Abstract
How do we choose a particular action among equally valid alternatives? Nonhuman 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 electroencephalography (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 with instructed saccades, free-choice trials exhibited delayed and longer-lasting HG activity during the delay period. The temporal dynamics of the decision-specific sustained HG activity indexed the unfolding of a deliberation process, rather than memory maintenance. Taken together, these findings provide the first direct electrophysiological evidence in humans for the role of sustained high-frequency neural activation in frontoparietal cortex in mediating the intrinsically driven process of freely choosing among competing behavioral alternatives.
Highlights
Deciding where to look to explore the visual world, i.e., picking one out of many alternative targets is a crucial aspect of our daily interactions with the environment
Six participants (4 females, mean age 30.3 ± 9.6, see Material and methods and Fig 1B and 1C) performed a delayed saccade task (Fig 1A) while electrophysiological data were recorded from multilead EEG depth electrodes
We found that most free-choicespecific sites exhibited enhanced HG activity only during the early part of the delay period (29 electrodes, 3/4 participants) in a network of regions including superior frontal gyrus (SFG), middle frontal gyrus (MFG), SMA, intraparietal sulcus (IPS), and frontal eye field (FEF)
Summary
Deciding where to look to explore the visual world, i.e., picking one out of many alternative targets is a crucial aspect of our daily interactions with the environment. 2 fMRI studies using the same delayed saccade task used in this article have shown that voluntary saccades were preceded by activation in the dorsolateral prefrontal cortex (DLPFC) and in the FEF, suggesting the involvement of these areas in the process of choosing where to look when facing 2 possible visual targets [39,40]. Noninvasive techniques have several limitations in terms of signal quality, spatial resolution, and sensitivity to artifacts It is possible in some rare cases to access invasive electrophysiological recordings in humans (e.g., surgical epilepsy patients) and probe task-based changes via direct LFP recordings. The unique intracerebral recordings reported here provide important insights into the spatiotemporal characteristics of the neural patterns underlying free choice and help bridge the gap with previous animal electrophysiology and noninvasive studies in humans
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