The temporal structure of self-generated cognition is a key attribute to the formation of a meaningful stream of consciousness. When at rest, our mind wanders from thought to thought in distinct mental states. Despite the marked importance of ongoing mental processes, 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 22sec. 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 enhanced activity in temporal, parietal and occipital areas during the memory compared to the mental arithmetic condition, 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, previously associated to “scene-reconstruction” and “self-experience” subsystems. EEG microstate analysis allowed studying these participant-driven thoughts in the millisecond range by determining the temporal dynamics of brief periods of stable scalp potential fields. This analysis revealed selective modulation of occurrence and duration of specific microstates in the memory and in the mental arithmetic condition, respectively. EEG source analysis revealed similar spatial distributions of 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 brief periods of integrated coherent neuronal activity, lasting only fractions of seconds.