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.

Highlights

  • Understanding the rules by which neuronal spike patterns encode information is essential for investigating the complex functioning of the nervous system [1, 2]

  • Our results indicate that intraburst interspike intervals (ISIs) encode oscillatory light intensity sequences that are different from the stimulus feature encoded by the spike number

  • Burst spike numbers encode the amplitude of light intensity modulation

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Summary

Introduction

Understanding the rules by which neuronal spike patterns encode information is essential for investigating the complex functioning of the nervous system [1, 2]. Burst spikes typically occur within the temporal window of postsynaptic integration (dozens of milliseconds), and thereby induce synaptic responses with a higher probability than isolated single spikes [6,7,8]. In this regard, bursts are believed to represent an important neuronal code [7, 9, 10]. These intraburst ISIs can carry information if, for example, they are modulated by sensory inputs Such burst ISI coding should have significant effects on information transfer, because the efficiency of synaptic transmission is sensitive to ISIs [24]. Whether burst ISIs encode information in such a combinatorial manner is unknown

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