Critical Dynamics Mediate Learning of New Distributed Memory Representations in Neuronal Networks

We explore the possible role of network dynamics near a critical point in the storage of new information in silico and in vivo, and show that learning and memory may rely on neuronal network features mediated by the vicinity of criticality. Using a mean-field, attractor-based model, we show that new information can be consolidated into attractors through state-based learning in a dynamical regime associated with maximal susceptibility at the critical point. Then, we predict that the subsequent consolidation process results in a shift from critical to sub-critical dynamics to fully encapsulate the new information. We go on to corroborate these findings using analysis of rodent hippocampal CA1 activity during contextual fear memory (CFM) consolidation. We show that the dynamical state of the CA1 network is inherently poised near criticality, but the network also undergoes a shift towards sub-critical dynamics due to successful consolidation of the CFM. Based on these findings, we propose that dynamical features associated with criticality may be universally necessary for storing new memories.