PMID- 33156853 OWN - NLM STAT- MEDLINE DCOM- 20210129 LR - 20210129 IS - 1553-7358 (Electronic) IS - 1553-734X (Print) IS - 1553-734X (Linking) VI - 16 IP - 11 DP - 2020 Nov TI - Interspike intervals within retinal spike bursts combinatorially encode multiple stimulus features. PG - e1007726 LID - 10.1371/journal.pcbi.1007726 [doi] LID - e1007726 AB - 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 k spikes has k-1 intraburst ISIs, and these k-1 ISIs could theoretically encode k-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. FAU - Ishii, Toshiyuki AU - Ishii T AUID- ORCID: 0000-0002-5067-1035 AD - RIKEN Center for Brain Science and RIKEN Brain Science Institute, Wako-shi, Saitama, Japan. AD - Toho University, Funabashi-shi, Chiba, Japan. AD - Department of Physiology, Nippon Medical School, Bunkyo-ku, Tokyo, Japan. FAU - Hosoya, Toshihiko AU - Hosoya T AUID- ORCID: 0000-0001-8559-8344 AD - RIKEN Center for Brain Science and RIKEN Brain Science Institute, Wako-shi, Saitama, Japan. LA - eng PT - Journal Article PT - Research Support, Non-U.S. Gov't DEP - 20201106 PL - United States TA - PLoS Comput Biol JT - PLoS computational biology JID - 101238922 SB - IM MH - Action Potentials/*physiology MH - Animals MH - Light MH - Models, Biological MH - Neurons/physiology MH - Photic Stimulation MH - Retina/cytology/*physiology MH - Urodela PMC - PMC7738174 COIS- The authors have declared that no competing interests exist. EDAT- 2020/11/07 06:00 MHDA- 2021/01/30 06:00 PMCR- 2020/11/06 CRDT- 2020/11/06 17:35 PHST- 2020/02/10 00:00 [received] PHST- 2020/09/22 00:00 [accepted] PHST- 2020/12/15 00:00 [revised] PHST- 2020/11/07 06:00 [pubmed] PHST- 2021/01/30 06:00 [medline] PHST- 2020/11/06 17:35 [entrez] PHST- 2020/11/06 00:00 [pmc-release] AID - PCOMPBIOL-D-20-00205 [pii] AID - 10.1371/journal.pcbi.1007726 [doi] PST - epublish SO - PLoS Comput Biol. 2020 Nov 6;16(11):e1007726. doi: 10.1371/journal.pcbi.1007726. eCollection 2020 Nov.