Beta activity in human anterior cingulate cortex mediates reward biases

Introduction

One of the hallmarks of human behavior is the ability to associate rewards with the stimuli that produce them^{1, 2–3}. The anticipation of a reward can influence our decision-making process by overriding our initial sensory judgments and subsequently altering our subjective evaluation of a stimulus^{4, 5, 6–7}. These alterations in judgment, though sometimes suboptimal, can also be beneficial by biasing our behavior in a manner that increases the likelihood of obtaining greater rewards⁸. A fundamental unresolved question in human neuroscience is, therefore, what neural processes drive the learning, or association of reward information, so as to bias subsequent decisions^9,10.

Dysfunction of these reward association processes is a common characteristic of several neuropsychiatric disorders, most notably major depressive disorder^{11, 12, 13, 14–15}. Depression is a disabling disease characterized by anhedonia, disengagement, and reduced enjoyment of life^16,17. Among its hallmarks is the diminished influence of reward anticipation on decision-making^18,19. Investigating the underlying mechanisms of this phenomenon is therefore important for the development of innovative interventions aimed at providing therapeutic benefit by enhancing the impact of reward^{20, 21–22}.

Several human electrophysiological studies have identified a mediofrontal oscillatory component associated with positive feedback in both gambling task and reversal learning task, tasks that have key features in common with our bias task. The increase observed in these tasks is in the beta range and occurs 200 to 400 ms after the feedback informing the participant about the monetary gains^{23, 24, 25, 26–27}. It has been proposed that this beta activity is generated in the prefrontal cortex; the most commonly inferred source site is the anterior cingulate cortex (ACC). It is further assumed that the ACC then transmits a fast motivational value signal, still in the beta band, from the frontal cortex to downstream reward-related regions²⁶. Moreover, beta activity in the cingulate cortex is of particular importance in depression^{28, 29–30}. For example, a recent study showed that beta activity best tracks depressive states, seen as a decrease in beta band power during the first month of chronic stimulation, followed by an eventual rise³¹. This result suggests that sustained, antidepressant responses might involve increased beta band power...