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

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...

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Main Authors: Fabrizio Lombardi, Hans J. Herrmann, Liborio Parrino, Dietmar Plenz, Silvia Scarpetta, Anna Elisabetta Vaudano, Lucilla de Arcangelis, Oren Shriki
Format: Article
Language:English
Published: Elsevier 2023-10-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723011749
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author Fabrizio Lombardi
Hans J. Herrmann
Liborio Parrino
Dietmar Plenz
Silvia Scarpetta
Anna Elisabetta Vaudano
Lucilla de Arcangelis
Oren Shriki
author_facet Fabrizio Lombardi
Hans J. Herrmann
Liborio Parrino
Dietmar Plenz
Silvia Scarpetta
Anna Elisabetta Vaudano
Lucilla de Arcangelis
Oren Shriki
author_sort Fabrizio Lombardi
collection DOAJ
description 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).
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spelling doaj.art-165692ea5a78457cabf083348b01923d2023-10-01T05:58:17ZengElsevierCell Reports2211-12472023-10-014210113162Beyond pulsed inhibition: Alpha oscillations modulate attenuation and amplification of neural activity in the awake resting stateFabrizio Lombardi0Hans J. Herrmann1Liborio Parrino2Dietmar Plenz3Silvia Scarpetta4Anna Elisabetta Vaudano5Lucilla de Arcangelis6Oren Shriki7Institute 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 authorDepartamento de Fisica, Universitade Federal do Ceara, Fortaleza 60451-970, Ceara, Brazil; PMMH, ESPCI, 7 quai St. Bernard, 75005 Paris, FranceSleep Disorders Center, Department of Neurosciences, University of Parma, 43121 Parma, ItalySection on Critical Brain Dynamics, NIH, Bethesda, MD 20892, USADepartment of Physics, University of Salerno, 84084 Fisciano, Italy; INFN sez, Napoli Gr. Coll, 84084 Fisciano, ItalyNeurology 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, ItalyDepartment of Mathematics and Physics, University of Campania “Luigi Vanvitelli”, Viale Lincoln 5, 81100 Caserta, Italy; Corresponding authorDepartment of Cognitive and Brain Sciences, Ben-Gurion University of the Negev, Beer-sheva, Israel; Corresponding authorSummary: 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).http://www.sciencedirect.com/science/article/pii/S2211124723011749CP: Neuroscience
spellingShingle Fabrizio Lombardi
Hans J. Herrmann
Liborio Parrino
Dietmar Plenz
Silvia Scarpetta
Anna Elisabetta Vaudano
Lucilla de Arcangelis
Oren Shriki
Beyond pulsed inhibition: Alpha oscillations modulate attenuation and amplification of neural activity in the awake resting state
Cell Reports
CP: Neuroscience
title Beyond pulsed inhibition: Alpha oscillations modulate attenuation and amplification of neural activity in the awake resting state
title_full Beyond pulsed inhibition: Alpha oscillations modulate attenuation and amplification of neural activity in the awake resting state
title_fullStr Beyond pulsed inhibition: Alpha oscillations modulate attenuation and amplification of neural activity in the awake resting state
title_full_unstemmed Beyond pulsed inhibition: Alpha oscillations modulate attenuation and amplification of neural activity in the awake resting state
title_short Beyond pulsed inhibition: Alpha oscillations modulate attenuation and amplification of neural activity in the awake resting state
title_sort beyond pulsed inhibition alpha oscillations modulate attenuation and amplification of neural activity in the awake resting state
topic CP: Neuroscience
url http://www.sciencedirect.com/science/article/pii/S2211124723011749
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