Alterations in rat brain modular organization during unconsciousness are dependent on communication efficiency and metabolic cost

Spontaneous brain activity exhibits a highly structured modular organization that varies across individuals and reconfigures over time. Although it has been proposed that brain organization is shaped by an economic trade-off between minimizing costs and facilitating efficient information transfer, it remains untested whether modular variability and its changes during unconscious conditions might be constrained by the economy of brain organization. We acquired functional MRI and FDG-PET in rats under three different levels of consciousness induced by propofol administration. We examined alterations in brain modular variability during loss of consciousness from mild sedation to deep anesthesia. We also investigated the relationships between modular variability with glucose metabolism and functional connectivity strength as well as their alterations during unconsciousness. We observed that modular variability increased during loss of consciousness. Critically, across-individual modular variability is oppositely associated with functional connectivity strength and cerebral metabolism, and with deepening dosage of anesthesia, becoming increasingly dependent on basal metabolism over functional connectivity. These results suggested that, propofol-induced unconsciousness may lead to brain modular reorganization, which are putatively shaped by re-negotiations between energetic resources and communication efficiency.