A new role for excitation in the retinal direction‐selective circuit
A key feature of the receptive field of neurons in the visual system is their centre–surround antagonism, whereby the centre and the surround exhibit responses of opposite polarity. This organization is thought to enhance visual acuity, but whether and how such antagonism plays a role in more comple...
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description | A key feature of the receptive field of neurons in the visual system is their centre–surround antagonism, whereby the centre and the surround exhibit responses of opposite polarity. This organization is thought to enhance visual acuity, but whether and how such antagonism plays a role in more complex processing remains poorly understood. Here, we investigate the role of centre and surround receptive fields in retinal direction selectivity by exposing posterior‐preferring On–Off direction‐selective ganglion cells (pDSGCs) to adaptive light and recording their response to globally moving objects. We reveal that light adaptation leads to surround expansion in pDSGCs. The pDSGCs maintain their original directional tuning in the centre receptive field, but present the oppositely tuned response in their surround. Notably, although inhibition is the main substrate for retinal direction selectivity, we found that following light adaptation, both the centre‐ and surround‐mediated responses originate from directionally tuned excitatory inputs. Multi‐electrode array recordings show similar oppositely tuned responses in other DSGC subtypes. Together, these data attribute a new role for excitation in the direction‐selective circuit. This excitation carries an antagonistic centre–surround property, possibly designed to sharpen the detection of motion direction in the retina.
Key points
Receptive fields of direction‐selective retinal ganglion cells expand asymmetrically following light adaptation.
The increase in the surround receptive field generates a delayed spiking phase that is tuned to the null direction and is mediated by excitation.
Following light adaptation, excitation rules the computation in the centre receptive field and is tuned to the preferred direction.
GABAergic and glycinergic inputs modulate the null‐tuned delayed response differentially.
Null‐tuned delayed spiking phases can be detected in all types of direction‐selective retinal ganglion cells.
Light adaptation exposes a hidden directional excitation in the circuit, which is tuned to opposite directions in the centre and surround receptive fields.
figure legend Direction‐selective retinal ganglion cells (DSGCs) respond to motion in the ‘preferred direction’ (PD), but barely to the motion in the opposite, ‘null direction’ (ND). Using targeted patch‐clamp and multi‐electrode array recordings, we investigated the effects of light adaptation on the response of DSGCs to moving bars. Light adaptation stre |
doi_str_mv | 10.1113/JP286581 |
format | Article |
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Key points
Receptive fields of direction‐selective retinal ganglion cells expand asymmetrically following light adaptation.
The increase in the surround receptive field generates a delayed spiking phase that is tuned to the null direction and is mediated by excitation.
Following light adaptation, excitation rules the computation in the centre receptive field and is tuned to the preferred direction.
GABAergic and glycinergic inputs modulate the null‐tuned delayed response differentially.
Null‐tuned delayed spiking phases can be detected in all types of direction‐selective retinal ganglion cells.
Light adaptation exposes a hidden directional excitation in the circuit, which is tuned to opposite directions in the centre and surround receptive fields.
figure legend Direction‐selective retinal ganglion cells (DSGCs) respond to motion in the ‘preferred direction’ (PD), but barely to the motion in the opposite, ‘null direction’ (ND). Using targeted patch‐clamp and multi‐electrode array recordings, we investigated the effects of light adaptation on the response of DSGCs to moving bars. Light adaptation strengthened the On response at the expense of the Off response. Moreover, it exposed a delayed spiking phase, which is tuned to the ND. Intracellular recordings revealed that before light adaptation, inhibition rules the directional response, whereas after light adaptation, both early and delayed directional responses are dominated by excitation. Interestingly, the PD response phase is mediated by excitation in the centre receptive field, whereas the ND delayed response phase is mediated by excitation from the surround. We thereby expose a new role for surround‐mediated excitation that occurs in light‐adapted conditions, potentially enhancing the detection of motion in specific lighting conditions.</description><identifier>ISSN: 0022-3751</identifier><identifier>ISSN: 1469-7793</identifier><identifier>EISSN: 1469-7793</identifier><identifier>DOI: 10.1113/JP286581</identifier><identifier>PMID: 39462912</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Acuity ; Adaptation ; Adaptation, Ocular - physiology ; Animals ; centre–surround ; Delayed response ; direction selectivity ; electrophysiology ; Information processing ; Light ; light adaptation ; Motion Perception - physiology ; mouse retina ; multi‐electrode array ; Photic Stimulation - methods ; Receptive field ; Retina ; Retina - physiology ; retinal ganglion cell ; Retinal ganglion cells ; Retinal Ganglion Cells - physiology ; Visual system ; γ-Aminobutyric acid</subject><ispartof>The Journal of physiology, 2024-11, Vol.602 (22), p.6301-6328</ispartof><rights>2024 The Author(s). published by John Wiley & Sons Ltd on behalf of The Physiological Society.</rights><rights>2024 The Author(s). The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.</rights><rights>2024. This article is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c2752-4933cf1069d6dc0119e020f8409097f86e11a23b9f0cfba661dcbb8c349ec6ab3</cites><orcidid>0000-0002-7622-6239 ; 0000-0002-1310-3370 ; 0000-0003-4369-4586</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1113%2FJP286581$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1113%2FJP286581$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,1416,27923,27924,45573,45574</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39462912$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ankri, Lea</creatorcontrib><creatorcontrib>Riccitelli, Serena</creatorcontrib><creatorcontrib>Rivlin‐Etzion, Michal</creatorcontrib><title>A new role for excitation in the retinal direction‐selective circuit</title><title>The Journal of physiology</title><addtitle>J Physiol</addtitle><description>A key feature of the receptive field of neurons in the visual system is their centre–surround antagonism, whereby the centre and the surround exhibit responses of opposite polarity. This organization is thought to enhance visual acuity, but whether and how such antagonism plays a role in more complex processing remains poorly understood. Here, we investigate the role of centre and surround receptive fields in retinal direction selectivity by exposing posterior‐preferring On–Off direction‐selective ganglion cells (pDSGCs) to adaptive light and recording their response to globally moving objects. We reveal that light adaptation leads to surround expansion in pDSGCs. The pDSGCs maintain their original directional tuning in the centre receptive field, but present the oppositely tuned response in their surround. Notably, although inhibition is the main substrate for retinal direction selectivity, we found that following light adaptation, both the centre‐ and surround‐mediated responses originate from directionally tuned excitatory inputs. Multi‐electrode array recordings show similar oppositely tuned responses in other DSGC subtypes. Together, these data attribute a new role for excitation in the direction‐selective circuit. This excitation carries an antagonistic centre–surround property, possibly designed to sharpen the detection of motion direction in the retina.
Key points
Receptive fields of direction‐selective retinal ganglion cells expand asymmetrically following light adaptation.
The increase in the surround receptive field generates a delayed spiking phase that is tuned to the null direction and is mediated by excitation.
Following light adaptation, excitation rules the computation in the centre receptive field and is tuned to the preferred direction.
GABAergic and glycinergic inputs modulate the null‐tuned delayed response differentially.
Null‐tuned delayed spiking phases can be detected in all types of direction‐selective retinal ganglion cells.
Light adaptation exposes a hidden directional excitation in the circuit, which is tuned to opposite directions in the centre and surround receptive fields.
figure legend Direction‐selective retinal ganglion cells (DSGCs) respond to motion in the ‘preferred direction’ (PD), but barely to the motion in the opposite, ‘null direction’ (ND). Using targeted patch‐clamp and multi‐electrode array recordings, we investigated the effects of light adaptation on the response of DSGCs to moving bars. Light adaptation strengthened the On response at the expense of the Off response. Moreover, it exposed a delayed spiking phase, which is tuned to the ND. Intracellular recordings revealed that before light adaptation, inhibition rules the directional response, whereas after light adaptation, both early and delayed directional responses are dominated by excitation. Interestingly, the PD response phase is mediated by excitation in the centre receptive field, whereas the ND delayed response phase is mediated by excitation from the surround. We thereby expose a new role for surround‐mediated excitation that occurs in light‐adapted conditions, potentially enhancing the detection of motion in specific lighting conditions.</description><subject>Acuity</subject><subject>Adaptation</subject><subject>Adaptation, Ocular - physiology</subject><subject>Animals</subject><subject>centre–surround</subject><subject>Delayed response</subject><subject>direction selectivity</subject><subject>electrophysiology</subject><subject>Information processing</subject><subject>Light</subject><subject>light adaptation</subject><subject>Motion Perception - physiology</subject><subject>mouse retina</subject><subject>multi‐electrode array</subject><subject>Photic Stimulation - methods</subject><subject>Receptive field</subject><subject>Retina</subject><subject>Retina - physiology</subject><subject>retinal ganglion cell</subject><subject>Retinal ganglion cells</subject><subject>Retinal Ganglion Cells - physiology</subject><subject>Visual system</subject><subject>γ-Aminobutyric acid</subject><issn>0022-3751</issn><issn>1469-7793</issn><issn>1469-7793</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1kM9Kw0AQhxdRtFbBJ5AFL16iM7vJJnssxfqHgj3oOSSbCa6kSd1NrL35CD6jT2JKrYLgaX4wHx8zP8ZOEC4QUV7ezUSiogR32ABDpYM41nKXDQCECGQc4QE79P4ZACVovc8OpA6V0CgGbDLiNS25ayriZeM4vRnbZq1tam5r3j4Rd9TaOqt4YR2Z9eLz_cNTtc6vxI11prPtEdsrs8rT8fccssfJ1cP4JpjeX9-OR9PAiDgSQailNCWC0oUqDCBqAgFlEoIGHZeJIsRMyFyXYMo8UwoLk-eJkaEmo7JcDtn5xrtwzUtHvk3n1huqqqympvOpRIEigRhVj579QZ-bzvWfrCkJIJWOol-hcY33jsp04ew8c6sUIV13m2677dHTb2GXz6n4Abdl9sDFBljailb_itKHu1l_XyzkF1mYgN8</recordid><startdate>20241101</startdate><enddate>20241101</enddate><creator>Ankri, Lea</creator><creator>Riccitelli, Serena</creator><creator>Rivlin‐Etzion, Michal</creator><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>WIN</scope><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><orcidid>https://orcid.org/0000-0002-7622-6239</orcidid><orcidid>https://orcid.org/0000-0002-1310-3370</orcidid><orcidid>https://orcid.org/0000-0003-4369-4586</orcidid></search><sort><creationdate>20241101</creationdate><title>A new role for excitation in the retinal direction‐selective circuit</title><author>Ankri, Lea ; Riccitelli, Serena ; Rivlin‐Etzion, Michal</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c2752-4933cf1069d6dc0119e020f8409097f86e11a23b9f0cfba661dcbb8c349ec6ab3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Acuity</topic><topic>Adaptation</topic><topic>Adaptation, Ocular - physiology</topic><topic>Animals</topic><topic>centre–surround</topic><topic>Delayed response</topic><topic>direction selectivity</topic><topic>electrophysiology</topic><topic>Information processing</topic><topic>Light</topic><topic>light adaptation</topic><topic>Motion Perception - physiology</topic><topic>mouse retina</topic><topic>multi‐electrode array</topic><topic>Photic Stimulation - methods</topic><topic>Receptive field</topic><topic>Retina</topic><topic>Retina - physiology</topic><topic>retinal ganglion cell</topic><topic>Retinal ganglion cells</topic><topic>Retinal Ganglion Cells - physiology</topic><topic>Visual system</topic><topic>γ-Aminobutyric acid</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ankri, Lea</creatorcontrib><creatorcontrib>Riccitelli, Serena</creatorcontrib><creatorcontrib>Rivlin‐Etzion, Michal</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Free Content</collection><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><jtitle>The Journal of physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ankri, Lea</au><au>Riccitelli, Serena</au><au>Rivlin‐Etzion, Michal</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A new role for excitation in the retinal direction‐selective circuit</atitle><jtitle>The Journal of physiology</jtitle><addtitle>J Physiol</addtitle><date>2024-11-01</date><risdate>2024</risdate><volume>602</volume><issue>22</issue><spage>6301</spage><epage>6328</epage><pages>6301-6328</pages><issn>0022-3751</issn><issn>1469-7793</issn><eissn>1469-7793</eissn><abstract>A key feature of the receptive field of neurons in the visual system is their centre–surround antagonism, whereby the centre and the surround exhibit responses of opposite polarity. This organization is thought to enhance visual acuity, but whether and how such antagonism plays a role in more complex processing remains poorly understood. Here, we investigate the role of centre and surround receptive fields in retinal direction selectivity by exposing posterior‐preferring On–Off direction‐selective ganglion cells (pDSGCs) to adaptive light and recording their response to globally moving objects. We reveal that light adaptation leads to surround expansion in pDSGCs. The pDSGCs maintain their original directional tuning in the centre receptive field, but present the oppositely tuned response in their surround. Notably, although inhibition is the main substrate for retinal direction selectivity, we found that following light adaptation, both the centre‐ and surround‐mediated responses originate from directionally tuned excitatory inputs. Multi‐electrode array recordings show similar oppositely tuned responses in other DSGC subtypes. Together, these data attribute a new role for excitation in the direction‐selective circuit. This excitation carries an antagonistic centre–surround property, possibly designed to sharpen the detection of motion direction in the retina.
Key points
Receptive fields of direction‐selective retinal ganglion cells expand asymmetrically following light adaptation.
The increase in the surround receptive field generates a delayed spiking phase that is tuned to the null direction and is mediated by excitation.
Following light adaptation, excitation rules the computation in the centre receptive field and is tuned to the preferred direction.
GABAergic and glycinergic inputs modulate the null‐tuned delayed response differentially.
Null‐tuned delayed spiking phases can be detected in all types of direction‐selective retinal ganglion cells.
Light adaptation exposes a hidden directional excitation in the circuit, which is tuned to opposite directions in the centre and surround receptive fields.
figure legend Direction‐selective retinal ganglion cells (DSGCs) respond to motion in the ‘preferred direction’ (PD), but barely to the motion in the opposite, ‘null direction’ (ND). Using targeted patch‐clamp and multi‐electrode array recordings, we investigated the effects of light adaptation on the response of DSGCs to moving bars. Light adaptation strengthened the On response at the expense of the Off response. Moreover, it exposed a delayed spiking phase, which is tuned to the ND. Intracellular recordings revealed that before light adaptation, inhibition rules the directional response, whereas after light adaptation, both early and delayed directional responses are dominated by excitation. Interestingly, the PD response phase is mediated by excitation in the centre receptive field, whereas the ND delayed response phase is mediated by excitation from the surround. We thereby expose a new role for surround‐mediated excitation that occurs in light‐adapted conditions, potentially enhancing the detection of motion in specific lighting conditions.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>39462912</pmid><doi>10.1113/JP286581</doi><tpages>28</tpages><orcidid>https://orcid.org/0000-0002-7622-6239</orcidid><orcidid>https://orcid.org/0000-0002-1310-3370</orcidid><orcidid>https://orcid.org/0000-0003-4369-4586</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Acuity Adaptation Adaptation, Ocular - physiology Animals centre–surround Delayed response direction selectivity electrophysiology Information processing Light light adaptation Motion Perception - physiology mouse retina multi‐electrode array Photic Stimulation - methods Receptive field Retina Retina - physiology retinal ganglion cell Retinal ganglion cells Retinal Ganglion Cells - physiology Visual system γ-Aminobutyric acid |
title | A new role for excitation in the retinal direction‐selective circuit |
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