The cognitive critical brain: Modulation of criticality in perception-related cortical regions

The constantly evolving world necessitates a brain that can swiftly 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 dynamics, positioning it to effectively respond to external stimuli. However, how near-criticality is dynamically modulated during task performance remains insufficiently understood. In this study, we utilized the prototypical Ising Hamiltonian model to investigate the modulation of near-criticality in neural activity at the cortical subsystem level during perceptual tasks. Specifically, we simulated 2D-Ising models in silico using structural MRI data and empirically estimated the system's state in vivo using functional MRI data. We first replicated previous findings that the resting state is typically near-critical as captured by the Ising model. Importantly, we observed heterogeneous changes in criticality across cortical subsystems during a naturalistic movie-watching task, with visual and auditory regions fine-tuned closer to criticality. A more fine-grained analysis of the ventral temporal cortex during an object recognition task further 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 provides empirical evidence from the domain of perception supporting the cognitive critical brain hypothesis that modulating the criticality of subsystems within the brain's hierarchical and modular organization may be a fundamental mechanism for achieving diverse cognitive functions.