex interplay across space, time and spectral content sculpts ganglion cell responses.
Key points
Responses to natural scenes are the business of the retina. We find primate ganglion cell responses to such scenes consistent with those to simpler stimuli. A biophysical model confirmed this and predicted ganglion cell responses with close to retinal reliability.
Primate ganglion cell responses to natural scenes were driven by temporal variations in colour and luminance over the receptive field centre caused by eye movements, and little influenced by interaction of centre and surround with structure in the scene.
We discuss implications in the context of efficient coding of the visual environment. Much information in a higher spatiotemporal frequency band is concentrated in the magnocellular pathway.</description><subject>Animals</subject><subject>Eye movements</subject><subject>Ganglion cells</subject><subject>Macaca</subject><subject>natural scenes</subject><subject>Neurons</subject><subject>Photic Stimulation</subject><subject>primate vision</subject><subject>Receptive field</subject><subject>Reproducibility of Results</subject><subject>Retina</subject><subject>retinal ganglion cells</subject><subject>Visual Fields</subject><subject>Visual perception</subject><issn>0022-3751</issn><issn>1469-7793</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kk1rHSEUhqW0NDdpob-gCN10M4kfM-OcLgohJG1DoFmkaznXcW4MMzpRJ-X--3jJR9tA3Yj68Pgej4R84OyQcy6Pzi9FxwVjr8iK1y1USoF8TVaMCVFJ1fA9sp_SDWNcMoC3ZE9K4JK39YrMx_R2QZ9dxuzuLO1tMtHN2QVPw0AnNHi7WLpBvxl3e8aOI402zcEnm2gO1GNeIo40Gett-kLztaXOZxvnEbc7R3aTpeh7mmY09h15M-CY7PvH-YD8Oju9OvleXfz89uPk-KIytYS2qvmaKSWGlknZI5NcQQ2CcYEDg66HQTZDY4zBHoWV0K8LxlpWLhBQVoM8IF8fvPOynmxfwuWSUs_RTRi3OqDT_554d6034U53AJ3qmiL4_CiIoTxBynpyaVc-ehuWpEXDQQEIAQX99AK9CUv0pbxC1SWWKuOP0MSQUrTDcxjO9K6N-qmNBf34d_hn8KlvBTh8AH670W7_K9JX55flQ7StvAd5k6b_</recordid><startdate>20210601</startdate><enddate>20210601</enddate><creator>Schottdorf, Manuel</creator><creator>Lee, Barry B.</creator><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TS</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5468-4255</orcidid><orcidid>https://orcid.org/0000-0002-0100-5351</orcidid></search><sort><creationdate>20210601</creationdate><title>A quantitative description of macaque ganglion cell responses to natural scenes: the interplay of time and space</title><author>Schottdorf, Manuel ; Lee, Barry B.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4396-41b0772f6033da03179492012af098d9f35f5cccada2e39db33d060ace299dbf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Eye movements</topic><topic>Ganglion cells</topic><topic>Macaca</topic><topic>natural scenes</topic><topic>Neurons</topic><topic>Photic Stimulation</topic><topic>primate vision</topic><topic>Receptive field</topic><topic>Reproducibility of Results</topic><topic>Retina</topic><topic>retinal ganglion cells</topic><topic>Visual Fields</topic><topic>Visual perception</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Schottdorf, Manuel</creatorcontrib><creatorcontrib>Lee, Barry B.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Physical Education Index</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Schottdorf, Manuel</au><au>Lee, Barry B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A quantitative description of macaque ganglion cell responses to natural scenes: the interplay of time and space</atitle><jtitle>The Journal of physiology</jtitle><addtitle>J Physiol</addtitle><date>2021-06-01</date><risdate>2021</risdate><volume>599</volume><issue>12</issue><spage>3169</spage><epage>3193</epage><pages>3169-3193</pages><issn>0022-3751</issn><eissn>1469-7793</eissn><abstract>Key points
Responses to natural scenes are the business of the retina. We find primate ganglion cell responses to such scenes consistent with those to simpler stimuli. A biophysical model confirmed this and predicted ganglion cell responses with close to retinal reliability.
Primate ganglion cell responses to natural scenes were driven by temporal variations in colour and luminance over the receptive field centre caused by eye movements, and little influenced by interaction of centre and surround with structure in the scene.
We discuss implications in the context of efficient coding of the visual environment. Much information in a higher spatiotemporal frequency band is concentrated in the magnocellular pathway.
Responses of visual neurons to natural scenes provide a link between classical descriptions of receptive field structure and visual perception of the natural environment. A natural scene video with a movement pattern resembling that of primate eye movements was used to evoke responses from macaque ganglion cells. Cell responses were well described through known properties of cell receptive fields. Different analyses converge to show that responses primarily derive from the temporal pattern of stimulation derived from eye movements, rather than spatial receptive field structure beyond centre size and position. This was confirmed using a model that predicted ganglion cell responses close to retinal reliability, with only a small contribution of the surround relative to the centre. We also found that the spatiotemporal spectrum of the stimulus is modified in ganglion cell responses, and this can reduce redundancy in the retinal signal. This is more pronounced in the magnocellular pathway, which is much better suited to transmit the detailed structure of natural scenes than the parvocellular pathway. Whitening is less important for chromatic channels. Taken together, this shows how a complex interplay across space, time and spectral content sculpts ganglion cell responses.
Key points
Responses to natural scenes are the business of the retina. We find primate ganglion cell responses to such scenes consistent with those to simpler stimuli. A biophysical model confirmed this and predicted ganglion cell responses with close to retinal reliability.
Primate ganglion cell responses to natural scenes were driven by temporal variations in colour and luminance over the receptive field centre caused by eye movements, and little influenced by interaction of centre and surround with structure in the scene.
We discuss implications in the context of efficient coding of the visual environment. Much information in a higher spatiotemporal frequency band is concentrated in the magnocellular pathway.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>33913164</pmid><doi>10.1113/JP281200</doi><tpages>25</tpages><orcidid>https://orcid.org/0000-0002-5468-4255</orcidid><orcidid>https://orcid.org/0000-0002-0100-5351</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Eye movements Ganglion cells Macaca natural scenes Neurons Photic Stimulation primate vision Receptive field Reproducibility of Results Retina retinal ganglion cells Visual Fields Visual perception |
title | A quantitative description of macaque ganglion cell responses to natural scenes: the interplay of time and space |
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