13Neurons in various regions of the brain generate spike bursts. While the number of spikes within 14 a burst has been shown to carry information, information coding by interspike intervals (ISIs) is 15 less well understood. In particular, a burst with k spikes has k−1 intraburst ISIs, and these k−1 16ISIs could theoretically encode k−1 independent values. In this study, we demonstrate that such 17 combinatorial coding occurs for retinal bursts. By recording ganglion cell spikes from isolated 18 salamander retinae, we found that intraburst ISIs encode oscillatory light sequences that are 19 much faster than the light intensity modulation encoded by the number of spikes. When a burst 20 has three spikes, the two intraburst ISIs combinatorially encode the amplitude and phase of the 21 oscillatory sequence. Analysis of trial-to-trial variability suggested that intraburst ISIs are 22 regulated by two independent mechanisms responding to orthogonal oscillatory components, one 23 of which is common to bursts with different number of spikes. Therefore, the retina encodes 24 multiple stimulus features by exploiting all degrees of freedom of burst spike patterns, i.e., the 25 spike number and multiple intraburst ISIs. 26
Author Summary
27Neurons in various regions of the brain generate spike bursts. Bursts are typically composed of a 28 few spikes generated within dozens of milliseconds, and individual bursts are separated by much 29 longer periods of silence (~hundreds of milliseconds). Recent evidence indicates that the number 30 of spikes in a burst, the interspike intervals (ISIs), and the overall duration of a burst, as well as 31 the timing of burst onset, encode information. However, it remains unknown whether multiple 32ISIs within a single burst encode multiple independent information contents. Here we 33 demonstrate that such combinatorial ISI coding occurs for spike bursts in the retina. We recorded 34 3 ganglion cell spikes from isolated salamander retinae stimulated with computer-generated 35 movies. Visual response analyses indicated that multiple ISIs within a single burst 36 combinatorially encode the phase and amplitude of oscillatory light sequences, which are 37 different from the stimulus feature encoded by the spike number. The result demonstrates that the 38 retina encodes multiple stimulus features by exploiting all degrees of freedom of burst spike 39 patterns, i.e., the spike number and multiple intraburst ISIs. Because synaptic transmission in the 40 visual system is highly sensitive to ISIs, the combinatorial ISI coding must have a major impact 41 on visual information processing. 42