Human Brain Functional Network Changes Associated with Enhanced and Impaired Attentional Task Performance

Abstract

How is the cognitive performance of the human brain related to its topological and spatial organization as a complex network embedded in anatomical space? To address this question, we used nicotine replacement and duration of attentionally demanding task performance (time-on-task), as experimental factors expected, respectively, to enhance and impair cognitive function. We measured resting-state fMRI data, performance and brain activation on a go/no-go task demanding sustained attention, and subjective fatigue in n ϭ 18 healthy, briefly abstinent, cigarette smokers scanned repeatedly in a placebo-controlled, crossover design. We tested the main effects of drug (placebo vs Nicorette gum) and time-on-task on behavioral performance and brain functional network metrics measured in binary graphs of 477 regional nodes (efficiency, measure of integrative topology; clustering, a measure of segregated topology; and the Euclidean physical distance between connected nodes, a proxy marker of wiring cost). Nicotine enhanced attentional task performance behaviorally and increased efficiency, decreased clustering, and increased connection distance of brain networks. Greater behavioral benefits of nicotine were correlated with stronger drug effects on integrative and distributed network configuration and with greater frequency of cigarette smoking. Greater time-on-task had opposite effects: it impaired attentional accuracy, decreased efficiency, increased clustering, and decreased connection distance of networks. These results are consistent with hypothetical predictions that superior cognitive performance should be supported by more efficient, integrated (high capacity) brain network topology at greater connection distance (high cost). They also demonstrate that brain network analysis can provide novel and theoretically principled pharmacodynamic biomarkers of pro-cognitive drug effects in humans.

Quantifying the Reconfiguration of Intrinsic Networks during Working Memory

“…This increased integration underlying increased performance has been previously observed, with greater integration across the entire brain underlying increased IQ across individuals [9], increased behavioral performance on a continuous performance task [33], and increased speed on an N-back WM task [20]. This study complements and extends those findings in two ways.…”

Top-down cortical interactions in visuospatial attention

“…This enhancement could reflect greater transmission fidelity from VOC to the frontoparietal areas that relaxes once the target stimulus disappears, a notion consistent with the putative gain enhancement of visual neurons thought to be driven by stimulus-independent, top-down influence. Independent of this speculation, these phasic effects indicate that increases in attentional demand drove greater integration between DAN and VOC components, consistent with the notion that cognitive demand induces greater integration among distributed regions via strengthening of long-range connectivity (Varela et al 2001; Kitzbichler et al 2011; Giessing et al 2013; Cohen et al 2014). …”

Effects of chronic and acute stimulants on brain functional connectivity hubs

“…This interpretation is consistent with the idea that MPH enhances attention and goal-directed action (Moeller et al, 2014; Pauls et al, 2012) and reduces brain-energy requirements needed for these kinds of functions (Swanson et al, 2011; Volkow et al, 2008). While this hypothesis remains to be directly tested, in support of this idea a previous study (Giessing et al, 2013) found that acute nicotine modified resting state network topology by increasing global efficiency and decreasing clustering (number of local connections) in the basal ganglia and thalamus among other regions, as indicative of a more integrative network configuration, whereas continuous performance on a cognitively demanding task had the opposite effects. Both manipulations (acute nicotine and time-on-task) were further differentially associated with attentional performance in the expected direction (enhanced by nicotine and impaired by cognitive fatigue).…”