Hyper-Hierarchical Brain States Are Associated with Disorders of Consciousness

Abstract

BackgroundConsciousness is increasingly understood as an emergent property of large-scale brain dynamics that depend upon flexible interactions among distributed cortical and subcortical systems. Although disorders of consciousness (DOC) have traditionally been associated with impaired integration and reduced network complexity, the role of hierarchical brain organization in supporting conscious awareness remains poorly understood. Here, we investigated how hierarchical organization relates to behavioral responsiveness in DOC by combining trophic-level analysis, trophic coherence, and whole-brain dynamical metrics. MethodsResting-state functional MRI data were analyzed from healthy controls (CNT), minimally conscious state (MCS) patients, and unresponsive wakefulness syndrome (UWS) patients drawn from a previously published DOC cohort. Static global and regional measures of functional hierarchy were computed from directed effective-connectivity networks. Dynamic trophic states were identified using time-resolved phase-coupling analyses and clustering of recurrent coordination patterns. State occupancy, dwell time, metastability, synchrony, and behavioral associations with Coma Recovery Scale-Revised (CRS-R) scores were evaluated. ResultsRegional trophic levels were positively associated with behavioral responsiveness, with higher frontal and thalamic trophic levels and lower insular trophic levels predicting higher Coma Recovery Scale-Revised (CRS-R) scores. Dynamic trophic-state analysis identified a pathological hyper-hierarchical state, defined by elevated frontal, thalamic, and insular trophic levels, that exhibited progressively greater occupancy and longer dwell times from healthy controls to minimally conscious state and unresponsive wakefulness syndrome patients. In contrast, occupancy and dwell time of this state distinguished diagnostic groups but were not significantly associated with behavioral responsiveness. Independent analyses demonstrated significant reductions in metastability and global synchrony across disorders of consciousness. Anatomical mapping localized elevated trophic levels within the pathological state predominantly to fronto-thalamo-limbic systems. ConclusionsDisorders of consciousness are characterized not simply by loss of hierarchical organization but by prolonged stabilization within recurrent hyper-hierarchical brain states. Conscious awareness appears to depend not only on hierarchical organization itself but also on the capacity to flexibly transition between distinct brain states. Severe disorders of consciousness are associated with persistent occupation of pathological hyper-hierarchical states, potentially restricting the dynamical repertoire available for conscious processing.