Efficiency and Cost of Economical Brain Functional Networks

Abstract

Brain anatomical networks are sparse, complex, and have economical small-world properties. We investigated the efficiency and cost of human brain functional networks measured using functional magnetic resonance imaging (fMRI) in a factorial design: two groups of healthy old ( N = 11; mean age = 66.5 years) and healthy young ( N = 15; mean age = 24.7 years) volunteers were each scanned twice in a no-task or “resting” state following placebo or a single dose of a dopamine receptor antagonist (sulpiride 400 mg). Functional connectivity between 90 cortical and subcortical regions was estimated by wavelet correlation analysis, in the frequency interval 0.06–0.11 Hz, and thresholded to construct undirected graphs. These brain functional networks were small-world and economical in the sense of providing high global and local efficiency of parallel information processing for low connection cost. Efficiency was reduced disproportionately to cost in older people, and the detrimental effects of age on efficiency were localised to frontal and temporal cortical and subcortical regions. Dopamine antagonism also impaired global and local efficiency of the network, but this effect was differentially localised and did not interact with the effect of age. Brain functional networks have economical small-world properties—supporting efficient parallel information transfer at relatively low cost—which are differently impaired by normal aging and pharmacological blockade of dopamine transmission.

Author Summary

It is increasingly evident that many complex networks, in diverse fields and over a wide range of spatial and time scales, may have topological properties in common. These unifying organizational principles have been described in terms of “small-world” parameters—meaning that many networks have both local clustering of connections and a short path length between any pair of nodes. Recent work has shown that we can also define small-world networks as having high global and local efficiency of parallel information transfer; and that many networks are economical in the sense of supporting high efficiency for low cost. Here we extend these ideas for the first time to an analysis of human brain functional networks derived from functional magnetic resonance imaging data. We show that human brain functional networks have economical small-world properties and that economical performance of these networks is detrimentally but differently affected by normal aging and by treatment with a dopamine receptor antagonist. The results illustrate concepts and techniques that could be important in further exploration of developmental, pathological, and pharmacological effects on human brain functional networks. They are also likely to be generalisable to applications in other fields of computational biology.