The Cognitive Critical Brain: Modulation of Criticality in Task-Engaged Regions

ABSTRACT The constantly evolving world necessitates a brain that can adapt and respond to rapid changes. The brain, conceptualized as a system performing cognitive functions through collective neural activity, has been shown to maintain a resting state characterized by near-critical neural activity, poised to respond to external stimuli. The dynamic adaptation of nearcriticality during various tasks, however, remains poorly understood. In this study, we utilized the prototypical Hamiltonian Ising model to investigate the modulation of near-criticality in neural activity at the cortical subsystem level during cognitive tasks. Specifically, we theoretically simulated cortical 2D-Ising models in silico using structural MRI data and empirically estimated the system state in vivo using functional MRI data. First, our findings corroborated previous studies that the resting state is typically near-critical as captured by the Ising model. Notably, we found that cortical subsystems changed their criticality levels heterogeneously during a naturalistic movie-watching task, where visual and auditory cortical regions were fine-tuned closer to criticality. A more fine-grained analysis of the ventral temporal cortex during an object recognition task revealed that only regions selectively responsive to a specific object category were tuned closer to criticality when processing that object category. In conclusion, our study supports the cognitive critical brain hypothesis that modulating the criticality of subsystems within the hierarchical modular brain may be a general mechanism for achieving diverse cognitive functions.