Beyond pulsed inhibition: Alpha oscillations modulate attenuation and amplification of neural activity in the awake resting-state

Abstract

Rhythmical cortical activity has long been recognized as a pillar in the architecture of brain functions. Yet, the dynamic organization of its underlying neuronal population activity remains elusive. Here we uncover a unique organizational principle regulating collective neural dynamics associated with the alpha rhythm in the awake resting-state. We demonstrate that cascades of neural activity obey attenuation-amplification dynamics (AAD), with a transition from the attenuation regime—within alpha cycles—to the amplification regime—across a few alpha cycles—that correlates with the characteristic frequency of the alpha rhythm. We find that this short-term AAD is part of a large-scale, size-dependent temporal structure of neural cascades that obeys the Omori law: Following large cascades, smaller cascades occur at a rate that decays as a power-law of the time elapsed from such events—a long-term AAD regulating brain activity over the timescale of seconds. We show that such an organization corresponds to the “waxing and waning” of the alpha rhythm. Importantly, we observe that short- and long-term AAD are unique to the awake resting-state, being absent during NREM sleep. These results provide a quantitative, dynamical description of the so-far-qualitative notion of the “waxing and waning” phenomenon, and suggest the AAD as a key principle governing resting-state dynamics across timescales.

Criticality of neuronal avalanches in human sleep and their relationship with sleep macro- and micro-architecture

“…Deviations of the EEG amplitude distributions from a Gaussian behavior indicate presence of spatiotemporal correlations that signal the occurrence of clustered, synchronized neural activity. 33 , 54 , 59 , 60 Thus, for further analysis, we identify large positive and negative signal deflections using an amplitude threshold SD ( STAR methods ; see supplementary information for robustness of avalanche statistics with respect to θ values).

Figure 1 Identification of neuronal avalanches and definition of avalanche size and duration (A) Segments (2 h) of Z score normalized EEG signal traces for an individual subject.

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“…In a recent human study, it has been shown that the dynamics of avalanches depends on the dominant, coexisting brain oscillations, and differs between awake resting-state and NREM sleep. 60 During resting wake, alpha oscillations induce attenuation of avalanches (i.e., consecutive sizes tend to be smaller) within a single alpha cycle, and corresponding amplification over several alpha cycles (i.e., consecutive sizes tend to be smaller). In contrast, during NREM sleep, only the attenuation regime has been observed, both at short and long timescales.…”

“…In contrast, during NREM sleep, only the attenuation regime has been observed, both at short and long timescales. 60 …”