Observations of neurons in a resting brain and neurons in cultures often display spontaneous scale-free (SF) 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 behavior and whether it persists under behavioral transitions has remained a fundamental knowledge gap. Here, we aim to tackle this challenge by studying behavioral transitions in mice using two-photon calcium imaging of the retrosplenial cortex (RSC)—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 behavioral 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 RSC contains at least one sub-population capable of switching between two different SF regimes, indicating an intricate relationship between behavior 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.