Synchronization between prefrontal and posterior association cortex during human working memory

Abstract

We measured coherence between the electroencephalogram at different scalp sites while human subjects performed delayed response tasks. The tasks required the retention of either verbalizable strings of characters or abstract line drawings. In both types of tasks, a significant enhancement in coherence in the theta range (4-7 Hz) was found between prefrontal and posterior electrodes during 4-s retention intervals. During 6-s perception intervals, far fewer increases in theta coherence were found. Also in other frequency bands, coherence increased; however, the patterns of enhancement made a relevance for working memory processes seem unlikely. Our results suggest that working memory involves synchronization between prefrontal and posterior association cortex by phase-locked, low frequency (4-7 Hz) brain activity.

Figure 1

Schematic drawing of the events on each trial of the verbal (I, Top) and visuo-spatial (II, Bottom) working memory tasks. First a stimulus was presented for 6 s (perception). During the ensuing dark-screen interval of 4 s, subjects actively retained the stimulus in memory (retention). Finally, subjects reproduced the stimuli with paper and pencil (reproduction).

Figure 2

Sample of raw θ-coherence values obtained for recordings from one electrode pair (Fz-T5) during retention of character strings (black bars) and control (white bars). In seven of the 10 recording sessions, coherence is higher during retention. The Wilcoxon test indicates a significant increase in coherence (P < 0.02).

Figure 3

Enhanced coherence in the θ range (4–7 Hz) during preception and retention intervals. Connections between electrode sites represent significant increases of coherence above control (P < 0.05 or better). The significance level was evaluated by applying paired Wilcoxon tests to group results. The shaded areas indicate the range of positions of individual electrodes as determined in an MRI study (24). Note that the occipital electrodes (O1, O2) are placed not over primary visual areas, but closer to the parieto-temporo-occipital association region. (a) During retention of character strings in memory (task I), enhanced coherence appeared between prefrontal and posterior cortex. In posterior cortex, the left hemisphere was predominantly involved. (b) Coherence-increases during retention of abstract line drawings in memory (task II). Patterns of enhanced coherence were similar to those in the verbal memory task a, although more connections appeared in the right hemisphere.

Figure 4

Enhanced θ coherence (4–7 Hz) during perception of character strings (a) and line drawings (b) (P < 0.05 or better). The number of significant coherence-increases was small compared with the retention intervals. Furthermore, the two patterns showed no topographic similarity.

Figure 5

Enhanced coherence in the γ range (19–32 Hz) during retention and perception intervals (P < 0.05 or better). In both the visual and the verbal task, the topographic pattern during perception intervals (a and b) were similar to that during retention intervals (c and d). γ range coherence patterns were also similar between tasks. Compared with the θ patterns (Fig. 3), γ band coherence-increases involved a higher percentage of ipsilateral electrode pairs.