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 their 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 preceded by neural activity changes in frontal and parietal EEG channels qualitatively different to that for voluntary saccades. However, only the rate of signal change in frontal channels, but not in parietal channels, surpassed that observed when comparing NVS to normal saccades. Frequency spectrum analyses showed activity patterns reflecting complex top-down and bottom-up processing. A source reconstruction analysis additionally revealed that presaccadic signals originated mainly in the premotor cortex. 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 employs premotor areas responsible for evaluating and manipulating objects also when evaluating and manipulating concepts.