Neural Networks Are Tuned Near Criticality During a Cognitive Task and Distanced from Criticality In a Psychopharmacological Model of Alzheimer's Disease

Dynamical systems exhibit transitions between ordered and disordered states and "criticality" occurs when the system lies at the borderline between these states at which the input is neither strongly damped nor excessively amplified. Impairments in brain function such as dementia or epilepsy could arise from failure of adaptive criticality, and deviation from criticality may be a potential biomarker for cognition-related neurological and psychiatric impairments. Miniscope wide-field calcium imaging of several hundred hippocampal CA1 neurons in freely-behaving mice was studied during rest, a cognitive task of novel object recognition (NOR), and novel object recognition following scopolamine administration that greatly impairs spatial memory encoding. We find that while hippocampal networks exhibit characteristics of a near-critical system at rest, the network activity shifts significantly closer to a critical state when the mice engaged in the NOR task. The dynamics shift away from criticality with impairment of novel object performance due to scopolamine-induced memory impairment. These results support the concept that hippocampal neural networks move closer to criticality when successfully processing increased cognitive load, taking advantage of maximal dynamical range, information content, and transmission that occur in critical regimes.