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WIREs Cogn Sci
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Resting‐state functional connectivity MRI reveals active processes central to cognition

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Analysis of spontaneously correlated low‐frequency activity fluctuations across the brain using functional magnetic resonance imaging (MRI)—commonly referred to as resting‐state functional connectivity (RSFC) MRI—was initially seen as a useful tool for mapping functional‐anatomic networks in the living human brain, characterizing brain changes and differences in clinical populations, and studying comparative anatomy across species. However, little was known about the potential relevance of RSFC to cognitive processes. Indeed, there has been considerable controversy and debate as to the utility of studying the resting‐state in cognitive neuroscience. However, recent work has shown that RSFC, rather than merely reflecting passive or epiphenomenal activity within underlying functional‐anatomic networks, reveals important dynamic processes that play an active role in cognition. RSFC has been associated with individual differences in a number of behavioral and cognitive domains, including perception, language, learning and memory, and the organization of conceptual knowledge. In this article, we review and integrate the latest research demonstrating that RSFC is functionally relevant to human behavior and higher‐level cognition, and propose a hypothesis regarding its mechanism of action on functional network dynamics and cognition. We conclude that RSFC MRI will be an invaluable tool for future discovery of the fundamental neurocognitive interactions that underlie cognition. WIREs Cogn Sci 2014, 5:233–245. doi: 10.1002/wcs.1275 This article is categorized under: Neuroscience > Cognition Neuroscience > Physiology Neuroscience > Plasticity
Congruence of task‐evoked and resting‐state functional connectivity (RSFC) networks. Left lateral parietal lobe activity for (a) autobiographical planning, (b) visuospatial planning, and (c) activity common to these two planning tasks (left); and the (a) default, (b) dorsal attention, and (c) frontoparietal control RSFC networks (right). (a) Posterior inferior parietal lobule activity in autobiographical planning subsumes the posterior inferior parietal lobule cluster in the default resting‐state network. (b) Visuospatial planning engaged the same superior parietal lobule to MT+ arc seen in the posterior portion of the dorsal attention network. (C) The two planning tasks commonly engaged a dorsal segment of the anterior extent of the inferior parietal lobule, part of the frontoparietal control network. (Reprinted with permission from Ref . Copyright 2010 Elsevier Ltd)
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Illustration of the proposed mechanism of action of resting‐state functional connectivity (RSFC): experience‐dependent modulation leads to sustained network changes that facilitate future performance. Time 1: the RSFC network is comprised of two modules (i.e., communities) with a single connector hub. Time 2: Experience causes task‐driven activity and coupling between regions. Time 3: Sustained changes to the network may be either (a) Quantitative or (b) Qualitative. (a) Quantitative changes to the network at Time 3 reflect increases and/or decreases in the magnitude of RSFC among network nodes relative to Time 1, which may be associated with changes in task performance. (b) Qualitative changes in RSFC at Time 3 would reflect the pruning of RSFC or the addition of new RSFC among nodes relative to Time 1, both of which may be associated with changes in performance. Qualitative changes, however, may modify features of the network that are remote from the activity site. In the above example, new RSFC between modules reduces the importance of the connector hub, and causes a decrease in this node's ‘betweenness centrality’, a graph analytic measure of its contribution as an inter‐module connector hub. These remote changes may also be associated with performance. We review evidence supporting experience dependent quantitative changes. At this point, it is unclear if experience produces qualitative changes in RSFC. Line weights signify RSFC magnitude. Red circles indicate an increase in activity; blue circles, a decrease in activity. Red lines indicate an increase in coupling; blue lines, a decrease in coupling. Dotted line indicates the former location of a pruned connection. Initial network topology derived from Ref .
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Hemispheric functional asymmetry of the parahippocampal place area (PPA) is associated with differential resting‐state functional connectivity (RSFC). (a) Independently localized right (blue) and left (orange/yellow) PPA. (b) Percent signal change relative to fixation baseline for scenes in three repetition priming test conditions (repeated SAME, repeated SIMILAR, and NEW): A significant hemisphere by test condition interaction indicates hemispheric asymmetry of repetition suppression. Form‐specific perceptual processing in the right PPA is indicated by a graded repetition suppression effect, with a lower response for SIMILAR than NEW scenes and for SAME than SIMILAR scenes. Conversely, form‐abstract processing in the left PPA is indicated by equivalent suppression of the response for SIMILAR and SAME scenes relative to NEW scenes. (c) Whole‐brain RSFC analyses confirm hemispheric asymmetry of PPA connectivity, with differential RSFC of the right (blue scale) versus left (yellow/orange scale) PPA. The right PPA showed differentially higher correlations with primarily visual perceptual brain regions. The left PPA showed differentially higher correlations with regions primarily involved in abstract/conceptual processes. (Reprinted with permission from Ref . Copyright 2012 Oxford University Press)
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Resting‐state functional connectivity (RSFC) is modulated by previous task, which predicts future memory. (a) Region in the right inferior frontal gyrus (rIFG; circled) involved in both face‐ and scene‐processing showed a task by region of interest (ROI) interaction for RSFC with the fusiform face area (FFA) and parahippocampal place area (PPA) ROIs (b) Paired samples comparisons revealed a significant simple effect of task on subsequent RSFC between rIFG and both the FFA and PPA. (c) RSFC with the FFA increased during rest after a face‐task (‘face‐rest’) relative to after a scene‐task (‘scene‐rest’); conversely, (d) RSFC with the PPA increased during scene‐rest relative to face‐rest. Red and blue lines indicate RSFC with the FFA and PPA, respectively; solid lines and dotted lines indicate increased RSFC and decreased RSFC, respectively. (e) Modulation of the RSFC of the rIFG with category‐preferential visual regions during rest predicts subsequent memory. Across all participants, the magnitude of the interaction in rIFG was significantly correlated with subsequent recognition accuracy for scenes. (Reprinted with permission from Ref . Copyright 2010 Oxford University Press)
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Resting‐state functional connectivity (RSFC) of visual regions predicts visual perceptual performance. Individual differences in pre‐training RSFC predicted task fitness. Colored regions projected onto the lateral and medial cortical surfaces approximate visual (yellow, dorsal; green, ventral) and control (dark blue, prefrontal cortex; light blue, insula) regions. Task fitness was positively correlated with pre‐training RSFC (red arrows) between heterotopic (i.e., dorsal to ventral within and across hemispheres) but not homotopic (ventral to ventral and dorsal to dorsal across hemispheres) or local (within visual quadrant) visual regions. Conversely, task fitness was negatively correlated with pre‐training RSFC (blue arrow) between visual regions and both prefrontal and insular areas involved in cognitive control. (Reprinted with permission from Ref . Copyright 2012 National Academy of Sciences)
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