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Abstract A diverse set of white matter connections supports seamless transitions between cognitive states. However, it remains unclear how these connections guide the temporal progression of large-scale brain activity patterns in different cognitive states. Here, we analyze the brain’s trajectories across a set of single time point activity patterns from functional magnetic resonance imaging data acquired during the resting state and an n-back working memory task. We find that specific temporal sequences of brain activity are modulated by cognitive load, associated with age, and related to task performance. Using diffusion-weighted imaging acquired from the same subjects, we apply tools from network control theory to show that linear spread of activity along white matter connections constrains the probabilities of these sequences at rest, while stimulus-driven visual inputs explain the sequences observed during the n-back task. Overall, these results elucidate the structural underpinnings of cognitively and developmentally relevant spatiotemporal brain dynamics. 

Executive function is a quintessential human capacity that emerges late in development and displays different developmental trends in males and females. Sex differences in executive function in youth have been linked to vulnerability to psychopathology as well as to behaviors that impinge on health, wellbeing, and longevity. Yet, the neurobiological basis of these differences is not well understood, in part due to the spatiotemporal complexity inherent in patterns of brain network maturation supporting executive function. Here we test the hypothesis that sex differences in impulsivity in youth stem from sex differences in the controllability of structural brain networks as they rewire over development. Combining methods from network neuroscience and network control theory, we characterize the network control properties of structural brain networks estimated from diffusion imaging data acquired in males and females in a sample of 879 youth aged 8–22 years. We summarize the control properties of these networks by estimating average and modal controllability, two statistics that probe the ease with which brain areas can drive the network towards easy versus difficult-to-reach states. We find that females have higher modal controllability in frontal, parietal, and subcortical regions while males have higher average controllability in frontal and subcortical regions. Furthermore, controllability profiles in males are negatively related to the false positive rate on a continuous performance task, a common measure of impulsivity. Finally, we find associations between average controllability and individual differences in activation during an n-back working memory task. Taken together, our findings support the notion that sex differences in the controllability of structural brain networks can partially explain sex differences in executive function. Controllability of structural brain networks also predicts features of task-relevant activation, suggesting the potential for controllability to represent context- specific constraints on network state more generally. 

Adolescents are known for taking risks, from driving too fast to experimenting with drugs and alcohol. Such behaviors tend to decrease as individuals move into adulthood. Most people in their mid-twenties have greater self-control than they did as teenagers. They are also often better at planning, sustaining attention, and inhibiting impulsive behaviors. These skills, which are known as executive functions, develop over the course of adolescence. Executive functions rely upon a series of brain regions distributed across the frontal lobe and the lobe that sits just behind it, the parietal lobe. Fiber tracts connect these regions to form a fronto-parietal network. These fiber tracts are also referred to as white matter due to the whitish fatty material that surrounds and insulates them. Cui et al. now show that changes in white matter networks have implications for teen behavior. Almost 950 healthy young people aged between 8 and 23 years underwent a type of brain scan called diffusion-weighted imaging that visualizes white matter. The scans revealed that white matter networks in the frontal and parietal lobes mature over adolescence. This makes it easier for individuals to activate their fronto-parietal networks by decreasing the amount of energy required. Cui et al. show that a computer model can predict the maturity of a person's brain based on the energy needed to activate their fronto-parietal networks. These changes help explain why executive functions improve during adolescence. This in turn explains why behaviors such as risk-taking tend to decrease with age. That said, adults with various psychiatric disorders, such as ADHD and psychosis, often show impaired executive functions. In the future, it may be possible to reduce these impairments by applying magnetic fields to the scalp to reduce the activity of specific brain regions. The techniques used in the current study could help reveal which brain regions to target with this approach.