Carrying the past to the future: Distinct brain networks underlie individual differences in human spatial working memory capacity

ABSTRACT Spatial working memory (SWM) relies on the interplay of anatomically separated and interconnected large‐scale brain networks. EEG studies often observe load‐associated sustained negative activity during SWM retention. Yet, whether and how such sustained negative activity in retention relates to network‐specific functional activation/deactivation and relates to individual differences in SWM capacity remain to be elucidated. To cover these gaps, we recorded concurrent EEG‐fMRI data in 70 healthy young adults during the Sternberg delayed‐match‐to‐sample SWM task with three memory load levels. To a subset of participants (N=28) that performed the task properly and had artefact‐free fMRI and EEG data, we employed a novel temporo‐spatial principal component analysis to derive load‐dependent negative slow wave (NSW) from retention‐related event‐related potentials. The associations between NSW responses with SWM capacity were divergent in the higher (N=14) and lower (N=14) SWM capacity groups. Specifically, larger load‐related increase in NSW amplitude was associated with greater SWM capacity for the higher capacity group but lower SWM capacity for the lower capacity group. Furthermore, for the higher capacity group, larger NSW amplitude was related to greater activation in bilateral parietal areas of the fronto‐parietal network (FPN) and greater deactivation in medial frontal gyrus and posterior mid‐cingulate cortex of the default mode network (DMN) during retention. In contrast, the lower capacity group did not show similar pattern. Instead, greater NSW was linked to higher deactivation in right posterior middle temporal gyrus. Our findings shed light on the possible differential EEG‐informed neural network mechanism during memory maintenance underlying individual differences in SWM capacity. HIGHLIGHTSNegative slow wave (NSW) is related to spatial working memory (SWM) load during retentionNSW in the high and low capacity groups showed divergent associations with SWM capacity and network activitiesNSW was related to higher FPN activation and DMN deactivation in the high capacity groupNSW was related to greater temporal deactivation in the low capacity groupDistinct NSW‐related brain networks are related to individual differences in SWM capacities