Infraslow EEG activity modulates cortical excitability in postanoxic encephalopathy
Open accessAbstract
Infraslow activity represents an important component of physiological and pathological brain function. We study infraslow activity (<0.1 Hz) in 41 patients with postanoxic coma after cardiac arrest, including the relationship between infraslow activity and EEG power in the 3–30 Hz range, using continuous full-band scalp EEG. In all patients, infraslow activity (0.015–0.06 Hz) was present, irrespective of neurological outcome or EEG activity in the conventional frequency bands. In two patients, low-amplitude (10–30 μV) infraslow activity was present while the EEG showed no rhythmic activity above 0.5 Hz. In 13/15 patients with a good outcome and 20/26 patients with a poor one, EEG power in the 3–30 Hz frequency range was correlated with the phase of infraslow activity, quantified by the modulation index. In 9/14 patients with burst-suppression with identical bursts, bursts appeared in clusters, phase-locked to the infraslow oscillations. This is substantiated by a simulation of burst-suppression in a minimal computational model. Infraslow activity is preserved in postanoxic encephalopathy and modulates cortical excitability. The strongest modulation is observed in patients with severe postanoxic encephalopathy and burst-suppression with identical bursts.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The text we found for this paper looks like another document, so the self-check wasn’t run.
Cites
R: A Language and Environment for Statistical Computing
R Core Team (2000) · doi:10.32614/r.manuals · Cited by 355,706 · see citing works
A default mode of brain function
Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.2.676 · Cited by 12,190 · see citing works
Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging
Fox, M. D., & Raichle, M. E. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2201 · Cited by 6,700 · see citing works
Dynamical Systems in Neuroscience
Izhikevich, E. M. (2006) · The MIT Press eBooks · doi:10.7551/mitpress/2526.001.0001 · Cited by 3,776 · see citing works
Low-frequency neuronal oscillations as instruments of sensory selection
Schroeder, C. E., & Lakatos, P. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2008.09.012 · Cited by 1,528 · see citing works
Measuring Phase-Amplitude Coupling Between Neuronal Oscillations of Different Frequencies
Tort, A. B. L., Komorowski, R. W., Eichenbaum, H., & Kopell, N. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00106.2010 · Cited by 1,365 · see citing works
Electrophysiological correlates of the brain's intrinsic large-scale functional architecture
He, B. J., Snyder, A. Z., Zempel, J. M., Smyth, M. D., & Raichle, M. E. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807010105 · Cited by 670 · see citing works
Spontaneous astrocytic Ca2+ oscillations in situ drive NMDAR-mediated neuronal excitation
Parri, H. R., Gould, T. M., & Crunelli, V. (2001) · Nature Neuroscience · doi:10.1038/90507 · Cited by 625 · see citing works
Prognostication after cardiac arrest and hypothermia: A prospective study
Rossetti, A. O., Oddo, M., Logroscino, G., & Kaplan, P. W. (2010) · Annals of Neurology · doi:10.1002/ana.21984 · Cited by 616 · see citing works
Vanhatalo, S., Palva, J. M., Holmes, M., Miller, J. W., Voipio, J., & Kaila, K. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0305375101 · Cited by 517 · see citing works
Resting-state brain networks: literature review and clinical applications
Rosazza, C., & Minati, L. (2011) · Neurological Sciences · doi:10.1007/s10072-011-0636-y · Cited by 509 · see citing works
Monto, S., Palva, S., Voipio, J., & Palva, J. M. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1910-08.2008 · Cited by 453 · see citing works
Cortical and thalamic cellular correlates of electroencephalographic burst-suppression
Steriade, M., Amzica, F., & Contreras, D. (1994) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(94)90108-2 · Cited by 323 · see citing works
Tjepkema‐Cloostermans, M. C., van Meulen, F., Eertman, C. J., Hom, H. W., & van Putten, M. J. A. M. (2012) · Critical Care Medicine · doi:10.1097/ccm.0b013e31825b94f0 · Cited by 278 · see citing works
Self-citationHofmeijer, J., & van Putten, M. J. A. M. (2011) · Stroke · doi:10.1161/strokeaha.111.632943 · Cited by 272 · see citing works
Self-citationMurphy, T. H., Li, P., Betts, K., & Liu, R. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.5128-07.2008 · Cited by 261 · see citing works
Burst-suppression with identical bursts: A distinct EEG pattern with poor outcome in postanoxic coma
Hofmeijer, J., Tjepkema‐Cloostermans, M. C., & van Putten, M. J. A. M. (2013) · Clinical Neurophysiology · doi:10.1016/j.clinph.2013.10.017 · Cited by 233 · see citing works
Self-citationInfraslow LFP correlates to resting-state fMRI BOLD signals
Pan, W.-J., Thompson, G. J., Magnuson, M. E., Jaeger, D., & Keilholz, S. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.02.035 · Cited by 231 · see citing works
Infra-Slow EEG Fluctuations Are Correlated with Resting-State Network Dynamics in fMRI
Hiltunen, T., Kantola, J., Elseoud, A. A., Lepola, P., Suominen, K., Starck, T., Nikkinen, J., Remes, J. J., Tervonen, O. A., Palva, S., et al. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0276-13.2014 · Cited by 215 · see citing works
Tabak, J., Senn, W., O'Donovan, M. J., & Rinzel, J. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-08-03041.2000 · Cited by 199 · see citing works
Full-band EEG (FbEEG): an emerging standard in electroencephalography
Vanhatalo, S., Voipio, J., & Kaila, K. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2004.09.015 · Cited by 196 · see citing works
Infra-Slow Rhythmic Oscillations of The Steady Potential of the Cerebral Cortex
ALADJALOVA, N. A. (1957) · Nature · doi:10.1038/179957a0 · Cited by 168 · see citing works
Scalp EEG is not a Blur: It Can See High Frequency Oscillations Although Their Generators are Small
Zelmann, R., Lina, J.-M., Schulze‐Bonhage, A., Gotman, J., & Jacobs, J. (2013) · Brain Topography · doi:10.1007/s10548-013-0321-y · Cited by 163 · see citing works
Neuronal and Glial Membrane Potentials during Sleep and Paroxysmal Oscillations in the Neocortex
Amzica, F., & Steriade, M. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-17-06648.2000 · Cited by 157 · see citing works
Millivolt-Scale DC Shifts in the Human Scalp EEG: Evidence for a Nonneuronal Generator
Voipio, J., Tallgren, P., Heinonen, E., Vanhatalo, S., & Kaila, K. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00915.2002 · Cited by 148 · see citing works
Castro‐Alamancos, M. A., & Connors, B. W. (1997) · Progress in Neurobiology · doi:10.1016/s0301-0082(97)00002-6 · Cited by 114 · see citing works
Slow Electrical Processes in the Brain
(1964) · Progress in brain research · doi:10.1016/s0079-6123(08)x6123-0 · Cited by 104 · see citing works
Infraslow (<0.1Hz) oscillations in thalamic relay nuclei
Hughes, S. W., Lőrincz, M. L., Parri, H. R., & Crunelli, V. (2011) · Progress in Brain Research · doi:10.1016/b978-0-444-53839-0.00010-7 · Cited by 104 · see citing works
ATP-Dependent Infra-Slow (<0.1 Hz) Oscillations in Thalamic Networks
Lőrincz, M. L., Geall, F., Bao, Y., Crunelli, V., & Hughes, S. W. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004447 · Cited by 103 · see citing works
Tjepkema‐Cloostermans, M. C., Hofmeijer, J., Trof, R. J., Blans, M. J., Beishuizen, A., & van Putten, M. J. A. M. (2014) · Critical Care Medicine · doi:10.1097/ccm.0000000000000626 · Cited by 94 · see citing works
Self-citationPacemaker calcium oscillations in thalamic astrocytes in situ
Parri, H. R., & Crunelli, V. (2001) · Neuroreport · doi:10.1097/00001756-200112210-00008 · Cited by 93 · see citing works
Meanfield modeling of propofol-induced changes in spontaneous EEG rhythms
Hindriks, R., & van Putten, M. J. A. M. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.02.042 · Cited by 88 · see citing works
Mild hypoxia affects synaptic connectivity in cultured neuronal networks
Hofmeijer, J., Mulder, A. T. B., Farinha, A. C., van Putten, M. J. A. M., & le Feber, J. (2014) · Brain Research · doi:10.1016/j.brainres.2014.02.027 · Cited by 69 · see citing works
Self-citationPicchioni, D., Horovitz, S. G., Fukunaga, M., Carr, W. S., Meltzer, J. A., Balkin, T. J., Duyn, J. H., & Braun, A. R. (2010) · Brain Research · doi:10.1016/j.brainres.2010.12.035 · Cited by 68 · see citing works
The Mesoscopic Modeling of Burst Suppression during Anesthesia
Liley, D. T. J., & Walsh, M. (2013) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2013.00046 · Cited by 63 · see citing works
Quasi-periodic Fluctuations in Default Mode Network Electrophysiology
Ko, A. L., Darvas, F., Poliakov, A. V., Ojemann, J. G., & Sorensen, L. B. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5730-10.2011 · Cited by 62 · see citing works
Helps, S. K., James, C. J., Debener, S., Karl, A., & Sonuga-Barke, E. J. S. (2007) · Journal of Neural Transmission · doi:10.1007/s00702-007-0825-2 · Cited by 61 · see citing works
The N20 in post-anoxic coma: Are you listening?
van Putten, M. J. A. M. (2011) · Clinical Neurophysiology · doi:10.1016/j.clinph.2011.10.049 · Cited by 60 · see citing works
Electrophysiological Monitoring and Mild Hypothermia
Kochs, E. F. (1995) · Journal of Neurosurgical Anesthesiology · doi:10.1097/00008506-199507000-00022 · Cited by 52 · see citing works
EEG and visual evoked potentials of conscious man during moderate hypothermia
Fitzgibbon, T., Hayward, J. S., & Walker, D. R. (1984) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(84)90199-8 · Cited by 50 · see citing works
Slow Oscillation in Non-Lemniscal Auditory Thalamus
He, J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-23-08281.2003 · Cited by 50 · see citing works
Albrecht, D., Royl, G., & Kaneoke, Y. (1998) · Neuroscience Research · doi:10.1016/s0168-0102(98)00087-x · Cited by 46 · see citing works
An electroencephalographic comparison of effects of propofol and methohexital
Reddy, R. V., Moorthy, S. S., Mattice, T., Dierdorf, S. F., & Deitch, R. (1992) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(92)90030-l · Cited by 39 · see citing works
Whitten, T. A., Martz, L. J., Guico, A., Gervais, N., & Dickson, C. T. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00374.2009 · Cited by 36 · see citing works
Uncommon EEG burst-suppression in severe postanoxic encephalopathy
van Putten, M. J. A. M., & van Putten, M. H. P. M. (2010) · Clinical Neurophysiology · doi:10.1016/j.clinph.2010.02.162 · Cited by 33 · see citing works
Energy demands of diverse spiking cells from the neocortex, hippocampus, and thalamus
Moujahid, A., d’Anjou, A., & Graña, M. (2014) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2014.00041 · Cited by 32 · see citing works
Interictal infraslow activity in patients with epilepsy
Rodin�, E., Constantino, T., & Bigelow, J. M. (2013) · Clinical Neurophysiology · doi:10.1016/j.clinph.2013.10.014 · Cited by 28 · see citing works
Very slow oscillations of activity in geniculate neurones of urethane-anaesthetized rats
Albrecht, D., & Gabriel, S. (1994) · Neuroreport · doi:10.1097/00001756-199410000-00017 · Cited by 25 · see citing works
Wu, D., Xiong, W., Jia, X., Geocadin, R. G., & Thakor, N. V. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00681.2011 · Cited by 25 · see citing works
Extreme Stereotypy in the Burst Suppression Pattern
Hughes, J. (1986) · Clinical Electroencephalography · doi:10.1177/155005948601700406 · Cited by 19 · see citing works
EEG-Burst-Suppression-Controlled Propofol Anesthesia in the Dog
Kusters, A. H. A., Vijn, P. C. M., van den Brom, W. E., Haberham, Z. L., Haagen, A. J. V., & Hellebrekers, L. J. (1998) · Veterinary Quarterly · doi:10.1080/01652176.1998.10807448 · Cited by 17 · see citing works
Zanatta, P., TOFFOLO, G. M., Sartori, E., Bet, A., Baldanzi, F., Agarwal, N., & Golanov, E. V. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.01.033 · Cited by 14 · see citing works
Kemp, B., van Beelen, T., Stijl, M., van Someren, P. J., Roessen, M., & van Dijk, J. G. (2010) · Clinical Neurophysiology · doi:10.1016/j.clinph.2010.05.006 · Cited by 9 · see citing works
The expanding field of purinergic signalling
Burnstock, G., Abbracchio, M. P., Lewis, S., Verkhratsky, A., & Zimmermann, H. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.09.011 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Quantitative Electroencephalogram Trends Predict Recovery in Hypoxic-Ischemic Encephalopathy*
Ghassemi, M. M., Amorim, E., Alhanai, T., Lee, J. W., Herman, S. T., Sivaraju, A., Gaspard, N., Hirsch, L. J., Scirica, B. M., Biswal, S., et al. (2019) · Critical Care Medicine · doi:10.1097/ccm.0000000000003840 · Cited by 41 · see citing works
Infra-Low Frequency Neurofeedback in Depression: Three case studies
Grin-Yatsenko, V. A., Othmer, S., Ponomarev, V. A., Evdokimov, S. A., Konoplev, Y. Y., & Kropotov, J. D. (2018) · NeuroRegulation · doi:10.15540/nr.5.1.30 · Cited by 34 · see citing works
Infraslow activity as a potential modulator of corticomotor excitability
de Goede, A. A., & van Putten, M. J. A. M. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00663.2018 · Cited by 24 · see citing works
Functional ultrasound imaging: A useful tool for functional connectomics?
de Paz, J. M. M., & Macé, É. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118722 · Cited by 19 · see citing works
Effect of Infra-Low Frequency Neurofeedback on Infra-Slow EEG Fluctuations
Grin-Yatsenko, V. A., Ponomarev, V. A., Kara, O., Wandernoth, B., Gregory, M., Ilyukhina, V. A., & Kropotov, J. D. (2018) · InTech eBooks · doi:10.5772/intechopen.77154 · Cited by 13 · see citing works
Perez, T. M., Glue, P., Adhia, D. B., Navid, M. S., Zeng, J., Dillingham, P., Smith, M., Niazi, I. K., Young, C. K., & De Ridder, D. (2022) · Trials · doi:10.1186/s13063-022-06863-z · Cited by 8 · see citing works
“This IIR filter has been utilized in previous studies of eISFs [80, 241].”
MethodA methodological framework for inverse-modeling of propagating cortical activity using MEG/EEG
Hindriks, R. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117345 · Cited by 10 · see citing works
DC-EEG recordings of mindfulness
Rodin, E. A., Bornfleth, H., & Johnson, M. (2017) · Clinical Neurophysiology · doi:10.1016/j.clinph.2016.12.031 · Cited by 7 · see citing works
Resolving and characterizing the incidence of millihertz EEG modulation in critically ill children
Loe, M. E., Khanmohammadi, S., Morrissey, M., Landre, R., Tomko, S. R., Guerriero, R. M., & Ching, S. (2022) · Clinical Neurophysiology · doi:10.1016/j.clinph.2022.02.010 · Cited by 6 · see citing works
Jafarian, A., & Wykes, R. C. (2022) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2022.900063 · Cited by 4 · see citing works
Grin-Yatsenko, V. A., Ponomarev, V. A., & Kropotov, J. D. (2023) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s002209302303016x · Cited by 3 · see citing works
Togo, M., Hitomi, T., Murai, T., Yoshimura, H., Matsuhashi, M., Matsumoto, R., Kawamoto, M., Kohara, N., Takahashi, R., & Ikeda, A. (2018) · Journal of Clinical Neurophysiology · doi:10.1097/wnp.0000000000000507 · Cited by 4 · see citing works
Vanhatalo, S., & Palva, J. M. (2017) · doi:10.1093/med/9780190228484.003.0032 · Cited by 3 · see citing works
Perez, T. M., Glue, P., Adhia, D. B., Smith, M. J., Ridder, D. D., Zeng, J., Dillingham, P. W., & Niazi, I. K. (2021) · Research Square · doi:10.21203/rs.3.rs-173667/v1 · Cited by 3 · see citing works
Zavaleta-Viveros, J. A., Toledo, P., Avendaño‐Garrido, M. L., & Escalante-Martínez, J. E. (2020) · Lecture notes in computer science · doi:10.1007/978-3-030-60887-3_28 · Cited by 2 · see citing works
Arrufat‐Pié, E., Estévez‐Báez, M., Estévez‐Carreras, J. M., Curbelo, C. M., Leisman, G., & Leon, C. A. B. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.06.138065 · Cited by 2 · see citing works
Arrufat‐Pié, E., Estévez‐Báez, M., Estévez‐Carreras, J. M., Leisman, G., Machado, C., & Leon, C. A. B. (2023) · Signals · doi:10.3390/signals4030026 · Cited by 1 · see citing works
Perez, T. M., Adhia, D. B., Glue, P., Zeng, J., Dillingham, P. W., Navid, M. S., Niazi, I. K., Young, C. K., Smith, M. L., & Ridder, D. J. M. K. D. (2025) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-025-01279-z · Cited by 1 · see citing works
P 57. Effect of Infra-Low Frequency Neurofeedback on Infra-Slow EEG Fluctuations
Grin-Yatsenko, V. A., Ponomarev, V. A., Kara, O., Wandernoth, B., Gregory, M., Ilyukhina, V. A., Kropotov, J. D., & Schneider, H. (2021) · Clinical Neurophysiology · doi:10.1016/j.clinph.2021.02.373 · Cited by 1 · see citing works
Hepatic encephalopathy revisited: Beyond the triphasic waves
Togo, M., & Kinoshita, M. (2018) · Clinical Neurophysiology · doi:10.1016/j.clinph.2018.12.003 · Cited by 1 · see citing works
Testing brains with burst suppressions
Vanhatalo, S. (2016) · Clinical Neurophysiology · doi:10.1016/j.clinph.2016.04.018
de Goede, A. A. (2019) · doi:10.3990/1.9789036547345
Kortikale Aktivität, EEG und Signalverarbeitung
Sidiropoulos, K., Kilian, B., & Ströhle, G. (2023) · Springer eBooks · doi:10.1007/978-3-662-65726-3_12
Grin-Yatsenko, V. A., Ponomarev, V. A., & Kropotov, J. D. (2023) · Российский физиологический журнал им И М Сеченова · doi:10.31857/s0869813923050047
Hayashi, K., Usami, K., Togo, M., Yamao, Y., Funaki, T., Hitomi, T., Kikuchi, T., Matsuhashi, M., Yoshida, K., Arakawa, Y., et al. (2025) · Clinical Neurophysiology · doi:10.1016/j.clinph.2025.2110748
Jafarian, A., & Wykes, R. C. (2026) · PLoS ONE · doi:10.1371/journal.pone.0353399
Sitti, G., Pitti, L., & Candia‐Rivera, D. (2026) · The Journal of Physiology · doi:10.1113/jp291568
- Authors
- van Putten, M. J. A. M., Tjepkema-Cloostermans, M. C., & Hofmeijer, J.
- Affiliations
- Department of Neurology and Clinical Neurophysiology, Medisch Spectrum Twente, Enschede, the Netherlands;
- Rijnstate Hospital (NL)
- ORCID
- Hofmeijer, Jeannette
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 2015-05
- Volume
- 113
- Issue
- 9
- Pages
- 3256-3267
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- PMC
- PMC4440240
- OpenAlex
- W2095024261
- Cited by
- 27
- References
- 54
- Citations by year
- 2026: 2 · 2025: 2 · 2023: 4 · 2022: 3 · 2021: 3 · 2020: 3 · 2019: 3 · 2018: 4 · 2017: 2 · 2016: 1
- FWCI
- 1.40
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- University of Twente Research Information (publishedVersion, other-oa)
- University of Twente Research Information (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Health Sciences › Medicine › Epidemiology › Traumatic Brain Injury Research
- Keywords
- postanoxic encephalopathy, postanoxic coma, cardiac arrest, cortical excitability, burst suppression, EEG spectral power, modulation index, phase locking, neurological outcome
- MeSH terms
- Alkaloids, Brain Diseases, Cerebral Cortex, Electroencephalography, Female, Heart Arrest, Humans, Intensive Care Units, Male, Brain Waves
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review