Spontaneous eye movements reveal that premotor cortex is involved in human thinking

Non-visual saccades (NVS) are spontaneous eye movements humans make while thinking. Their role is puzzling and there is no framework to explain them in terms of underlying neural systems. Here we studied neural activity preceding NVS when subjects performed standardized abstract thinking tasks. We used high-density EEG and focused on frontal and parietal channels representing oculomotor cortical areas. We found that NVS are distinctively preceded by neural activity changes in frontal and parietal EEG channels qualitatively different to that for voluntary saccades. However, only the ERP amplitude changes in frontal channels, but not in parietal channels, were different from saccadic preparation. A source reconstruction analysis additionally revealed that presaccadic neural activity originated mainly in the premotor cortex. Frequency spectrum analyses showed increased synchronization in alpha to low gamma bands suggesting complex top-down and bottom-up processing. We propose that this presaccadic activity while thinking represents evidence accumulation and attentional shifts, as shown before in the premotor cortex during sensorimotor tasks. Our findings suggest that human thinking appears to function similarly to human actions and engages premotor areas responsible for evaluating and manipulating objects also when evaluating and manipulating concepts.