Decoding the neural dynamics of free choice in humans

Summary How do we choose a particular action among equally valid alternatives? Non-human primate findings have shown that decision-making implicates modulations in unit firing rates and local field potentials (LFPs) across frontal and parietal cortices. Yet the electrophysiological brain mechanisms that underlie free choice in humans remain ill defined. Here, we address this question using rare intracerebral EEG recordings in surgical epilepsy patients performing a delayed oculomotor decision task. We find that the temporal dynamics of high gamma (HG, 60-140 Hz) neural activity in distinct frontal and parietal brain areas robustly discriminate free choice from instructed saccade planning at the level of single trials. Classification analysis was applied to the LFP signals to isolate decision-related activity from sensory and motor planning processes. Compared to instructed saccades, free choice trials exhibited delayed and longer-lasting HG activity. The temporal dynamics of these sustained decision-related responses distinguished deliberation-related from working memory processes. Taken together, these findings provide the first direct electrophysiological evidence in humans for the role of sustained high-frequency neural activation in fronto-parietal cortex in mediating the intrinsically driven process of freely choosing among competing behavioral alternatives. Highlights First intracerebral recordings in humans performing an oculomotor decision-making task Machine learning analytics unravel underlying spectral and temporal brain dynamics Free choice trials exhibit sustained fronto-parietal high gamma (HG) activity during the delay Making a decision and maintaining it in working memory are associated with distinct sustained HG dynamics