Average Is Optimal: An Inverted-U Relationship between Trial-to-Trial Brain Activity and Behavioral Performance

Biyu J He,John M Zempel,Olaf Sporns

doi:10.1371/journal.pcbi.1003348

Abstract

It is well known that even under identical task conditions, there is a tremendous amount of trial-to-trial variability in both brain activity and behavioral output. Thus far the vast majority of event-related potential (ERP) studies investigating the relationship between trial-to-trial fluctuations in brain activity and behavioral performance have only tested a monotonic relationship between them. However, it was recently found that across-trial variability can correlate with behavioral performance independent of trial-averaged activity. This finding predicts a U- or inverted-U- shaped relationship between trial-to-trial brain activity and behavioral output, depending on whether larger brain variability is associated with better or worse behavior, respectively. Using a visual stimulus detection task, we provide evidence from human electrocorticography (ECoG) for an inverted-U brain-behavior relationship: When the raw fluctuation in broadband ECoG activity is closer to the across-trial mean, hit rate is higher and reaction times faster. Importantly, we show that this relationship is present not only in the post-stimulus task-evoked brain activity, but also in the pre-stimulus spontaneous brain activity, suggesting anticipatory brain dynamics. Our findings are consistent with the presence of stochastic noise in the brain. They further support attractor network theories, which postulate that the brain settles into a more confined state space under task performance, and proximity to the targeted trajectory is associated with better performance.

Highlights

An inverted-U relationship is well established between brain function and many neuromodulatory influences, including arousal [1], dopaminergic [2,3], cholinergic [4] and noradrenergic [5,6] systems, with both insufficient and excessive levels of neuromodulation causing impaired brain function and performance
It is thought that the relationship between trial-to-trial brain activity and behavioral performance is monotonic: the highest or lowest brain activity levels are associated with the best behavioral performance
These results have significant implications for our understanding of brain functioning. They further support recent theoretical frameworks that view the brain as an active nonlinear dynamical system instead of a passive signal-processing device

Summary

Introduction

An inverted-U relationship is well established between brain function and many neuromodulatory influences, including arousal [1], dopaminergic [2,3], cholinergic [4] and noradrenergic [5,6] systems, with both insufficient and excessive levels of neuromodulation causing impaired brain function and performance. The vast majority of studies on the relationship between trial-to-trial brain activity and behavior have only investigated a monotonic relationship between them by, for example, comparing trialaveraged brain activity between different categories of behavioral performance (e.g., hits vs misses) or computing the linear correlation between trial-to-trial brain activity and performance metrics [e.g., reaction times (RTs)] These methods have been successfully applied to reveal influence on cognition/behavior by both pre-stimulus ongoing brain activity and post-stimulus brain responses in functional magnetic resonance imaging (fMRI) [11,12,13,14,15] and magnetoencephalography (MEG) [16,17] signals from humans, as well as local field potentials (LFP) [18,19] and neuronal spiking activity from primates [20,21,22]. In light of the prevalent phase-amplitude coupling in the human brain whereby lower-frequency phase modulates higher-frequency power [31,32], we conjectured that such an inverted-U relationship might manifest in the raw fluctuations of field potentials, which is dominated by lowfrequency activity [31]

Methods

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Discussion

Conclusion