Capturing the spatiotemporal dynamics of task-initiated thoughts with combined EEG and fMRI

When at rest, our mind wanders from thought to thought in distinct mental states, portrayed by William James as the brief flights and perchings of a bird. Despite the marked importance of ongoing mental processes, in cognitive neuroscience and clinical contexts alike, it is challenging to capture and relate these states to specific cognitive contents. In this work, we employed ultra-high field functional magnetic resonance imaging (fMRI) and high-density electroencephalography (EEG) to study the ongoing thoughts of participants instructed to retrieve self-relevant past episodes for periods of 20s. These task-initiated, participant-driven activity patterns were compared to a distinct condition where participants performed serial mental arithmetic operations, thereby shifting from self-related to self-unrelated thoughts. BOLD activity mapping revealed selective activity changes across conditions, namely in temporal, parietal and occipital areas ("posterior hot zone"), evincing their role in integrating the re-experienced past events into conscious representations during memory retrieval. Functional connectivity analysis showed that these regions were organized in two major subparts of the default mode network, previously associated to "scene-reconstruction" and "self-experience" subsystems. EEG microstate analysis allowed studying these brief participant-driven thoughts in the millisecond range. While the microstate topographies were found stable across conditions, the occurrence and duration of specific microstates were selectively modulated. EEG source analysis revealed similar spatial distributions between the sources of these microstates and the regions identified with fMRI. These findings imply a functional link between BOLD activity changes in regions related to a certain mental activity and the temporal dynamics of mentation, and support growing evidence that specific fMRI networks can be captured with EEG as repeatedly occurring, integrated brief periods of synchronized neuronal activity, lasting only fractions of seconds.