Dynamic reorganization of human resting-state networks during visuospatial attention

• Published in: Proceedings of the National Academy of Sciences - PNAS 2015-06, Vol.112 (26), p.8112-8117
• Main Authors: Spadone, Sara, Stefania Della Penna, Carlo Sestieri, Viviana Betti, Annalisa Tosoni, Mauro Gianni Perrucci, Gian Luca Romani, Maurizio Corbetta
• Format: Article
• Language: English
• Subjects: Adult; Animals; Attention - physiology; attention networks; Behavior; Behavior, Animal; Biological Sciences; Brain; Brain - physiology; directional connectivity; functional connectivity; Humans; Magnetic Resonance Imaging; neurophysiology; Neurosciences; resting-state networks; task-evoked activity; Vision, Ocular - physiology; Visual task performance; Young Adult
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1415439112

Significance The brain is never at rest, and patterns of ongoing correlated activity have been found to resemble patterns during active behavior. A fundamental problem in neuroscience concerns the relationship between spontaneous and task-driven activity. During a demanding task that requires selective attention to sensory stimuli, correlated patterns of spontaneous (rest) activity are generally preserved. However, specific changes in synchronization occur within and between networks that correlate with behavioral performance. These results indicate that attention modifies spontaneous activity patterns in support of task performance. Fundamental problems in neuroscience today are understanding how patterns of ongoing spontaneous activity are modified by task performance and whether/how these intrinsic patterns influence task-evoked activation and behavior. We examined these questions by comparing instantaneous functional connectivity (IFC) and directed functional connectivity (DFC) changes in two networks that are strongly correlated and segregated at rest: the visual (VIS) network and the dorsal attention network (DAN). We measured how IFC and DFC during a visuospatial attention task, which requires dynamic selective rerouting of visual information across hemispheres, changed with respect to rest. During the attention task, the two networks remained relatively segregated, and their general pattern of within-network correlation was maintained. However, attention induced a decrease of correlation in the VIS network and an increase of the DAN→VIS IFC and DFC, especially in a top-down direction. In contrast, within the DAN, IFC was not modified by attention, whereas DFC was enhanced. Importantly, IFC modulations were behaviorally relevant. We conclude that a stable backbone of within-network functional connectivity topography remains in place when transitioning between resting wakefulness and attention selection. However, relative decrease of correlation of ongoing “idling” activity in visual cortex and synchronization between frontoparietal and visual cortex were behaviorally relevant, indicating that modulations of resting activity patterns are important for task performance. Higher order resting connectivity in the DAN was relatively unaffected during attention, potentially indicating a role for simultaneous ongoing activity as a “prior” for attention selection.