Deconstructing scale-free neuronal avalanches: behavioral transitions and neuronal response
Abstract Observations of neurons in a resting brain and neurons in cultures often display spontaneous scale-free collective dynamics in the form of information cascades, also called “neuronal avalanches”. This has motivated the so called critical brain hypothesis which posits that the brain is self-tuned to a critical point or regime, separating exponentially-growing dynamics from quiescent states, to achieve optimality. Yet, how such optimality of information transmission is related to behaviour and whether it persists under behavioural transitions has remained a fundamental knowledge gap. Here, we aim to tackle this challenge by studying behavioural transitions in mice using two-photon calcium imaging of the retrosplenial cortex -- an area of the brain well positioned to integrate sensory, mnemonic, and cognitive information by virtue of its strong connectivity with the hippocampus, medial prefrontal cortex, and primary sensory cortices. Our work shows that the response of the underlying neural population to behavioural transitions can vary significantly between different sub-populations such that one needs to take the structural and functional network properties of these sub-populations into account to understand the properties at the total population level. Specifically, we show that the retrosplenial cortex contains at least one sub-population capable of switching between two different scale-free regimes, indicating an intricate relationship between behaviour and the optimality of neuronal response at the subgroup level. This asks for a potential reinterpretation of the emergence of self-organized criticality in neuronal systems.