Beyond pulsed inhibition: Alpha oscillations modulate attenuation and amplification of neural activity in the awake resting state
Fabrizio Lombardi,
Hans J. Herrmann,
Liborio Parrino,
Dietmar Plenz,
Silvia Scarpetta,
Anna Elisabetta Vaudano,
Lucilla de Arcangelis,
Oren Shriki
Affiliations
Fabrizio Lombardi
Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria; Department of Biomedical Sciences, University of Padova, Via Ugo Bassi 58B, 35131 Padova, Italy; Corresponding author
Hans J. Herrmann
Departamento de Fisica, Universitade Federal do Ceara, Fortaleza 60451-970, Ceara, Brazil; PMMH, ESPCI, 7 quai St. Bernard, 75005 Paris, France
Liborio Parrino
Sleep Disorders Center, Department of Neurosciences, University of Parma, 43121 Parma, Italy
Dietmar Plenz
Section on Critical Brain Dynamics, NIH, Bethesda, MD 20892, USA
Silvia Scarpetta
Department of Physics, University of Salerno, 84084 Fisciano, Italy; INFN sez, Napoli Gr. Coll, 84084 Fisciano, Italy
Anna Elisabetta Vaudano
Neurology Unit, Azienda Ospedaliero-Universitaria of Modena, OCB Hospital, 41125 Modena, Italy; Department of Biomedical, Metabolic, and Neural Sciences, University of Modena and Reggio Emilia, 41125 Modena, Italy
Lucilla de Arcangelis
Department of Mathematics and Physics, University of Campania “Luigi Vanvitelli”, Viale Lincoln 5, 81100 Caserta, Italy; Corresponding author
Oren Shriki
Department of Cognitive and Brain Sciences, Ben-Gurion University of the Negev, Beer-sheva, Israel; Corresponding author
Summary: Alpha oscillations are a distinctive feature of the awake resting state of the human brain. However, their functional role in resting-state neuronal dynamics remains poorly understood. Here we show that, during resting wakefulness, alpha oscillations drive an alternation of attenuation and amplification bouts in neural activity. Our analysis indicates that inhibition is activated in pulses that last for a single alpha cycle and gradually suppress neural activity, while excitation is successively enhanced over a few alpha cycles to amplify neural activity. Furthermore, we show that long-term alpha amplitude fluctuations—the “waxing and waning” phenomenon—are an attenuation-amplification mechanism described by a power-law decay of the activity rate in the “waning” phase. Importantly, we do not observe such dynamics during non-rapid eye movement (NREM) sleep with marginal alpha oscillations. The results suggest that alpha oscillations modulate neural activity not only through pulses of inhibition (pulsed inhibition hypothesis) but also by timely enhancement of excitation (or disinhibition).
