Cognitive fitness of cost-efficient brain functional networks - PubMed (original) (raw)

Cognitive fitness of cost-efficient brain functional networks

Danielle S Bassett et al. Proc Natl Acad Sci U S A. 2009.

Abstract

The human brain's capacity for cognitive function is thought to depend on coordinated activity in sparsely connected, complex networks organized over many scales of space and time. Recent work has demonstrated that human brain networks constructed from neuroimaging data have economical small-world properties that confer high efficiency of information processing at relatively low connection cost. However, it has been unclear how the architecture of complex brain networks functioning at different frequencies can be related to behavioral performance on cognitive tasks. Here, we show that impaired accuracy of working memory could be related to suboptimal cost efficiency of brain functional networks operating in the classical beta frequency band, 15-30 Hz. We analyzed brain functional networks derived from magnetoencephalography data recorded during working-memory task performance in 29 healthy volunteers and 28 people with schizophrenia. Networks functioning at higher frequencies had greater global cost efficiency than low-frequency networks in both groups. Superior task performance was positively correlated with global cost efficiency of the beta-band network and specifically with cost efficiency of nodes in left lateral parietal and frontal areas. These results are consistent with biophysical models highlighting the importance of beta-band oscillations for long-distance functional connections in brain networks and with pathophysiological models of schizophrenia as a dysconnection syndrome. More generally, they echo the saying that "less is more": The information processing performance of a network can be enhanced by a sparse or low-cost configuration with disproportionately high efficiency.

PubMed Disclaimer

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

Effciency and cost efficiency as a function of network cost. (A) Plot of global efficiency in the γ-band network versus cost averaged over all 6 blocks of 2-back trials for 1 healthy control (blue), 1 person with schizophrenia (red), a random network (black), and a regular network (green). (B) Plot of cost efficiency in the γ-band versus cost averaged over all six 2-back trials for the same subjects, random, and regular networks. Broken lines indicate the maximum cost efficiency for the healthy control (CEHC) and for the person with schizophrenia (CESCZ) and the costs at which these maximum differences occur: CHC and CSCZ, respectively.

Fig. 2.

Fig. 2.

Brain functional network properties as a function of frequency band for healthy volunteers (blue) and people with schizophrenia (red): average mutual information (A), efficiency (B), cost (C), and cost efficiency (D). Differences between groups significant at P < 0.05 uncorrected are identified by an asterisk. Error bars denote 95% confidence intervals. For specific t values and P values, see

Table S1

.

Fig. 3.

Fig. 3.

Head surface mapping of associations between nodal cost efficiency and performance accuracy (Left) and diagnostic group (Right) for functional networks operating in all classical frequency bands from γ (top row) to δ (bottom row). Red indicates an association was significant at P < 0.05 uncorrected, orange indicates that the association passed false-positive correction (all P < 0.0036), and bright yellow indicates that the association passed FDR correction (minimum P < 0.00018). The strongest associations between nodal cost efficiency and task accuracy were found in left frontal and parietal nodes of the β-band network.

Fig. 4.

Fig. 4.

Associations between cognitive performance and cost efficiency of β1 and β2 band networks. (A) Scatter plots of the significant relationships between accuracy and global cost efficiency for the β1-band (Left) and β2-band (Right) networks including regression lines for healthy controls (blue), people with schizophrenia (red), and both groups together (black). (B) Head surface maps showing regions where nodal cost efficiency in the β1-band (Left) and β2-band (Right) networks predicted accuracy of task performance across all subjects (Top), in healthy controls alone (Middle), and in schizophrenics alone (Bottom). As in the previous figure, red indicates an association between task accuracy and nodal cost efficiency was significant at P < 0.05 uncorrected, orange indicates that the association passed false-positive correction (all P < 0.0036), and bright yellow indicates that the association passed FDR correction (minimum P < 0.00018).

Similar articles

Cited by

References

    1. Chen BL, Hall DH, Chklovskii DB. Wiring optimization can relate neuronal structure and function. Proc Natl Acad Sci USA. 2006;103:4723–4728. - PMC - PubMed
    1. Latora V, Marchiori M. Efficient behavior of small-world networks. Phys Rev Lett. 2001;87:198701. - PubMed
    1. Achard S, Bullmore E. Efficiency and cost of economical brain functional networks. PLoS Comput Biol. 2007;3:e17. - PMC - PubMed
    1. Sporns O, Chialvo DR, Kaiser M, Hilgetag CC. Organization, development and function of complex brain networks. Trends Cognit Sci. 2004;8:418–425. - PubMed
    1. Salvador R, et al. Neurophysiological architecture of functional magnetic resonance images of human brain. Cereb Cortex. 2005;15:1332–1342. - PubMed

Publication types

MeSH terms

LinkOut - more resources