Brain activity dynamics after traumatic brain injury indicate increased state transition energy and preference of lower order states

Traumatic Brain Injury (TBI) can cause structural damage to the neural tissue and white matter connections in the brain, disrupting its functional coactivation patterns. Although there are a wealth of studies investigating TBI-related changes in the brain’s structural and functional connectomes, fewer studies have investigated TBI-related changes to the brain’s dynamic landscape. Network control theory is a framework that integrates structural connectomes and functional time-series to quantify brain dynamics. Using this approach, we analyzed longitudinal trajectories of brain dynamics from acute to chronic injury phases in two cohorts of individuals with mild and moderate to severe TBI, and compared them to non-brain-injured, age- and sex-matched control individuals’ trajectories. Our analyses suggest individuals with mild TBI initially have brain activity dynamics similar to controls but then shift in the subacute and chronic stages of the injury (1 month and 12 months post-injury) to favor lower-order visual-dominant states compared to higher-order default mode dominant states. We further find that, compared to controls, individuals with mild TBI have overall decreased entropy and increased transition energy demand in the sub-acute and chronic stages that correlates with poorer attention performance. Finally, we found that the asymmetry in top-down to bottom-up transition energies increased in subacute and chronic stages of mild TBI, possibly indicating decreased efficacy of top-down inhibition. We replicate most findings with the moderate to severe TBI dataset, indicating their robustness, with the notable exception of finding the opposite correlation between global transition energy and mean reaction time (MRT). We attribute differences to the cohorts’ varied injury severity, with perhaps a stronger compensatory mechanism in moderate to severe TBI. Overall, our findings reveal shifting brain dynamics after mild to severe TBI that relate to behavioral measures of attention, shedding light on post-injury mechanisms of recovery.