Multiple Spike Time Patterns Occur at Bifurcation Points of Membrane Potential Dynamics

J Vincent Toups,Jean-Marc Fellous,Peter J Thomas,Terrence J Sejnowski,Paul H Tiesinga

doi:10.1371/journal.pcbi.1002615

Abstract

The response of a neuron to repeated somatic fluctuating current injections in vitro can elicit a reliable and precisely timed sequence of action potentials. The set of responses obtained across trials can also be interpreted as the response of an ensemble of similar neurons receiving the same input, with the precise spike times representing synchronous volleys that would be effective in driving postsynaptic neurons. To study the reproducibility of the output spike times for different conditions that might occur in vivo, we somatically injected aperiodic current waveforms into cortical neurons in vitro and systematically varied the amplitude and DC offset of the fluctuations. As the amplitude of the fluctuations was increased, reliability increased and the spike times remained stable over a wide range of values. However, at specific values called bifurcation points, large shifts in the spike times were obtained in response to small changes in the stimulus, resulting in multiple spike patterns that were revealed using an unsupervised classification method. Increasing the DC offset, which mimicked an overall increase in network background activity, also revealed bifurcation points and increased the reliability. Furthermore, the spike times shifted earlier with increasing offset. Although the reliability was reduced at bifurcation points, a theoretical analysis showed that the information about the stimulus time course was increased because each of the spike time patterns contained different information about the input.

Highlights

Neural recordings in vivo are often analyzed with the peristimulus time histogram, which measures increases or decreases in firing rate in response to stimulus onset [1]
Neurons respond with precise spike times to fluctuating current injections, leading to peaks in ensemble firing rate
We explore the consequences of precise spike times for neural coding in vivo, by investigating the spike event structure of virtual cell assemblies constructed in vitro

Summary

Introduction

Neural recordings in vivo are often analyzed with the peristimulus time histogram, which measures increases or decreases in firing rate in response to stimulus onset [1]. Ensemble recordings in cortex and hippocampus have shown that populations of cells could dynamically reactivate during sleep and quiet awake periods with high precision [6,7]. These precisely timed spikes drive target neurons [8,9,10], but only a few studies have reported stimuluslocked responses in cortex [11,12,13]. Whether cortical neurons in vivo respond as precisely as those measured in vitro depends on the impact of the external stimulus in the context of the background cortical state [14]. We refer to a group of neurons with common input as a neural assembly or ensemble [20], which will be further explained in the Discussion

Methods

Results

Discussion

Conclusion