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.
Individuals differ in their cognitive resilience. Less resilient people demonstrate a greater tendency to vigilance decrements within sustained attention tasks. We hypothesized that a period of sustained attention is followed by prolonged changes in the organization of “resting state” brain networks and that individual differences in cognitive resilience are related to differences in post-task network reorganization. We compared the topological and spatial properties of brain networks as derived from functional MRI data (N = 20) recorded for 6 mins before and 12 mins after the performance of an attentional task. Furthermore we analysed changes in brain topology during task performance and during the switches between rest and task conditions. The cognitive resilience of each individual was quantified as the rate of increase in response latencies over the 32-minute time course of the attentional paradigm. On average, functional networks measured immediately post-task demonstrated significant and prolonged changes in network organization compared to pre-task networks with higher connectivity strength, more clustering, less efficiency, and shorter distance connections. Individual differences in cognitive resilience were significantly correlated with differences in the degree of recovery of some network parameters. Changes in network measures were still present in less resilient individuals in the second half of the post-task period (i.e. 6–12 mins after task completion), while resilient individuals already demonstrated significant reductions of functional connectivity and clustering towards pre-task levels. During task performance brain topology became more integrated with less clustering and higher global efficiency, but linearly decreased with ongoing time-on-task. We conclude that sustained attentional task performance has prolonged, “hang-over” effects on the organization of post-task resting-state brain networks; and that more cognitively resilient individuals demonstrate faster rates of network recovery following a period of attentional effort.
Reorienting of visuospatial attention can be investigated by comparing reaction times to validly and invalidly cued targets ("validity effect"). The cholinergic agonist nicotine reduces the validity effect and neural activity in the posterior parietal cortex. Behavioral effects of nicotine in nonsmokers are weak and it has been suggested that differences in baseline behavior before nicotine exposure may influence the effect of nicotine. This study investigates whether individual differences in reorienting-related neural activity under placebo may be used to predict individual nicotine effects. Individual nicotine effects are defined as the behavioral effects under nicotine that cannot be predicted by the behavioral data under placebo. Fifteen nonsmoking subjects were given either placebo or nicotine gum (2 mg) prior to performing a cued target detection task inside a magnetic resonance imaging scanner. The results of a partial least square analysis suggest that neural data under placebo can be used to predict individual behavioral effects of nicotine. Neural activity in the left posterior cingulate cortex, the right superior parietal cortex, the right dorsal medial prefrontal cortex, and the left ventral medial prefrontal cortex significantly contributes to that prediction. We conclude that nicotine effects on reorienting attention depend on individual differences in reorienting-related neural activity under placebo and suggest that functional magnetic resonance imaging data can contribute to the prediction of individual drug effects.
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