Hippocampal criticality tracks cognitive demand and shifts with memory impairment

Dynamical systems exhibit transitions between ordered and disordered states, and a "critical state" occurs when the system lies at the borderline between these phases, where input is neither strongly damped nor excessively amplified. Systems maintaining critical dynamics are considered adaptive, and it is widely believed that brains operate at near-critical states where memory encoding and information processing are optimized. Impairments in brain function, such as dementia or epilepsy, may arise from failure of adaptive criticality, making deviation from criticality a potential biomarker for cognition-related neurological and psychiatric impairments. Wide-field calcium imaging using miniscopes is performed to record activity of hundreds of hippocampal CA1 neurons in freely behaving mice during rest, a novel object recognition (NOR) task, and NOR following scopolamine administration that severely impairs spatial memory. We find that while hippocampal networks exhibit some features of a near-critical system at rest, network activity shifts significantly closer to a critical state during NOR, and away from criticality when memory performance is impaired by the muscarinic antagonist scopolamine. These results support that hippocampal networks move toward criticality with increasing cognitive load, leveraging maximal dynamical range, information content, and transmission of critical regimes, while pathophysiological impairment alters criticality metrics reflecting network-level effects.