The Differential Weights of Motivational and Task Performance Measures on Medial and Lateral Frontal Neural Activity

Behavioral adaptations are triggered by different constraints given by rules, and are informed by outcomes, or motivational changes. Neural activity in multiple frontal areas is modulated during behavioral adaptations, but the source of these modulations and the nature of the mechanisms involved are unclear. Here we tested how different variables related to changes in task performance and to behavioral adaptation impact the amplitude of event-related local field potentials (LFPs) in the lateral prefrontal and midcingulate cortex of male rhesus macaques. We found that the behavioral task used induced consistently different types of performance modulation: in relation to task difficulty (imposed by the experimental setup), to successes and errors, and to the time spent in the task. Difficulty had a significant effect on monkeys' accuracy and reaction times. Interestingly, there is also a strong interaction between difficulty and trial success on the reaction times variation. However, LFP modulations were mostly related to reaction times, touch position, feedback valence and time-in-session, with little, if any, effect of difficulty. Hence, difficulty modulated performance but not LFP activity. This suggests that, in our experimental design, execution, regulation, and motivation-related factors are the main factors influencing medial and lateral frontal activity. SIGNIFICANCE STATEMENT Adapting decisions might be determined by several mechanisms and might be driven by motivational factors and/or factors inherent to the task at hand. Multiple frontal areas contribute to behavioral adaptations. One current challenge is to understand which information they process contributes to behavioral changes. Diverging views have emerged on whether task demands, like the decision difficulty, or factors linked to incentives to adapt, are driving frontal activity. Here we show that task difficulty had a strong effect on performance (accuracy and reaction times) but little effect on LFP recorded in monkey lateral prefrontal and midcingulate cortex. However, information related to actions, outcome valence, and time-in-session had major influences. Thus, task difficulty modulated performance but not LFP activity in frontal areas.