Reduced Variability of Ongoing and Evoked Cortical Activity Leads to Improved Behavioral Performance

Anders Ledberg,Steven L Bressler,Richard Coppola,Anna Montagnini,Olaf Sporns

doi:10.1371/journal.pone.0043166

Abstract

Sensory responses of the brain are known to be highly variable, but the origin and functional relevance of this variability have long remained enigmatic. Using the variable foreperiod of a visual discrimination task to assess variability in the primate cerebral cortex, we report that visual evoked response variability is not only tied to variability in ongoing cortical activity, but also predicts mean response time. We used cortical local field potentials, simultaneously recorded from widespread cortical areas, to gauge both ongoing and visually evoked activity. Trial-to-trial variability of sensory evoked responses was strongly modulated by foreperiod duration and correlated both with the cortical variability before stimulus onset as well as with response times. In a separate set of experiments we probed the relation between small saccadic eye movements, foreperiod duration and manual response times. The rate of eye movements was modulated by foreperiod duration and eye position variability was positively correlated with response times. Our results indicate that when the time of a sensory stimulus is predictable, reduction in cortical variability before the stimulus can improve normal behavioral function that depends on the stimulus.

Highlights

In sensory areas of the brain, neuronal responses to the same stimulus may vary considerably from one trial to the [1,2,3,4] and this variability is weakly correlated between neighboring neurons [5,6]
We show that VEP variability in widespread cortical regions is strongly modulated by foreperiod duration, that VEP variability depends on ongoing cortical activity at the time of stimulus onset, and that foreperiod-dependent reduction of mean response times can be explained by the reduction in VEP variability
VEP variability is modulated by foreperiod duration Previously we showed that local field potentials (LFPs) recorded from widespread cortical areas have a short-latency (50–100 ms) VEP response, time-locked to the onset of the visual stimulus [32]

Summary

Introduction

In sensory areas of the brain, neuronal responses to the same stimulus may vary considerably from one trial to the [1,2,3,4] and this variability is weakly correlated between neighboring neurons [5,6]. Neuronal response variability may have several causes, and in the case of visual stimuli, subtle between trial differences in eye movements are a prominent such cause [11]. Since both macroand micro saccades influence the firing of single neurons [12,13,14] as well as the amplitude of local field potentials [15,16] one possible way to reduce trial-to-trial variability of the cortical response is to reduce the rate of saccadic eye movements. Recent evidence obtained in both human- [17] and nonhuman primates [18], indicates that microsaccades in close temporal relation to the imperative stimulus lead to impaired behavioral performance, an observation suggesting that cortical response variability, induced by eye movements, interferes with normal behavior

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Conclusion