The brain is in a state of perpetual reverberant neural activity, even in the absence of specific tasks or stimuli. Shedding light on the origin and functional significance of such activity is essential to understanding how the brain transmits, processes, and stores information. An inspiring, albeit controversial, conjecture proposes that some statistical characteristics of empirically observed neuronal activity can be understood by assuming that brain networks operate in a dynamical regime near the edge of a phase transition. Moreover, the resulting critical behavior, with its concomitant scale invariance, is assumed to carry crucial functional advantages. Here, we present a data-driven analysis based on simultaneous high-throughput recordings of the activity of thousands of individual neurons in various regions of the mouse brain. To analyze these data, we construct a unified theoretical framework that synergistically combines cutting-edge methods for the study of brain activity (such as a phenomenological renormalization group approach and techniques that infer the general dynamical state of a neural population), while designing complementary tools. This unified approach allows us to uncover strong signatures of scale invariance that is “quasi-universal” across brain regions and reveal that these areas operate, to a greater or lesser extent, at the edge of instability. Furthermore, this framework allows us to distinguish between quasi-universal background activity and non-universal input-related activity. Taken together, the following study provides strong evidence that brain networks actually operate in a critical regime which, among other functional advantages, provides them with a scale-invariant substrate of activity in which optimal input representations can be sustained.