Functional independence in resting-state connectivity facilitates higher-order cognition

Abstract

Growing evidence suggests that intrinsic functional connectivity (i.e. highly structured patterns of communication between brain regions during wakeful rest) may encode cognitive ability. However, the generalizability of these findings is limited by between-study differences in statistical methodology and cognitive domains evaluated. To address this barrier, we evaluated resting-state neural representations of multiple cognitive domains within a relatively large normative adult sample. Forty-four participants (mean(sd) age=31(10) years; 18 male and 26 female) completed a resting-state functional MRI scan and neuropsychological assessments spanning motor, visuospatial, language, learning, memory, attention, working memory, and executive function performance. Robust linear regression related cognitive performance to resting-state connectivity among 200 a priori determined functional regions of interest (ROIs). Only higher-order cognitions (such as learning and executive function) demonstrated significant relationships between brain function and behavior. Additionally, all significant relationships were negative - characterized by moderately positive correlations among low performers and weak to moderately negative correlations among high performers. These findings suggest that functional independence among brain regions at rest facilitates cognitive performance. Our interpretation is consistent with graph theoretic analyses which represent the brain as independent functional nodes that undergo dynamic reorganization with task demand. Future work will build upon these findings by evaluating domain-specific variance in resting-state neural representations of cognitive impairment among patient populations.

Keywords: Attention; Connectome; Executive functioning; Individual differences; Memory; fMRI.

Fig. 1

Relationship of working memory to resting-state brain connectivity. Digit Span Sequencing performance negatively regressed to resting-state functional connectivity of right middle occipital gyrus (bordering superior parietal lobule) to bilateral dorsomedial prefrontal cortex (top). Spatial Span Forward performance negatively regressed to functional connectivity of right fusiform/parahippocampal gyrus with right lateral premotor area (bottom). All depicted relationships survived FDR correction (q ≤ 0.05). Scatterplots indicate significant robust linear regressions between performance (abscissa) and functional connectivity (ordinate), with data points indicated by subject number (01-79). ROIs are color-coded by region for all figures: light green for prefrontal, yellow for cingulate, red for striatum, magenta for sensorimotor, cyan for temporal, blue for occipital, and dark green for cerebellum. Brain connectivity is depicted with BrainNet Viewer (Xia, Wang, & He, 2013).

Fig. 2

Relationship of learning to resting-state brain connectivity. Brief Visuospatial Memory Test – Revised performance negatively regressed to resting-state functional connectivity of left ventrolateral prefrontal cortex to right superior lobule (top). California Verbal Learning Test performance negatively regressed to functional connectivity of left rostrolateral prefrontal cortex (adjacent to the ventrolateral prefrontal cortex region) with right frontal eye fields (bottom). All depicted relationships survived FDR correction (q ≤ 0.05).

Fig. 3

Relationship of executive function to resting-state brain connectivity. D-KEFS Color-Word Interference Performance (Color-Word condition minus Color condition) negatively regressed to four pairs of resting-state connectivity: connectivity of right superior dorsolateral prefrontal cortex with bilateral anterior insula, and right posterior inferior parietal cortex with bilateral pre-SMA/dorsal anterior cingulate (top). Performance on D-KEFS Trail Making Test Condition IV negatively regressed to resting-state functional connectivity of right ventrolateral prefonrtal Cortex with left superior parietal lobule (bottom). All depicted relationships survived FDR correction (q ≤ 0.05).