Electrophysiological underpinnings of reward processing: Are we exploiting the full potential of EEG?

Garance M Meyer,Josep Marco-Pallarés,Philippe Boulinguez,Guillaume Sescousse

doi:10.1016/j.neuroimage.2021.118478

Abstract

Understanding how the brain processes reward is an important and complex endeavor, which has involved the use of a range of complementary neuroimaging tools, including electroencephalography (EEG). EEG has been praised for its high temporal resolution but, because the signal recorded at the scalp is a mixture of brain activities, it is often considered to have poor spatial resolution. Besides, EEG data analysis has most often relied on event-related potentials (ERPs) which cancel out non-phase locked oscillatory activity, thus limiting the functional discriminative power of EEG attainable through spectral analyses. Because these three dimensions -temporal, spatial and spectral- have been unequally leveraged in reward studies, we argue that the full potential of EEG has not been exploited. To back up our claim, we first performed a systematic survey of EEG studies assessing reward processing. Specifically, we report on the nature of the cognitive processes investigated (i.e., reward anticipation or reward outcome processing) and the methods used to collect and process the EEG data (i.e., event-related potential, time-frequency or source analyses). A total of 359 studies involving healthy subjects and the delivery of monetary rewards were surveyed. We show that reward anticipation has been overlooked (88% of studies investigated reward outcome processing, while only 24% investigated reward anticipation), and that time-frequency and source analyses (respectively reported by 19% and 12% of the studies) have not been widely adopted by the field yet, with ERPs still being the dominant methodology (92% of the studies). We argue that this focus on feedback-related ERPs provides a biased perspective on reward processing, by ignoring reward anticipation processes as well as a large part of the information contained in the EEG signal. Finally, we illustrate with selected examples how addressing these issues could benefit the field, relying on approaches combining time-frequency analyses, blind source separation and source localization.

Highlights

Reward processing is at the very heart of goal-directed behavior and decision-making
Our survey of the literature reveals that a majority of EEG studies on reward processing have been designed to investigate how ex
Using source-space connectivity analyses to unravel the interaction between the reward network and the attentional, executive, or motor networks, that mediates the behavioral effects of reward

Summary

Introduction

Reward processing is at the very heart of goal-directed behavior and decision-making. While reward anticipation corresponds to the cognitive operations that precede an incoming reward, including incentive valuation, probability estimation or motor preparation, reward outcome corresponds to those operations triggered by the actual delivery of the reward, including hedonic feelings, reward value update and behavioral reinforcement. Reward processing involves large brain networks as well as various neuromodulators (Haber and Knutson, 2010; Kranz et al, 2010; Liu et al, 2011). This complexity requires the use of complementary neuroimaging techniques

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