{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T06:09:36Z","timestamp":1772172576597,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1007726","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2020,12,15]],"date-time":"2020-12-15T00:00:00Z","timestamp":1607990400000}}],"reference-count":52,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2020,11,6]],"date-time":"2020-11-06T00:00:00Z","timestamp":1604620800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100013107","name":"RIKEN Brain Science Institute","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100013107","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["19300116"],"award-info":[{"award-number":["19300116"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>\n                    Neurons in various regions of the brain generate spike bursts. While the number of spikes within a burst has been shown to carry information, information coding by interspike intervals (ISIs) is less well understood. In particular, a burst with\n                    <jats:italic>k<\/jats:italic>\n                    spikes has\n                    <jats:italic>k\u2212<\/jats:italic>\n                    1 intraburst ISIs, and these\n                    <jats:italic>k\u2212<\/jats:italic>\n                    1 ISIs could theoretically encode\n                    <jats:italic>k\u2212<\/jats:italic>\n                    1 independent values. In this study, we demonstrate that such combinatorial coding occurs for retinal bursts. By recording ganglion cell spikes from isolated salamander retinae, we found that intraburst ISIs encode oscillatory light sequences that are much faster than the light intensity modulation encoded by the number of spikes. When a burst has three spikes, the two intraburst ISIs combinatorially encode the amplitude and phase of the oscillatory sequence. Analysis of trial-to-trial variability suggested that intraburst ISIs are regulated by two independent mechanisms responding to orthogonal oscillatory components, one of which is common to bursts with a different number of spikes. Therefore, the retina encodes multiple stimulus features by exploiting all degrees of freedom of burst spike patterns, i.e., the spike number and multiple intraburst ISIs.\n                  <\/jats:p>","DOI":"10.1371\/journal.pcbi.1007726","type":"journal-article","created":{"date-parts":[[2020,11,6]],"date-time":"2020-11-06T13:36:49Z","timestamp":1604669809000},"page":"e1007726","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":6,"title":["Interspike intervals within retinal spike bursts combinatorially encode multiple stimulus 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II. Retinal inputs and the generation of receptive-field properties","volume":"57","author":"DN Mastronarde","year":"1987","journal-title":"J Neurophysiol"},{"issue":"41","key":"pcbi.1007726.ref043","doi-asserted-by":"crossref","first-page":"13558","DOI":"10.1523\/JNEUROSCI.0909-10.2010","article-title":"Spike timing and information transmission at retinogeniculate synapses","volume":"30","author":"DL Rathbun","year":"2010","journal-title":"J Neurosci"},{"issue":"2","key":"pcbi.1007726.ref044","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1017\/S0952523801182076","article-title":"Dynamic properties of retino-geniculate synapses in the cat","volume":"18","author":"MH Rowe","year":"2001","journal-title":"Vis Neurosci"},{"issue":"10","key":"pcbi.1007726.ref045","doi-asserted-by":"crossref","first-page":"2683","DOI":"10.1523\/JNEUROSCI.5077-06.2007","article-title":"Transmission of spike trains at the retinogeniculate synapse","volume":"27","author":"LC Sincich","year":"2007","journal-title":"J Neurosci"},{"issue":"6700","key":"pcbi.1007726.ref046","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1038\/26487","article-title":"Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus","volume":"395","author":"WM Usrey","year":"1998","journal-title":"Nature"},{"issue":"2","key":"pcbi.1007726.ref047","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1152\/jn.00929.2006","article-title":"Retinogeniculate transmission in wakefulness","volume":"98","author":"TG Weyand","year":"2007","journal-title":"J Neurophysiol"},{"issue":"14","key":"pcbi.1007726.ref048","doi-asserted-by":"crossref","first-page":"5461","DOI":"10.1523\/JNEUROSCI.20-14-05461.2000","article-title":"Synaptic interactions between thalamic inputs to simple cells in cat visual cortex","volume":"20","author":"WM Usrey","year":"2000","journal-title":"J Neurosci"},{"issue":"1","key":"pcbi.1007726.ref049","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/0165-0270(94)90030-2","article-title":"Multi-neuronal signals from the retina: acquisition and analysis","volume":"51","author":"M Meister","year":"1994","journal-title":"J Neurosci Methods"},{"issue":"4","key":"pcbi.1007726.ref050","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1163\/156856897X00357","article-title":"The Psychophysics Toolbox","volume":"10","author":"DH Brainard","year":"1997","journal-title":"Spat Vis"},{"issue":"4","key":"pcbi.1007726.ref051","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1163\/156856897X00366","article-title":"The VideoToolbox software for visual psychophysics: transforming numbers into movies","volume":"10","author":"DG Pelli","year":"1997","journal-title":"Spat Vis."},{"issue":"23","key":"pcbi.1007726.ref052","doi-asserted-by":"crossref","first-page":"3407","DOI":"10.1016\/S0042-6989(97)00105-3","article-title":"Processing of natural time series of intensities by the visual system of the blowfly","volume":"37","author":"JH van Hateren","year":"1997","journal-title":"Vision Res"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1007726","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2020,12,15]],"date-time":"2020-12-15T00:00:00Z","timestamp":1607990400000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1007726","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,12,15]],"date-time":"2020-12-15T15:00:53Z","timestamp":1608044453000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1007726"}},"subtitle":[],"editor":[{"given":"Stefano","family":"Panzeri","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2020,11,6]]},"references-count":52,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2020,11,6]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1007726","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.02.13.947283","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,11,6]]}}}