Interspike intervals within retinal spike bursts combinatorially encode multiple stimulus features

PLoS Comput Biol. 2020 Nov 6;16(11):e1007726. doi: 10.1371/journal.pcbi.1007726. eCollection 2020 Nov.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology*
  • Animals
  • Light
  • Models, Biological
  • Neurons / physiology
  • Photic Stimulation
  • Retina / cytology
  • Retina / physiology*
  • Urodela

Grant support

This work was supported by research funds from RIKEN to T.H. and Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan to T.H. (19300116). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.