Brain state expression and transitions are related to complex executive cognition in normative neurodevelopment

Abstract

Adolescence is marked by rapid development of executive function. Mounting evidence suggests that executive function in adults may be driven by dynamic control of neurophysiological processes. Yet, how these dynamics evolve over adolescence and contribute to cognitive development is unknown. In a sample of 780 youth aged 8-22 yr (42.7% male) from the Philadelphia Neurodevelopment Cohort, we use a dynamic graph approach to extract activation states in BOLD fMRI data from 264 brain regions. We construct a graph in which each observation in time is a node and the similarity in brain states at two different times is an edge. Using this graphical approach, we identify two primary brain states reminiscent of intrinsic and task-evoked systems. We show that time spent in these two states is higher in older adolescents, as is the flexibility with which the brain switches between them. Increasing time spent in primary states and flexibility among states relates to increases in a complex executive accuracy factor score over adolescence. Flexibility is more positively associated with accuracy toward early adulthood. These findings suggest that brain state dynamics are associated with complex executive function across a critical period of adolescence.

Development of Dynamic Functional Architecture during Early Infancy

“…Emerging data demonstrate the time-varying properties of FC change across years of childhood to support a remarkable range of emerging cognitive abilities (Marusak et al, 2017). For instance, previous studies revealed age-related development in the frequency and dwelling time (how long the brain spends on a given mode) of specific FC "modes" Hutchison and Morton, 2015;Qin et al, 2015;Marusak et al, 2017;Medaglia et al, 2018) and between-state transitions from late childhood to young adult Qin et al, 2015). Such developmental changes in the dynamic FC are related to the reduced behavioral variability and more accurate performance (McIntosh et al, 2008).…”

“…Many behavioral studies have presented various emerging high-order cognitive functions in the first a few years of life, such as self-awareness (Amsterdam, 1972), spatial attention (Haith et al, 1988), and working memory (Reznick, 2008). All these skills request better cognitive flexibility, controllability, adaptivity for brain regions to accommodate and adapt to quickly changing environments (Medaglia et al, 2018). For example, to respond to the internal (i.e., feelings about self) and external stimuli (i.e., multimodal sensory input from the environment) promptly, the task control and attention control regions in the infant brains are more likely to become increasingly variable with increased FC flexibility, i.e., their FC profiles could be more variable, linking different functional systems at different time for their coordination and communication.…”

“…Such developmental changes in the dynamic FC are related to the reduced behavioral variability and more accurate performance (McIntosh et al, 2008). However, all existing evidence comes from the age groups spanning from late childhood (>7) to young adult Hutchison and Morton, 2015;Qin et al, 2015;Marusak et al, 2017;Medaglia et al, 2018).…”

Dynamic functioning of transient resting‐state coactivation networks in the Human Connectome Project

“…The application of the above methods has indicated that network dynamics are relevant to psychological processes. For example, research has yielded early evidence that network dynamics are associated with individual differences in development (Faghiri, Stephen, Wang, Wilson, & Calhoun, ; Hutchison & Morton, ; Marusak et al, ; Tian, Li, Wang, & Yu, ) and cognitive functioning (Cohen, ; Kaiser et al, ; Medaglia et al, ), and can provide insight into mental health (Damaraju et al, ; Kaiser et al, , ; Kaiser, Snyder, et al, ; Ma, Calhoun, Phlypo, & Adali, ; Rashid et al, ; Rashid, Damaraju, Pearlson, & Calhoun, ). However, more work is needed to evaluate the reliability of the spatial organization of TNS, and to understand the extent to which these properties are common across people or time.…”

Linking flexibility of brain networks to cognitive development in preschool children

“…Importantly, numerous studies in adults have shown evidence for the dynamic nature of FC characterized by the variations of connection strengths, the sign of interactions or changes in node membership among modules Hutchison et al (2013) during task conditions as well as rest Calhoun et al (2014). Further such transient nature of brain network is reported to increase over development Chai et al (2017), and directly related with learning Bassett et al (2011), task performance Shine et al (2016); Keerativittayayut et al (2018), executive functions Medaglia et al (2018), and in general, with healthy cognitive functioning Thomas Yeo et al (2011) including general intelligence Barbey (2018) and creativity Li et al (2017); Sun et al (2018)…”