{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T19:53:50Z","timestamp":1792785230654,"version":"4.5.0"},"reference-count":110,"publisher":"National Academy of Sciences","issue":"52","license":[{"start":{"date-parts":[[2024,12,19]],"date-time":"2024-12-19T00:00:00Z","timestamp":1734566400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"name":"Center for the Physics of Biological Function","award":["PHY-1734030"],"award-info":[{"award-number":["PHY-1734030"]}]},{"name":"National Institute of Health BRAIN Initiative","award":["R01EB026943"],"award-info":[{"award-number":["R01EB026943"]}]},{"DOI":"10.13039\/100023581","name":"NSF | National Science Foundation Graduate Research Fellowship Program","doi-asserted-by":"publisher","award":["DGE-2039656"],"award-info":[{"award-number":["DGE-2039656"]}],"id":[{"id":"10.13039\/100023581","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2024,12,24]]},"abstract":"<jats:p>Everything that the brain sees must first be encoded by the retina, which maintains a reliable representation of the visual world in many different, complex natural scenes while also adapting to stimulus changes. This study quantifies whether and how the brain selectively encodes stimulus features about scene identity in complex naturalistic environments. While a wealth of previous work has dug into the static and dynamic features of the population code in retinal ganglion cells (RGCs), less is known about how populations form both flexible and reliable encoding in natural moving scenes. We record from the larval salamander retina responding to five different natural movies, over many repeats, and use these data to characterize the population code in terms of single-cell fluctuations in rate and pairwise couplings between cells. Decomposing the population code into independent and cell\u2013cell interactions reveals how broad scene structure is encoded in the retinal output. while the single-cell activity adapts to different stimuli, the population structure captured in the sparse, strong couplings is consistent across natural movies as well as synthetic stimuli. We show that these interactions contribute to encoding scene identity. We also demonstrate that this structure likely arises in part from shared bipolar cell input as well as from gap junctions between RGCs and amacrine cells.<\/jats:p>","DOI":"10.1073\/pnas.2313676121","type":"journal-article","created":{"date-parts":[[2024,12,19]],"date-time":"2024-12-19T13:40:01Z","timestamp":1734615601000},"update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":15,"title":["Stimulus-invariant aspects of the retinal code drive discriminability of natural scenes"],"prefix":"10.1073","volume":"121","author":[{"ORCID":"https:\/\/orcid.org\/0009-0000-9121-3500","authenticated-orcid":false,"given":"Benjamin D.","family":"Hoshal","sequence":"first","affiliation":[{"name":"Committee on Computational Neuroscience","place":["Chicago"]},{"name":"Department of Organismal Biology and Anatomy, University of Chicago","place":["Chicago"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9885-4933","authenticated-orcid":false,"given":"Caroline M.","family":"Holmes","sequence":"additional","affiliation":[{"name":"Department of Physics","place":["Princeton"]},{"name":"Princeton University","place":["Princeton"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kyle","family":"Bojanek","sequence":"additional","affiliation":[{"name":"Committee on Computational Neuroscience","place":["Chicago"]},{"name":"Department of Organismal Biology and Anatomy, University of Chicago","place":["Chicago"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-0215-9717","authenticated-orcid":false,"given":"Jared M.","family":"Salisbury","sequence":"additional","affiliation":[{"name":"Department of Organismal Biology and Anatomy","place":["Chicago"]},{"name":"University of Chicago","place":["Chicago"]},{"name":"Department of Physics","place":["Chicago"]},{"name":"University of Chicago","place":["Chicago"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4133-7999","authenticated-orcid":false,"suffix":"II","given":"Michael J.","family":"Berry","sequence":"additional","affiliation":[{"name":"Princeton Neuroscience Institute","place":["Princeton"]},{"name":"Department of Molecular Biology, Princeton University","place":["Princeton"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0090-6190","authenticated-orcid":false,"given":"Olivier","family":"Marre","sequence":"additional","affiliation":[{"name":"Institut de la Vision","place":["Paris"]},{"name":"Sorbonne Universit\u00e9, INSERM","place":["Paris"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6211-6293","authenticated-orcid":false,"given":"Stephanie E.","family":"Palmer","sequence":"additional","affiliation":[{"name":"Committee on Computational Neuroscience","place":["Chicago"]},{"name":"Department of Organismal Biology and Anatomy, University of Chicago","place":["Chicago"]},{"name":"Department of Organismal Biology and Anatomy","place":["Chicago"]},{"name":"University of Chicago","place":["Chicago"]},{"name":"Department of Physics","place":["Chicago"]},{"name":"University of Chicago","place":["Chicago"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2024,12,19]]},"reference":[{"key":"e_1_3_4_1_2","doi-asserted-by":"publisher","DOI":"10.1113\/jphysiol.1953.sp004829"},{"key":"e_1_3_4_2_2","doi-asserted-by":"publisher","DOI":"10.1113\/jphysiol.1959.sp006308"},{"key":"e_1_3_4_3_2","doi-asserted-by":"publisher","DOI":"10.1152\/ajplegacy.1940.130.4.690"},{"key":"e_1_3_4_4_2","doi-asserted-by":"publisher","DOI":"10.1152\/jn.1997.78.5.2336"},{"key":"e_1_3_4_5_2","first-page":"36","article-title":"Reading a neural code","volume":"2","author":"Bialek W.","year":"1989","unstructured":"W. Bialek, F. Rieke, R. van Steveninck, D. Warland, Reading a neural code. Adv. Neural. Inf. Process. Syst. 2, 36\u201343 (1989).","journal-title":"Adv. Neural. Inf. Process. Syst."},{"key":"e_1_3_4_6_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2009.12.009"},{"key":"e_1_3_4_7_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.4206-07.2008"},{"key":"e_1_3_4_8_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0896-6273(00)80992-7"},{"key":"e_1_3_4_9_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.conb.2008.09.010"},{"key":"e_1_3_4_10_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature07140"},{"key":"e_1_3_4_11_2","unstructured":"L. Ramirez W. Bialek Compression as a path to simplification: Models of collective neural activity. arXiv [Preprint] (2021). https:\/\/arxiv.org\/abs\/2112.14334 (Accessed 29 November 2024)."},{"key":"e_1_3_4_12_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1418092112"},{"key":"e_1_3_4_13_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2023.06.007"},{"key":"e_1_3_4_14_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1006057"},{"key":"e_1_3_4_15_2","unstructured":"M. Molano-Mazon A. Onken E. Piasini S. Panzeri \u201cSynthesizing realistic neural population activity patterns using Generative Adversarial Networks\u201d in International Conference on Learning Representations (2018). https:\/\/openreview.net\/forum?id=r1VVsebAZ. Accessed 29 November 2024."},{"key":"e_1_3_4_16_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-019-1346-5"},{"key":"e_1_3_4_17_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.0723-12.2012"},{"key":"e_1_3_4_18_2","doi-asserted-by":"publisher","DOI":"10.1152\/jn.00785.2013"},{"key":"e_1_3_4_19_2","doi-asserted-by":"crossref","unstructured":"C. M. Lopez et al. \u201c22.7 a 966-electrode neural probe with 384 configurable channels in 0.13 mum SOI CMOS\u201d in 2016 IEEE International Solid-State Circuits Conference (ISSCC) (IEEE 2016) pp. 392\u2013393.","DOI":"10.1109\/ISSCC.2016.7418072"},{"key":"e_1_3_4_20_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.abf4588"},{"key":"e_1_3_4_21_2","volume-title":"The First Steps in Seeing","author":"Rodieck R. W.","year":"1998","unstructured":"R. W. Rodieck, The First Steps in Seeing (Sinauer Associates, 1998)."},{"key":"e_1_3_4_22_2","doi-asserted-by":"publisher","DOI":"10.1103\/PhysRevLett.73.814"},{"key":"e_1_3_4_23_2","doi-asserted-by":"publisher","DOI":"10.1038\/90526"},{"key":"e_1_3_4_24_2","doi-asserted-by":"publisher","DOI":"10.1088\/0954-898X_6_3_003"},{"key":"e_1_3_4_25_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1998.0577"},{"key":"e_1_3_4_26_2","doi-asserted-by":"publisher","DOI":"10.1038\/35090500"},{"key":"e_1_3_4_27_2","doi-asserted-by":"publisher","DOI":"10.1162\/neco.1992.4.2.196"},{"key":"e_1_3_4_28_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1000025"},{"key":"e_1_3_4_29_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.5570-08.2009"},{"key":"e_1_3_4_30_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2018.04.075"},{"key":"e_1_3_4_31_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF01111929"},{"key":"e_1_3_4_32_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0952523806231043"},{"key":"e_1_3_4_33_2","doi-asserted-by":"crossref","unstructured":"J. M. Salisbury S. E. Palmer A dynamic scale-mixture model of motion in natural scenes. bioRxiv [Preprint] (2023). https:\/\/doi.org\/10.1101\/2023.10.19.563101 (Accessed 29 November 2024).","DOI":"10.1101\/2023.10.19.563101"},{"key":"e_1_3_4_34_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10955-015-1439-y"},{"key":"e_1_3_4_35_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.23-04-01506.2003"},{"key":"e_1_3_4_36_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.21-23-09445.2001"},{"key":"e_1_3_4_37_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature04701"},{"key":"e_1_3_4_38_2","doi-asserted-by":"publisher","DOI":"10.1167\/6.4.9"},{"key":"e_1_3_4_39_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1002922"},{"key":"e_1_3_4_40_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1019641108"},{"key":"e_1_3_4_41_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1003408"},{"key":"e_1_3_4_42_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1000380"},{"key":"e_1_3_4_43_2","doi-asserted-by":"publisher","DOI":"10.1103\/PhysRev.106.620"},{"key":"e_1_3_4_44_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1004906107"},{"key":"e_1_3_4_45_2","first-page":"150","article-title":"Inferring structured connectivity from spike trains under negative-binomial generalized linear models","volume":"50","author":"Linderman S. W.","year":"2015","unstructured":"S. W. Linderman, R. P. Adams, J. W. Pillow, Inferring structured connectivity from spike trains under negative-binomial generalized linear models. Neuron 50, 150 (2015).","journal-title":"Neuron"},{"key":"e_1_3_4_46_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.conb.2020.11.005"},{"key":"e_1_3_4_47_2","doi-asserted-by":"publisher","DOI":"10.3389\/fncom.2010.00012"},{"key":"e_1_3_4_48_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1005390"},{"key":"e_1_3_4_49_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.1282-06.2006"},{"key":"e_1_3_4_50_2","doi-asserted-by":"publisher","DOI":"10.1103\/PhysRevE.98.042410"},{"key":"e_1_3_4_51_2","unstructured":"L. Meshulam J. L. Gauthier C. D. Brody D. W. Tank W. Bialek Successes and failures of simplified models for a network of real neurons. arXiv [Preprint] (2021). https:\/\/arxiv.org\/abs\/2112.14735 (Accessed 29 November 2024)."},{"key":"e_1_3_4_52_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1008501"},{"key":"e_1_3_4_53_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1003344"},{"key":"e_1_3_4_54_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0805923106"},{"key":"e_1_3_4_55_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrn3687"},{"key":"e_1_3_4_56_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-neuro-062111-150410"},{"key":"e_1_3_4_57_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-022-04724-y"},{"key":"e_1_3_4_58_2","doi-asserted-by":"publisher","DOI":"10.1002\/cpa.20124"},{"key":"e_1_3_4_59_2","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms2388"},{"key":"e_1_3_4_60_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature09178"},{"key":"e_1_3_4_61_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ceca.2005.01.010"},{"key":"e_1_3_4_62_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature09570"},{"key":"e_1_3_4_63_2","doi-asserted-by":"crossref","unstructured":"D. Lee J. Kim S. A. Baccus Classification and analysis of retinal interneurons by computational structure under natural scenes. bioRxiv [Preprint] (2024). https:\/\/doi.org\/10.1101\/2024.03.18.585364 (Accessed 29 November 2024).","DOI":"10.1101\/2024.03.18.585364"},{"key":"e_1_3_4_64_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrn1888"},{"key":"e_1_3_4_65_2","doi-asserted-by":"publisher","DOI":"10.1186\/s13408-020-00101-z"},{"key":"e_1_3_4_66_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.0808-13.2013"},{"key":"e_1_3_4_67_2","doi-asserted-by":"publisher","DOI":"10.1038\/nn.3308"},{"key":"e_1_3_4_68_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.2631-11.2011"},{"key":"e_1_3_4_69_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2006.03.039"},{"key":"e_1_3_4_70_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.3749-12.2013"},{"key":"e_1_3_4_71_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-022-33242-8"},{"key":"e_1_3_4_72_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jphysparis.2012.12.001"},{"key":"e_1_3_4_73_2","doi-asserted-by":"publisher","DOI":"10.1085\/jgp.201110629"},{"key":"e_1_3_4_74_2","doi-asserted-by":"publisher","DOI":"10.1152\/jn.00995.2005"},{"key":"e_1_3_4_75_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tins.2022.03.005"},{"key":"e_1_3_4_76_2","doi-asserted-by":"publisher","DOI":"10.1038\/nn1887"},{"key":"e_1_3_4_77_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature01652"},{"key":"e_1_3_4_78_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2007.07.042"},{"key":"e_1_3_4_79_2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.45743"},{"key":"e_1_3_4_80_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.1460-13.2014"},{"key":"e_1_3_4_81_2","doi-asserted-by":"publisher","DOI":"10.1038\/nn.3241"},{"key":"e_1_3_4_82_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2013.11.029"},{"key":"e_1_3_4_83_2","doi-asserted-by":"publisher","DOI":"10.1167\/8.13.2"},{"key":"e_1_3_4_84_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-017-01798-5"},{"key":"e_1_3_4_85_2","doi-asserted-by":"publisher","DOI":"10.1038\/35079612"},{"key":"e_1_3_4_86_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.1660-15.2015"},{"key":"e_1_3_4_87_2","doi-asserted-by":"publisher","DOI":"10.1038\/nn.3707"},{"key":"e_1_3_4_88_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tics.2009.10.011"},{"key":"e_1_3_4_89_2","first-page":"11355","article-title":"Learning low-dimensional generalizable natural features from retina using a U-net","volume":"35","author":"Wang S.","year":"2022","unstructured":"S. Wang , Learning low-dimensional generalizable natural features from retina using a U-net. Adv. Neural. Inf. Process. Syst. 35, 11355\u201311368 (2022).","journal-title":"Adv. Neural. Inf. Process. Syst."},{"key":"e_1_3_4_90_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1007409"},{"key":"e_1_3_4_91_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tins.2009.12.001"},{"key":"e_1_3_4_92_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1720995115"},{"key":"e_1_3_4_93_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.66.1.1"},{"key":"e_1_3_4_94_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.66.1.15"},{"key":"e_1_3_4_95_2","doi-asserted-by":"publisher","DOI":"10.1159\/000118864"},{"key":"e_1_3_4_96_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2005.03.026"},{"key":"e_1_3_4_97_2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.06134"},{"key":"e_1_3_4_98_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41593-021-00902-9"},{"key":"e_1_3_4_99_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2017.04.034"},{"key":"e_1_3_4_100_2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.32671"},{"key":"e_1_3_4_101_2","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.53.3.758"},{"key":"e_1_3_4_102_2","doi-asserted-by":"publisher","DOI":"10.1093\/cercor\/3.5.488"},{"key":"e_1_3_4_103_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature11110"},{"key":"e_1_3_4_104_2","unstructured":"S. E. Palmer Larval salamander retinal population data in response to natural movies from the Chicago Motion Database [Dataset]. Dryad. https:\/\/doi.org\/10.5061\/dryad.4qrfj6qm8. Deposited 29 November 2024."},{"key":"e_1_3_4_105_2","doi-asserted-by":"publisher","DOI":"10.1113\/jphysiol.2008.156638"},{"key":"e_1_3_4_106_2","doi-asserted-by":"publisher","DOI":"10.1038\/334069a0"},{"key":"e_1_3_4_107_2","doi-asserted-by":"publisher","DOI":"10.1103\/PhysRevE.94.023301"},{"key":"e_1_3_4_108_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1111471108"},{"key":"e_1_3_4_109_2","doi-asserted-by":"publisher","DOI":"10.1109\/TSP.2018.2844203"},{"key":"e_1_3_4_110_2","doi-asserted-by":"publisher","DOI":"10.1109\/TCYB.2020.3042513"}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.2313676121","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,12,19]],"date-time":"2024-12-19T13:40:52Z","timestamp":1734615652000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/10.1073\/pnas.2313676121"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,12,19]]},"references-count":110,"journal-issue":{"issue":"52","published-print":{"date-parts":[[2024,12,24]]}},"alternative-id":["10.1073\/pnas.2313676121"],"URL":"https:\/\/doi.org\/10.1073\/pnas.2313676121","relation":{},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,19]]},"assertion":[{"value":"2023-08-08","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2024-11-11","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2024-12-19","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e2313676121"}}