Miller et al.The temporal profile of neuronal avalanches 2 ABSTRACT Activity cascades are found in many complex systems. In the cortex, they arise in the form of neuronal avalanches which 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, which describes how avalanches initiate locally, extend spatially and shrink as they evolve in time, follows a symmetrical, inverted parabola spanning up to hundreds of milliseconds. 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.
Significance StatementThe most common framework for understanding the temporal organization of brain activity is that of oscillations, or "brain waves". In oscillations, distinct physiological frequencies emerge at well-defined temporal scales, dividing brain activity into time segments underlying cortex function. Here, we identify a fundamentally different temporal parsing of activity in cortex. In awake Macaque monkeys, we demonstrate the motif of an inverted parabola that governs the temporal unfolding of brain activity in the form of neuronal avalanches. This symmetrical motif is scale-invariant, that is, it is not tied to time segments, and exhibits a scaling exponent close to 2 in line with prediction from theory of critical systems. We suggest that oscillations provide a Miller et al.The temporal profile of neuronal avalanches 3 transient "wrinkle" of regularity in an otherwise scale-invariant temporal organization pervading cortical activity at numerous scales.