---
_id: '14402'
abstract:
- lang: eng
text: 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).
acknowledgement: This research was funded in whole or in part by the Austrian Science
Fund (FWF) (grant PT1013M03318 to F.L.). For the purpose of open access, the author
has applied a CC BY public copyright license to any Author Accepted Manuscript version
arising from this submission. The study was supported by the European Union Horizon
2020 Research and Innovation Program under the Marie Sklodowska-Curie action (grant
agreement 754411 to F.L.) and in part by the NextGenerationEU through the grant
TAlent in ReSearch@University of Padua – STARS@UNIPD (to F.L.) (project BRAINCIP
[brain criticality and information processing]). L.d.A. acknowledges support from
the Italian MIUR project PRIN2017WZFTZP and partial support from NEXTGENERATIONEU
(NGEU) funded by the Ministry of University and Research (MUR), National Recovery
and Resilience Plan (NRRP), and project MNESYS (PE0000006)—a multiscale integrated
approach to the study of the nervous system in health and disease (DN. 1553 11.10.2022).
O.S. acknowledges support from the Israel Science Foundation, grant 504/17. The
work was supported in part by DIRP ZIAMH02797 (to D.P.).
article_number: '113162'
article_processing_charge: Yes
article_type: original
author:
- first_name: Fabrizio
full_name: Lombardi, Fabrizio
id: A057D288-3E88-11E9-986D-0CF4E5697425
last_name: Lombardi
orcid: 0000-0003-2623-5249
- first_name: Hans J.
full_name: Herrmann, Hans J.
last_name: Herrmann
- first_name: Liborio
full_name: Parrino, Liborio
last_name: Parrino
- first_name: Dietmar
full_name: Plenz, Dietmar
last_name: Plenz
- first_name: Silvia
full_name: Scarpetta, Silvia
last_name: Scarpetta
- first_name: Anna Elisabetta
full_name: Vaudano, Anna Elisabetta
last_name: Vaudano
- first_name: Lucilla
full_name: De Arcangelis, Lucilla
last_name: De Arcangelis
- first_name: Oren
full_name: Shriki, Oren
last_name: Shriki
citation:
ama: 'Lombardi F, Herrmann HJ, Parrino L, et al. Beyond pulsed inhibition: Alpha
oscillations modulate attenuation and amplification of neural activity in the
awake resting state. Cell Reports. 2023;42(10). doi:10.1016/j.celrep.2023.113162'
apa: 'Lombardi, F., Herrmann, H. J., Parrino, L., Plenz, D., Scarpetta, S., Vaudano,
A. E., … Shriki, O. (2023). Beyond pulsed inhibition: Alpha oscillations modulate
attenuation and amplification of neural activity in the awake resting state. Cell
Reports. Elsevier. https://doi.org/10.1016/j.celrep.2023.113162'
chicago: 'Lombardi, Fabrizio, Hans J. Herrmann, Liborio Parrino, Dietmar Plenz,
Silvia Scarpetta, Anna Elisabetta Vaudano, Lucilla De Arcangelis, and Oren Shriki.
“Beyond Pulsed Inhibition: Alpha Oscillations Modulate Attenuation and Amplification
of Neural Activity in the Awake Resting State.” Cell Reports. Elsevier,
2023. https://doi.org/10.1016/j.celrep.2023.113162.'
ieee: 'F. Lombardi et al., “Beyond pulsed inhibition: Alpha oscillations
modulate attenuation and amplification of neural activity in the awake resting
state,” Cell Reports, vol. 42, no. 10. Elsevier, 2023.'
ista: 'Lombardi F, Herrmann HJ, Parrino L, Plenz D, Scarpetta S, Vaudano AE, De
Arcangelis L, Shriki O. 2023. Beyond pulsed inhibition: Alpha oscillations modulate
attenuation and amplification of neural activity in the awake resting state. Cell
Reports. 42(10), 113162.'
mla: 'Lombardi, Fabrizio, et al. “Beyond Pulsed Inhibition: Alpha Oscillations Modulate
Attenuation and Amplification of Neural Activity in the Awake Resting State.”
Cell Reports, vol. 42, no. 10, 113162, Elsevier, 2023, doi:10.1016/j.celrep.2023.113162.'
short: F. Lombardi, H.J. Herrmann, L. Parrino, D. Plenz, S. Scarpetta, A.E. Vaudano,
L. De Arcangelis, O. Shriki, Cell Reports 42 (2023).
date_created: 2023-10-08T22:01:15Z
date_published: 2023-10-31T00:00:00Z
date_updated: 2024-01-30T14:07:40Z
day: '31'
ddc:
- '570'
department:
- _id: GaTk
doi: 10.1016/j.celrep.2023.113162
ec_funded: 1
external_id:
isi:
- '001086695500001'
pmid:
- '37777965'
file:
- access_level: open_access
checksum: 9c71eb2a03aa160415f01ad95f49ceb5
content_type: application/pdf
creator: dernst
date_created: 2024-01-30T14:07:08Z
date_updated: 2024-01-30T14:07:08Z
file_id: '14914'
file_name: 2023_CellReports_Lombardi.pdf
file_size: 5599007
relation: main_file
success: 1
file_date_updated: 2024-01-30T14:07:08Z
has_accepted_license: '1'
intvolume: ' 42'
isi: 1
issue: '10'
language:
- iso: eng
month: '10'
oa: 1
oa_version: Published Version
pmid: 1
project:
- _id: eb943429-77a9-11ec-83b8-9f471cdf5c67
grant_number: M03318
name: Functional Advantages of Critical Brain Dynamics
- _id: 260C2330-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '754411'
name: ISTplus - Postdoctoral Fellowships
publication: Cell Reports
publication_identifier:
eissn:
- 2211-1247
publication_status: published
publisher: Elsevier
quality_controlled: '1'
scopus_import: '1'
status: public
title: 'Beyond pulsed inhibition: Alpha oscillations modulate attenuation and amplification
of neural activity in the awake resting state'
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 42
year: '2023'
...
---
_id: '12487'
abstract:
- lang: eng
text: Sleep plays a key role in preserving brain function, keeping the brain network
in a state that ensures optimal computational capabilities. Empirical evidence
indicates that such a state is consistent with criticality, where scale-free neuronal
avalanches emerge. However, the relationship between sleep, emergent avalanches,
and criticality remains poorly understood. Here we fully characterize the critical
behavior of avalanches during sleep, and study their relationship with the sleep
macro- and micro-architecture, in particular the cyclic alternating pattern (CAP).
We show that avalanche size and duration distributions exhibit robust power laws
with exponents approximately equal to −3/2 e −2, respectively. Importantly, we
find that sizes scale as a power law of the durations, and that all critical exponents
for neuronal avalanches obey robust scaling relations, which are consistent with
the mean-field directed percolation universality class. Our analysis demonstrates
that avalanche dynamics depends on the position within the NREM-REM cycles, with
the avalanche density increasing in the descending phases and decreasing in the
ascending phases of sleep cycles. Moreover, we show that, within NREM sleep, avalanche
occurrence correlates with CAP activation phases, particularly A1, which are the
expression of slow wave sleep propensity and have been proposed to be beneficial
for cognitive processes. The results suggest that neuronal avalanches, and thus
tuning to criticality, actively contribute to sleep development and play a role
in preserving network function. Such findings, alongside characterization of the
universality class for avalanches, open new avenues to the investigation of functional
role of criticality during sleep with potential clinical application.Significance
statementWe fully characterize the critical behavior of neuronal
avalanches during sleep, and show that avalanches follow precise scaling laws
that are consistent with the mean-field directed percolation universality class.
The analysis provides first evidence of a functional relationship between avalanche
occurrence, slow-wave sleep dynamics, sleep stage transitions and occurrence of
CAP phase A during NREM sleep. Because CAP is considered one of the major guardians
of NREM sleep that allows the brain to dynamically react to external perturbation
and contributes to the cognitive consolidation processes occurring in sleep, our
observations suggest that neuronal avalanches at criticality are associated with
flexible response to external inputs and to cognitive processes, a key assumption
of the critical brain hypothesis.
acknowledgement: FL acknowledges support from the European Union’s Horizon 2020 research
and innovation program under the Marie Sklodowska-Curie Grant Agreement No. 754411,
and from the Austrian Science Fund (FWF) under the Lise Meitner fellowship No. PT1013M03318.
IA acknowledges financial support from the MIUR PRIN 2017WZFTZP.
article_processing_charge: Yes
article_type: original
author:
- first_name: Silvia
full_name: Scarpetta, Silvia
last_name: Scarpetta
- first_name: Niccolò
full_name: Morrisi, Niccolò
last_name: Morrisi
- first_name: Carlotta
full_name: Mutti, Carlotta
last_name: Mutti
- first_name: Nicoletta
full_name: Azzi, Nicoletta
last_name: Azzi
- first_name: Irene
full_name: Trippi, Irene
last_name: Trippi
- first_name: Rosario
full_name: Ciliento, Rosario
last_name: Ciliento
- first_name: Ilenia
full_name: Apicella, Ilenia
last_name: Apicella
- first_name: Giovanni
full_name: Messuti, Giovanni
last_name: Messuti
- first_name: Marianna
full_name: Angiolelli, Marianna
last_name: Angiolelli
- first_name: Fabrizio
full_name: Lombardi, Fabrizio
id: A057D288-3E88-11E9-986D-0CF4E5697425
last_name: Lombardi
orcid: 0000-0003-2623-5249
- first_name: Liborio
full_name: Parrino, Liborio
last_name: Parrino
- first_name: Anna Elisabetta
full_name: Vaudano, Anna Elisabetta
last_name: Vaudano
citation:
ama: Scarpetta S, Morrisi N, Mutti C, et al. Criticality of neuronal avalanches
in human sleep and their relationship with sleep macro- and micro-architecture.
iScience. 2023;26(10):107840. doi:10.1016/j.isci.2023.107840
apa: Scarpetta, S., Morrisi, N., Mutti, C., Azzi, N., Trippi, I., Ciliento, R.,
… Vaudano, A. E. (2023). Criticality of neuronal avalanches in human sleep and
their relationship with sleep macro- and micro-architecture. IScience.
Elsevier. https://doi.org/10.1016/j.isci.2023.107840
chicago: Scarpetta, Silvia, Niccolò Morrisi, Carlotta Mutti, Nicoletta Azzi, Irene
Trippi, Rosario Ciliento, Ilenia Apicella, et al. “Criticality of Neuronal Avalanches
in Human Sleep and Their Relationship with Sleep Macro- and Micro-Architecture.”
IScience. Elsevier, 2023. https://doi.org/10.1016/j.isci.2023.107840.
ieee: S. Scarpetta et al., “Criticality of neuronal avalanches in human sleep
and their relationship with sleep macro- and micro-architecture,” iScience,
vol. 26, no. 10. Elsevier, p. 107840, 2023.
ista: Scarpetta S, Morrisi N, Mutti C, Azzi N, Trippi I, Ciliento R, Apicella I,
Messuti G, Angiolelli M, Lombardi F, Parrino L, Vaudano AE. 2023. Criticality
of neuronal avalanches in human sleep and their relationship with sleep macro-
and micro-architecture. iScience. 26(10), 107840.
mla: Scarpetta, Silvia, et al. “Criticality of Neuronal Avalanches in Human Sleep
and Their Relationship with Sleep Macro- and Micro-Architecture.” IScience,
vol. 26, no. 10, Elsevier, 2023, p. 107840, doi:10.1016/j.isci.2023.107840.
short: S. Scarpetta, N. Morrisi, C. Mutti, N. Azzi, I. Trippi, R. Ciliento, I. Apicella,
G. Messuti, M. Angiolelli, F. Lombardi, L. Parrino, A.E. Vaudano, IScience 26
(2023) 107840.
date_created: 2023-02-02T10:50:17Z
date_published: 2023-10-20T00:00:00Z
date_updated: 2023-12-13T11:11:24Z
day: '20'
ddc:
- '570'
department:
- _id: GaTk
doi: 10.1016/j.isci.2023.107840
ec_funded: 1
external_id:
isi:
- '001082331200001'
pmid:
- '37766992'
file:
- access_level: open_access
checksum: f499836af172ecc9865de4bb41fa99d1
content_type: application/pdf
creator: dernst
date_created: 2023-10-09T07:23:46Z
date_updated: 2023-10-09T07:23:46Z
file_id: '14412'
file_name: 2023_iScience_Scarpetta.pdf
file_size: 4872708
relation: main_file
success: 1
file_date_updated: 2023-10-09T07:23:46Z
has_accepted_license: '1'
intvolume: ' 26'
isi: 1
issue: '10'
language:
- iso: eng
month: '10'
oa: 1
oa_version: Published Version
page: '107840'
pmid: 1
project:
- _id: 260C2330-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '754411'
name: ISTplus - Postdoctoral Fellowships
- _id: eb943429-77a9-11ec-83b8-9f471cdf5c67
grant_number: M03318
name: Functional Advantages of Critical Brain Dynamics
publication: iScience
publication_identifier:
eissn:
- 2589-0042
publication_status: published
publisher: Elsevier
quality_controlled: '1'
scopus_import: '1'
status: public
title: Criticality of neuronal avalanches in human sleep and their relationship with
sleep macro- and micro-architecture
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 26
year: '2023'
...
---
_id: '12762'
abstract:
- lang: eng
text: Neurons in the brain are wired into adaptive networks that exhibit collective
dynamics as diverse as scale-specific oscillations and scale-free neuronal avalanches.
Although existing models account for oscillations and avalanches separately, they
typically do not explain both phenomena, are too complex to analyze analytically
or intractable to infer from data rigorously. Here we propose a feedback-driven
Ising-like class of neural networks that captures avalanches and oscillations
simultaneously and quantitatively. In the simplest yet fully microscopic model
version, we can analytically compute the phase diagram and make direct contact
with human brain resting-state activity recordings via tractable inference of
the model’s two essential parameters. The inferred model quantitatively captures
the dynamics over a broad range of scales, from single sensor oscillations to
collective behaviors of extreme events and neuronal avalanches. Importantly, the
inferred parameters indicate that the co-existence of scale-specific (oscillations)
and scale-free (avalanches) dynamics occurs close to a non-equilibrium critical
point at the onset of self-sustained oscillations.
acknowledgement: This research was funded in whole, or in part, by the Austrian Science
Fund (FWF) (grant no. PT1013M03318 to F.L. and no. P34015 to G.T.). For the purpose
of open access, the author has applied a CC BY public copyright licence to any Author
Accepted Manuscript version arising from this submission. The study was supported
by the European Union Horizon 2020 research and innovation program under the Marie
Sklodowska-Curie action (grant agreement No. 754411 to F.L.).
article_processing_charge: No
article_type: original
arxiv: 1
author:
- first_name: Fabrizio
full_name: Lombardi, Fabrizio
id: A057D288-3E88-11E9-986D-0CF4E5697425
last_name: Lombardi
orcid: 0000-0003-2623-5249
- first_name: Selver
full_name: Pepic, Selver
id: F93245C4-C3CA-11E9-B4F0-C6F4E5697425
last_name: Pepic
- first_name: Oren
full_name: Shriki, Oren
last_name: Shriki
- first_name: Gašper
full_name: Tkačik, Gašper
id: 3D494DCA-F248-11E8-B48F-1D18A9856A87
last_name: Tkačik
orcid: 0000-0002-6699-1455
- first_name: Daniele
full_name: De Martino, Daniele
id: 3FF5848A-F248-11E8-B48F-1D18A9856A87
last_name: De Martino
orcid: 0000-0002-5214-4706
citation:
ama: Lombardi F, Pepic S, Shriki O, Tkačik G, De Martino D. Statistical modeling
of adaptive neural networks explains co-existence of avalanches and oscillations
in resting human brain. Nature Computational Science. 2023;3:254-263. doi:10.1038/s43588-023-00410-9
apa: Lombardi, F., Pepic, S., Shriki, O., Tkačik, G., & De Martino, D. (2023).
Statistical modeling of adaptive neural networks explains co-existence of avalanches
and oscillations in resting human brain. Nature Computational Science.
Springer Nature. https://doi.org/10.1038/s43588-023-00410-9
chicago: Lombardi, Fabrizio, Selver Pepic, Oren Shriki, Gašper Tkačik, and Daniele
De Martino. “Statistical Modeling of Adaptive Neural Networks Explains Co-Existence
of Avalanches and Oscillations in Resting Human Brain.” Nature Computational
Science. Springer Nature, 2023. https://doi.org/10.1038/s43588-023-00410-9.
ieee: F. Lombardi, S. Pepic, O. Shriki, G. Tkačik, and D. De Martino, “Statistical
modeling of adaptive neural networks explains co-existence of avalanches and oscillations
in resting human brain,” Nature Computational Science, vol. 3. Springer
Nature, pp. 254–263, 2023.
ista: Lombardi F, Pepic S, Shriki O, Tkačik G, De Martino D. 2023. Statistical modeling
of adaptive neural networks explains co-existence of avalanches and oscillations
in resting human brain. Nature Computational Science. 3, 254–263.
mla: Lombardi, Fabrizio, et al. “Statistical Modeling of Adaptive Neural Networks
Explains Co-Existence of Avalanches and Oscillations in Resting Human Brain.”
Nature Computational Science, vol. 3, Springer Nature, 2023, pp. 254–63,
doi:10.1038/s43588-023-00410-9.
short: F. Lombardi, S. Pepic, O. Shriki, G. Tkačik, D. De Martino, Nature Computational
Science 3 (2023) 254–263.
date_created: 2023-03-26T22:01:08Z
date_published: 2023-03-20T00:00:00Z
date_updated: 2023-08-16T12:41:53Z
day: '20'
ddc:
- '570'
department:
- _id: GaTk
- _id: GradSch
doi: 10.1038/s43588-023-00410-9
ec_funded: 1
external_id:
arxiv:
- '2108.06686'
file:
- access_level: open_access
checksum: 7c63b2b2edfd68aaffe96d70ca6a865a
content_type: application/pdf
creator: dernst
date_created: 2023-08-16T12:39:57Z
date_updated: 2023-08-16T12:39:57Z
file_id: '14073'
file_name: 2023_NatureCompScience_Lombardi.pdf
file_size: 4474284
relation: main_file
success: 1
file_date_updated: 2023-08-16T12:39:57Z
has_accepted_license: '1'
intvolume: ' 3'
language:
- iso: eng
month: '03'
oa: 1
oa_version: Published Version
page: 254-263
project:
- _id: 260C2330-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '754411'
name: ISTplus - Postdoctoral Fellowships
- _id: eb943429-77a9-11ec-83b8-9f471cdf5c67
grant_number: M03318
name: Functional Advantages of Critical Brain Dynamics
- _id: 626c45b5-2b32-11ec-9570-e509828c1ba6
grant_number: P34015
name: Efficient coding with biophysical realism
publication: Nature Computational Science
publication_identifier:
eissn:
- 2662-8457
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
scopus_import: '1'
status: public
title: Statistical modeling of adaptive neural networks explains co-existence of avalanches
and oscillations in resting human brain
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 3
year: '2023'
...