Representational drift under spontaneous activity -- self-organized criticality enhances representational reliability

Abstract: Neural systems face the challenge of maintaining reliable representations amid variations from plasticity and spontaneous activity. In particular, the spontaneous dynamics in neuronal circuit is known to operate near a highly variable critical state, which intuitively contrasts with the requirement of reliable representation. It is intriguing to understand how reliable representation could be maintained or even enhanced by critical spontaneous states. We firstly examined the co-existence of the scale-free avalanche in the spontaneous activity of mouse visual cortex with restricted representational geometry manifesting representational reliability amid the representational drift with respect to the visual stimulus. To explore how critical spontaneous state influences the neural representation, we built an excitation-inhibition network with homeostatic plasticity, which self-organizes to the critical spontaneous state. This model successfully reproduced both representational drift and restricted representational geometry observed experimentally, in contrast with randomly shuffled plasticity which causes accumulated drift of representational geometry. We further showed that the self-organized critical state enhances the cross-session low-dimensional representation, comparing to the non-critical state, by restricting the synapse weight into a low variation space. Our findings suggest that spontaneous self-organized criticality serves not only as a ubiquitous property of neural systems but also as a functional mechanism for maintaining reliable information representation under continuously changing networks, providing a potential explanation how the brain maintains consistent perception and behavior despite ongoing synaptic rewiring.