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Activity cascades are found in many complex systems. In the cortex, they arise in the form of neuronal avalanches that capture ongoing and evoked neuronal activities at many spatial and temporal scales. The scale-invariant nature of avalanches suggests that the brain is in a critical state, yet predictions from critical theory on the temporal unfolding of avalanches have yet to be confirmed in vivo. Here we show in awake nonhuman primates that the temporal profile of avalanches follows a symmetrical, inverted parabola spanning up to hundreds of milliseconds. This parabola constrains how avalanches initiate locally, extend spatially and shrink as they evolve in time. Importantly, parabolas of different durations can be collapsed with a scaling exponent close to 2 supporting critical generational models of neuronal avalanches. Spontaneously emerging, transient γ-oscillations coexist with and modulate these avalanche parabolas thereby providing a temporal segmentation to inherently scale-invariant, critical dynamics. Our results identify avalanches and oscillations as dual principles in the temporal organization of brain activity.