In this work we estimated differences in the structure of brain systems that ensure encoding and retention in working memory (WM) of two types of information: verbal (letters) and non-verbal (segments of an open broken line) sequences presented either statically or dynamically. Brain systems were characterized by the strength of functional and effective connections between eight approximately bilaterally symmetrical cortical loci, including the dorsolateral prefrontal cortex (dlPFC) and regions of the temporal (STG), parietal (IPS), and occipital (v2) cortices. Using an 8-channel vector autoregressive model in the space of cortical EEG sources, it was shown in a group of subjects in whom high-density EEG was recorded that: (1) the brain organization of the WM when holding a sequence of letters differs from that when holding a sequence of broken line segments; (2) the brain organization of the WM depends on the mode of presentation of sequences: the strength of the functional connection is different during dynamic and static presentation of the sequence; (3) differences in the structure of functional and effective connections are not of a pronounced frequency-selective nature and are observed in all studied EEG frequency ranges from theta (4–8 Hz) to high-frequency gamma (50–60 Hz); (4) the most reliable differences between the task of retaining a sequence of letters and the task of retaining a sequence of broken line segments are observed in the alpha and beta frequency ranges during static visual presentation of sequences in the strength of functional connectivity measured using coherence between the left hemisphere dlPFC and the right hemisphere STG, as well as in theta range between the right hemisphere dlPFC and the left visual cortex v2; (5) the most reliable difference between static and dynamic presentation modes is observed in the task of holding broken line segments in the gamma frequency range (50–60 Hz) between the dlPFC in the right hemisphere and the left visual cortex v2.