Behavioural relevance of spontaneous, transient brain network interactions in fMRI

How spontaneously fluctuating functional magnetic resonance imaging (fMRI) signals in different brain regions relate to behaviour has been an open question for decades. Correlations in these signals, known as functional connectivity, can be averaged over several minutes of data to provide a stable representation of the functional network architecture for an individual. However, associations between these stable features and behavioural traits have been shown to be dominated by individual differences in anatomy. Here, using kernel learning tools, we propose methods to assess and compare the relation between time-varying functional connectivity, time-averaged functional connectivity, structural brain data, and non-imaging subject behavioural traits. We applied these methods on Human Connectome Project resting-state fMRI data to show that time-varying fMRI functional connectivity, detected at time-scales of a few seconds, has associations with some behavioural traits that are not dominated by anatomy. Despite time-averaged functional connectivity accounting for the largest proportion of variability in the fMRI signal between individuals, we found that some aspects of intelligence could only be explained by time-varying functional connectivity. The finding that time-varying fMRI functional connectivity has a unique relationship to population behavioural variability suggests that it might reflect transient neuronal communication fluctuating around a stable neural architecture. Significance statement Complex cognition is dynamic and emerges from the interaction between multiple areas across the whole brain, i.e. from brain networks. Hence, the utility of functional MRI to investigate brain activity depends on how well it can capture time-varying network interactions. Here, we develop methods to predict behavioural traits of individuals from either time-varying functional connectivity, time-averaged functional connectivity, or structural brain data. We use these to show that the time-varying nature of functional brain networks in fMRI can be reliably measured and can explain aspects of behaviour not captured by structural data or time-averaged functional connectivity. These results provide important insights to the question of how the brain represents information and how these representations can be measured with fMRI.

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