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

The alpha rhythm is a distinctive feature of the awake resting-state of the human brain. Recent evidence suggests that alpha plays an active role in information processing, modulating behavioral and cognitive performance. However, the functional role of alpha oscillations in the resting-state neuronal dynamics remains poorly understood. To address this question, we investigate collective neural activity during resting wake and NREM sleep, a physiologic state with marginal presence of alpha rhythm. We show that, during resting wake, alpha oscillations drive an alternation of attenuation and amplification bouts in neural activity. Our analysis indicates that inhibition is activated in pulses that last a single alpha cycle and gradually suppress neural activity, while excitation is successively enhanced over timescales of a few alpha cycles to amplify neural activity. Furthermore, we show that long-term, intermittent fluctuations in alpha amplitude—known as the “waxing and waning” phenomenon—are associated with an attenuation-amplification mechanism acting over the timescales of several seconds and described by a power law decay of the activity rate in the “waning” phase. Importantly, we do not observe such dynamics during NREM sleep. The results suggest that the alpha rhythm acts as a “pacemaker” for the alternation of inhibition and excitation bouts across multiple timescales, the “waxing and waning” being a long-term control mechanism of cortical excitability. The amplification regime observed beyond the timescales of the individual alpha cycle suggests in turn that alpha oscillations might modulate the intensity of neural activity not only through pulses of inhibition, as proposed in the pulsed inhibition hypothesis, but also by timely enhancing excitation (or dis-inhibition).