Neuronal synchrony reveals working memory networks and predicts individual memory capacity

Abstract

Visual working memory (VWM) is used to maintain sensory information for cognitive operations, and its deficits are associated with several neuropsychological disorders. VWM is based on sustained neuronal activity in a complex cortical network of frontal, parietal, occipital, and temporal areas. The neuronal mechanisms that coordinate this distributed processing to sustain coherent mental images and the mechanisms that set the behavioral capacity limit have remained unknown. We mapped the anatomical and dynamic structures of network synchrony supporting VWM by using a neuro informatics approach and combined magnetoencephalography and electroencephalography. Interareal phase synchrony was sustained and stable during the VWM retention period among frontoparietal and visual areas in alpha- (10-13 Hz), beta- (18-24 Hz), and gamma- (30-40 Hz) frequency bands. Furthermore, synchrony was strengthened with increasing memory load among the frontoparietal regions known to underlie executive and attentional functions during memory maintenance. On the other hand, the subjects' individual behavioral VWM capacity was predicted by synchrony in a network in which the intraparietal sulcus was the most central hub. These data suggest that interareal phase synchrony in the alpha-, beta-, and gamma-frequency bands among frontoparietal and visual regions could be a systems level mechanism for coordinating and regulating the maintenance of neuronal object representations in VWM.

Fig. 1.

Interareal phase synchrony in human cortex is robust, sustained, and memory load-dependent during VWM retention. (A) Example of a single experimental trial with a memory load of four and a test stimulus different from the sample stimulus. (B) Behavioral accuracy (mean ± SEM, n = 13) for the six memory load conditions. (C) Simplified graph showing the key graph theoretical concepts and the color code for Figs. 2–-4. d, vertex degree that is the number of connections (edges) the vertex has; K, connection density, which in this study indicates the proportion of edges in the graph (here, statistically significant interactions: A = 0.005, FDR < 0.01) from all possible edges. (D) Mean K during the VWM retention period as a function of frequency for average (black line) and load (gray line) conditions. Interareal phase synchrony in α-, β-, and γ-frequency bands is stronger during VWM retention than during baseline (black line) and is strengthened by the memory load increasing from one to six objects (gray line). (E) K of retention period α- (red), β- (green), and γ- (blue) frequency band networks obtained separately for each memory load condition (mean ± SEM across 16 retention period graphs per frequency band). The horizontal lines indicate the memory load pairs with a significantly different K (P < 0.05, Bonferroni corrected, n = 15). (F) Average condition K as a function of time shows sustained network synchrony during the VWM retention period in the α-, β-, and γ-bands (mean ± SEM and colors as in E, SEM bars are at time window centers, VWM retention period includes the four time windows between 0.4 and 1 s). (G) Load condition K as a function of time (mean ± SEM and colors as in E).

Fig. 2.

Structure of interareal interactions mediated by phase synchrony in α-, β-, and γ-frequency bands during VWM retention. (A) α-Band matching graph (M^E_min = 0.55, details provided in Fig. S3A). A matching graph reveals spectrally and temporally stable interactions that are likely to underlie the most important communication pathways. The underlying map shows the complete left and right flattened cerebral hemispheres with sulci colored according to the cortical region (Fig. 1C). Lines indicate interareal interactions and are colored according to the connected brain regions. Spheres and annotations indicate brain areas, with radii proportional to their degree. Yellow borders encircle areas with betweenness centrality values in the top 10th percentile. Brain regions with a large degree and betweenness centrality are the network hubs. The bolding of annotations indicates the top three hubs in individual graphs (Fig. S3B). (B) β-Band (18–24 Hz) matching graph (M^E_min = 0.3; Fig. S3 C and D). (C) γ-Band (30–40 Hz) matching graph (M^E_min = 0.5; Fig. S3 E and F). C, central; CA, calcarine; CI, cingulate; CN, cuneus; F, frontal; G, gyrus; IN, insula; P, parietal; S, sulcus; T, temporal; O, occipital; a, anterior; ang, angular; cal, callosal; col, collateral; i, inferior; int, intra; ist, isthmus; fus, fusiform; la, lateral; m, middle; orb, orbital; p, posterior; pa, para; pah, parahippocampal; pla, planum temporale and polare; pe, peri; pr, pre; po, post; s, superior; tr, transverse.

Fig. 3.

Retention period phase synchrony is strengthened among frontoparietal and visual regions with increasing memory load. (A) α-Band matching graph. Visualization as in Fig. 2 (M^E_min = 0.81; Fig. S5 A and B). (B) β-Band matching graph (M^E_min = 0.5; Fig. S5C). (C) γ-Band matching graph (M^E_min = 0.18; Fig. S5E). C, central; CA, calcarine; CI, cingulate; CN, cuneus; F, frontal; G, gyrus; IN, insula; P, parietal; S, sulcus; T, temporal; O, occipital; a, anterior; ang, angular; cal, callosal; col, collateral; i, inferior; int, intra; ist, isthmus; fus, fusiform; la, lateral; m, middle; orb, orbital; p, posterior; pa, para; pah, parahippocampal; pla, planum temporale and polare; pe, peri; pr, pre; po, post; s, superior; tr, transverse.

Fig. 4.

Individual behavioral VWM capacity is predicted by α- and β-band networks in which the intraparietal sulcus is the most central hub. (A) K as a function of frequency shows that the interactions correlated with individual VWM capacity are concentrated to the α- (here, 9–12 Hz) and β-bands. (B) Dynamics of K of the α- and β-band networks (mean ± SEM across 16 retention period graphs per frequency band). (C) α-Band matching graph for the VWM retention period (M^E_min = 0.35; details provided in Fig. S6A). (D) β-Band matching graph (M^E_min = 0.24; Fig. S6C). C, central; CA, calcarine; CI, cingulate; CN, cuneus; F, frontal; G, gyrus; IN, insula; P, parietal; S, sulcus; T, temporal; O, occipital; a, anterior; ang, angular; cal, callosal; col, collateral; i, inferior; int, intra; ist, isthmus; fus, fusiform; la, lateral; m, middle; orb, orbital; p, posterior; pa, para; pah, parahippocampal; pla, planum temporale and polare; pe, peri; pr, pre; po, post; s, superior; tr, transverse.