Brain-scale cortico-cortical functional connectivity in the delta-theta band is a robust signature of conscious states: an intracranial and scalp EEG study.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
20 08 2020
Historique:
received: 05 02 2020
accepted: 22 07 2020
entrez: 22 8 2020
pubmed: 21 8 2020
medline: 24 4 2021
Statut: epublish

Résumé

Long-range cortico-cortical functional connectivity has long been theorized to be necessary for conscious states. In the present work, we estimate long-range cortical connectivity in a series of intracranial and scalp EEG recordings experiments. In the two first experiments intracranial-EEG (iEEG) was recorded during four distinct states within the same individuals: conscious wakefulness (CW), rapid-eye-movement sleep (REM), stable periods of slow-wave sleep (SWS) and deep propofol anaesthesia (PA). We estimated functional connectivity using the following two methods: weighted Symbolic-Mutual-Information (wSMI) and phase-locked value (PLV). Our results showed that long-range functional connectivity in the delta-theta frequency band specifically discriminated CW and REM from SWS and PA. In the third experiment, we generalized this original finding on a large cohort of brain-injured patients. FC in the delta-theta band was significantly higher in patients being in a minimally conscious state (MCS) than in those being in a vegetative state (or unresponsive wakefulness syndrome). Taken together the present results suggest that FC of cortical activity in this slow frequency band is a new and robust signature of conscious states.

Identifiants

pubmed: 32820188
doi: 10.1038/s41598-020-70447-7
pii: 10.1038/s41598-020-70447-7
pmc: PMC7441406
doi:

Substances chimiques

Hypnotics and Sedatives 0
Propofol YI7VU623SF

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

14037

Références

Dehaene, S. & Changeux, J.-P. Experimental and theoretical approaches to conscious processing. Neuron 70, 200–227 (2011).
pubmed: 21521609
Dehaene, S. & Naccache, L. Towards a cognitive neuroscience of consciousness: Basic evidence and a workspace framework. Cognition 79, 1–37 (2001).
pubmed: 11164022
Boly, M. et al. Consciousness in humans and non-human animals: recent advances and future directions. Front. Psychol. 4, 625 (2013).
pubmed: 24198791 pmcid: 3814086
Amico, E. et al. Mapping the functional connectome traits of levels of consciousness. Neuroimage 148, 201–211 (2017).
pubmed: 28093358
Crone, J. S. et al. Altered network properties of the fronto-parietal network and the thalamus in impaired consciousness. NeuroImage. Clin. 4, 240–248 (2014).
pubmed: 24455474
Laureys, S. & Schiff, N. D. Coma and consciousness: paradigms (re)framed by neuroimaging. Neuroimage 61, 478–491 (2012).
pubmed: 22227888
Lamme, V. A. F. Towards a true neural stance on consciousness. Trends Cogn. Sci. 10, 494–501 (2006).
pubmed: 16997611
Barttfeld, P. et al. Signature of consciousness in the dynamics of resting-state brain activity. Proc. Natl. Acad. Sci. USA 112, 887–892 (2015).
pubmed: 25561541
He, B. J. & Raichle, M. E. The fMRI signal, slow cortical potential and consciousness. Trends Cogn. Sci. 13, 302–309 (2009).
pubmed: 19535283 pmcid: 2855786
He, B. J., Snyder, A. Z., Zempel, J. M., Smyth, M. D. & Raichle, M. E. Electrophysiological correlates of the brain’s intrinsic large-scale functional architecture. Proc. Natl. Acad. Sci. USA 105, 16039–16044 (2008).
pubmed: 18843113
Schiff, N. D., Nauvel, T. & Victor, J. D. Large-scale brain dynamics in disorders of consciousness. Curr. Opin. Neurobiol. 25, 7–14 (2014).
pubmed: 24709594
Naccache, L. & Dehaene, S. Unconscious semantic priming extends to novel unseen stimuli. Cognition 80, 215–229 (2001).
pubmed: 11274983
Leclair-Visonneau, L., Oudiette, D., Gaymard, B., Leu-Semenescu, S. & Arnulf, I. Do the eyes scan dream images during rapid eye movement sleep? Evidence from the rapid eye movement sleep behaviour disorder model. Brain 133, 1737–1746 (2010).
pubmed: 20478849
Siclari, F. et al. The neural correlates of dreaming. Nat. Neurosci. 20, 872–878 (2017).
pubmed: 28394322 pmcid: 5462120
Jouvet, M. Neurophysiology of the states of sleep. Physiol. Rev. 47, 117–177 (1967).
pubmed: 5342870
Jouvet, M., Michel, F. & Courjon, J. Sur un stade d’activité électrique cérébrale rapide au cours du sommeil physiologique. C. R. Seances Soc. Biol. Fil. 153, 1024–1028 (1959).
pubmed: 14408003
Massimini, M. et al. Neuroscience: Breakdown of cortical effective connectivity during sleep. Science 309, 2228–2232 (2005).
pubmed: 16195466
Ferrarelli, F. et al. Breakdown in cortical effective connectivity during midazolam-induced loss of consciousness. Proc. Natl. Acad. Sci. USA 107, 2681–2686 (2010).
pubmed: 20133802
Casali, A. G. et al. A theoretically based index of consciousness independent of sensory processing and behavior. Sci. Transl. Med. 5, 198 (2013).
King, J.-R. et al. Information sharing in the brain indexes consciousness in noncommunicative patients. Curr. Biol. 23, 1914–1919 (2013).
pubmed: 24076243 pmcid: 5635964
Sitt, J. D. et al. Large scale screening of neural signatures of consciousness in patients in a vegetative or minimally conscious state. Brain 137, 2258–2270 (2014).
pubmed: 24919971 pmcid: 4610185
Chennu, S. & Menon, D. Brain networks predict metabolism, diagnosis and prognosis at the bedside in disorders of consciousness. Brain https://doi.org/10.17863/CAM.10200 (2017).
doi: 10.17863/CAM.10200 pubmed: 28666351
Chennu, S. et al. Spectral signatures of reorganised brain networks in disorders of consciousness. PLoS Comput. Biol. 10, e1003887 (2014).
pubmed: 25329398 pmcid: 4199497
Chennu, S., O’Connor, S., Adapa, R., Menon, D. K. & Bekinschtein, T. A. Brain connectivity dissociates responsiveness from drug exposure during propofol-induced transitions of consciousness. PLoS Comput. Biol. 12, e1004669 (2016).
pubmed: 26764466 pmcid: 4713143
Shin, D.-J. et al. The effects of pharmacological treatment on functional brain connectome in obsessive-compulsive disorder. Biol. Psychiatry 75, 606–614 (2014).
pubmed: 24099506
Robinson, S. E. & Mandell, A. J. Mutual Information in a MEG complexity measure suggests regional hyper-connectivity in schizophrenic probands. Neuropsychopharmacology 40, 251–252 (2015).
pubmed: 25482179
Ortiz, E. et al. Weighted phase lag index and graph analysis: Preliminary investigation of functional connectivity during resting state in children. Comput. Math. Methods Med. 2012, (2012).
Minji Lee et al. Change in functional networks for transitions between states of consciousness during midazolam-induced sedation. Conf. Proc. Annu. Int. Conf. IEEE Eng. Med. Biol. Soc. IEEE Eng. Med. Biol. Soc. Annu. Conf. 2017, 958–961 (2017).
Srinivasan, R., Winter, W. R., Ding, J. & Nunez, P. L. EEG and MEG coherence: Measures of functional connectivity at distinct spatial scales of neocortical dynamics. J. Neurosci. Methods 166, 41–52 (2007).
pubmed: 17698205 pmcid: 2151962
Khadem, A. & Hossein-Zadeh, G. A. Quantification of the effects of volume conduction on the EEG/MEG connectivity estimates: An index of sensitivity to brain interactions. Physiol. Meas. 35, 2149–2164 (2014).
pubmed: 25243864
Imperatori, L. S. et al. EEG functional connectivity metrics wPLI and wSMI account for distinct types of brain functional interactions. Sci. Rep. 9, 8894 (2019).
pubmed: 31222021 pmcid: 6586889
Corazzol, M. et al. Restoring consciousness with vagus nerve stimulation. Curr. Biol. 27, 1 (2017).
Lachaux, J. P., Rodriguez, E., Martinerie, J. & Varela, F. J. Measuring phase synchrony in brain signals. Hum. Brain Mapp. 8, 194–208 (1999).
pubmed: 10619414 pmcid: 6873296
Hermann, B. et al. Combined behavioral and electrophysiological evidence for a direct cortical effect of prefrontal tDCS on disorders of consciousness. Sci. Rep. 10, 4323 (2020).
pubmed: 32152347 pmcid: 7062738
Naccache, L. Minimally conscious state or cortically mediated state?. Brain 141, 949–960 (2018).
pubmed: 29206895
Engemann, D. A. et al. Robust EEG-based cross-site and cross-protocol classification of states of consciousness. Brain 141, 3179–3192 (2018).
pubmed: 30285102 pmcid: 30285102
Bola, M. et al. Loss of consciousness is related to hyper-correlated gamma-band activity in anesthetized macaques and sleeping humans. Neuroimage 167, 130–142 (2017).
pubmed: 29162522
Attarian, H. P. & Undevia, N. S. Normal Sleep Stages. In Atlas of Electroencephalography in Sleep Medicine 1–24 (Springer, US, Berlin, 2012). https://doi.org/10.1007/978-1-4614-2293-8_1 .
doi: 10.1007/978-1-4614-2293-8_1
Sanei, S., Chambers, J. A., Sanei, S. & Chambers, J. A. Sleep EEG. In EEG Signal Processing 219–237 (John Wiley & Sons Ltd, New York, 2013). https://doi.org/10.1002/9780470511923.ch6 .
doi: 10.1002/9780470511923.ch6
Lewis, L. D. et al. Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness. Proc. Natl. Acad. Sci. USA. 109, E3377–E3386 (2012).
pubmed: 23129622
Frauscher, B. et al. Atlas of the normal intracranial electroencephalogram: neurophysiological awake activity in different cortical areas. Brain 141, 1130–1144 (2018).
pubmed: 29506200
von Ellenrieder, N. et al. How the human brain sleeps: Direct cortical recordings of normal brain activity. Ann. Neurol. 87, 289–301 (2020).
Li, Q., Hill, Z. & He, B. J. Spatiotemporal dissociation of brain activity underlying subjective awareness, objective performance and confidence. J. Neurosci. 34, 4382–4395 (2014).
pubmed: 24647958 pmcid: 3960476
Baria, A. T., Maniscalco, B. & He, B. J. Initial-state-dependent, robust, transient neural dynamics encode conscious visual perception. PLoS Comput. Biol. 13, e1005806 (2017).
pubmed: 29176808 pmcid: 5720802
Flounders, M. W., González-García, C., Hardstone, R. & He, B. J. Neural dynamics of visual ambiguity resolution by perceptual prior. Elife 8, 2 (2019).
Mitra, A. et al. Spontaneous infra-slow brain activity has unique spatiotemporal dynamics and laminar structure. Neuron 98, 297-305.e6 (2018).
pubmed: 29606579 pmcid: 5910292
Naccache, L. Why and how access consciousness can account for phenomenal consciousness. Philos. Trans. R. Soc. B Biol. Sci. 373, 1 (2018).
Gaillard, R. et al. Converging intracranial markers of conscious access. PLoS Biol. 7, e61 (2009).
pubmed: 19296722
Bekinschtein, T. A. et al. Neural signature of the conscious processing of auditory regularities. Proc. Natl. Acad. Sci. 106, 1672–1677 (2009).
pubmed: 19164526
Galanaud, D. et al. Assessment of white matter injury and outcome in severe brain trauma: A prospective multicenter cohort. Anesthesiology 117, 1300–1310 (2012).
pubmed: 23135261
Velly, L. et al. Use of brain diffusion tensor imaging for the prediction of long-term neurological outcomes in patients after cardiac arrest: A multicentre, international, prospective, observational, cohort study. Lancet. Neurol. 17, 317–326 (2018).
pubmed: 29500154
Demertzi, A. et al. Human consciousness is supported by dynamic complex patterns of brain signal coordination. Sci. Adv. 5, 7603 (2019).
Uhrig, L. et al. Resting-state dynamics as a cortical signature of anesthesia in monkeys. Anesthesiology 129, 942–958 (2018).
pubmed: 30028727
Amiri, M., Frauscher, B. & Gotman, J. Phase-amplitude coupling is elevated in deep sleep and in the onset zone of focal epileptic seizures. Front. Hum. Neurosci. 10, 387 (2016).
pubmed: 27536227 pmcid: 4971106
Usami, K. et al. The neural tides of sleep and consciousness revealed by single-pulse electrical brain stimulation. Sleep 42, 1 (2019).
Chialvo, D. R. Emergent complex neural dynamics. Nat. Phys. 6, 744–750 (2010).
Alonso, L. M. et al. Dynamical criticality during induction of anesthesia in human ECoG recordings. Front. Neural Circuits 8, 20 (2014).
pubmed: 24723852 pmcid: 3971201
Solovey, G. et al. Loss of consciousness is associated with stabilization of cortical activity. J. Neurosci. 35, 10866–10877 (2015).
pubmed: 26224868 pmcid: 4518057
Tajima, S., Yanagawa, T., Fujii, N. & Toyoizumi, T. Untangling brain-wide dynamics in consciousness by cross-embedding. PLoS Comput. Biol. 11, e1004537 (2015).
pubmed: 26584045 pmcid: 4652869
Krzemiński, D., Kamiński, M., Marchewka, A. & Bola, M. Breakdown of long-range temporal correlations in brain oscillations during general anesthesia. Neuroimage 159, 146–158 (2017).
pubmed: 28750775
Nir, Y. et al. Regional slow waves and spindles in human sleep. Neuron 70, 153–169 (2011).
pubmed: 21482364 pmcid: 3108825
Vizuete, J. A., Pillay, S., Ropella, K. M. & Hudetz, A. G. Graded defragmentation of cortical neuronal firing during recovery of consciousness in rats. Neuroscience 275, 340–351 (2014).
pubmed: 24952333 pmcid: 4165556
Lakatos, P., Karmos, G., Mehta, A. D., Ulbert, I. & Schroeder, C. E. Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320, 110–113 (2008).
pubmed: 18388295
Guenot, M. et al. Neurophysiological monitoring for epilepsy surgery: The Talairach SEEG method. StereoElectroEncephaloGraphy. Indications, results, complications and therapeutic applications in a series of 100 consecutive cases. Stereotact. Funct. Neurosurg. 77, 29–32 (2001).
pubmed: 12378053
Debailleul, A., Fichten, A. & Krivosic-Horber, R. L. Propofol et l’AIVOC en neuro-anesthésie. Ann. Fr. Anesth. Reanim. 23, 375–382 (2004).
pubmed: 15120784
Hans, P. et al. Target-controlled infusion of propofol and remifentanil combined with bispectral index monitoring for awake craniotomy. Anaesthesia 55, 255–259 (2000).
pubmed: 10671844
Rorden, C. & Brett, M. Stereotaxic display of brain lesions. Behav. Neurol. 12, 191–200 (2000).
pubmed: 11568431
Xia, M., Wang, J. & He, Y. BrainNet viewer: A network visualization tool for human brain connectomics. PLoS ONE 8, e68910 (2013).
pubmed: 23861951 pmcid: 3701683
Silber, M. H. et al. The visual scoring of sleep in adults. J. Clin. Sleep Med. 3, 121–131 (2007).
pubmed: 17557422
Magnin, M., Bastuji, H., Garcia-Larrea, L. & Mauguière, F. Human thalamic medial pulvinar nucleus is not activated during paradoxical sleep. Cereb. Cortex 14, 858–862 (2004).
pubmed: 15054059
Colombet, B., Woodman, M., Badier, J. M. & Bénar, C. G. AnyWave: A cross-platform and modular software for visualizing and processing electrophysiological signals. J. Neurosci. Methods 242, 118–126 (2015).
pubmed: 25614386
Oostenveld, R., Fries, P., Maris, E. & Schoffelen, J.-M. FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci. 2011, 156869 (2011).
pubmed: 21253357
Glickman, M. E., Rao, S. R. & Schultz, M. R. False discovery rate control is a recommended alternative to Bonferroni-type adjustments in health studies. J. Clin. Epidemiol. 67, 850–857 (2014).
pubmed: 24831050
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. 57, 289–300 (1995).
Hochberg, Y. & Benjamini, Y. More powerful procedures for multiple significance testing. Stat. Med. 9, 811–818 (1990).
pubmed: 2218183
Giacino, J. T. et al. The minimally conscious state: Definition and diagnostic criteria. Neurology 58, 349–353 (2002).
pubmed: 11839831 pmcid: 11839831
Kalmar, K. & Giacino, J. The JFK coma recovery scale—revised. Neuropsychol. Rehabil. 15, 454–460 (2005).
pubmed: 16350986
Gramfort, A. et al. MNE software for processing MEG and EEG data. Neuroimage 86, 446–460 (2014).
pubmed: 24161808
Engemann, D. A. & Gramfort, A. Automated model selection in covariance estimation and spatial whitening of MEG and EEG signals. Neuroimage 108, 328–342 (2015).
pubmed: 25541187
Wilcox, R. R. & Rousselet, G. A. A guide to robust statistical methods in neuroscience. Curr. Protoc. Neurosci. 82, 1–30 (2018).
Maris, E., Schoffelen, J.-M. & Fries, P. Nonparametric statistical testing of coherence differences. J. Neurosci. Methods 163, 161–175 (2007).
pubmed: 17395267
Maris, E. & Oostenveld, R. Nonparametric statistical testing of EEG- and MEG-data. J. Neurosci. Methods 164, 177–190 (2007).
pubmed: 17517438

Auteurs

Pierre Bourdillon (P)

Department of Neurophysiology, Hospital for Neurology and Neurosurgery, Hospices Civils de Lyon, Lyon, France. pierre.bourdillon@neurochirurgie.fr.
Faculté de médecine Claude Bernard, Université de Lyon, Lyon, France. pierre.bourdillon@neurochirurgie.fr.
Brain and Spine Institue, INSERM U1127, CNRS 7225, 47 boulevard de l'Hôpital, 75013, Paris, France. pierre.bourdillon@neurochirurgie.fr.
Sorbonne Université, Paris, France. pierre.bourdillon@neurochirurgie.fr.

Bertrand Hermann (B)

Brain and Spine Institue, INSERM U1127, CNRS 7225, 47 boulevard de l'Hôpital, 75013, Paris, France.
Sorbonne Université, Paris, France.
Neuro Intensive Care Unit, Groupe Hospitalier Pitié-Salpêtrière, Assistance Publique Hôpitaux de Paris, Paris, France.

Marc Guénot (M)

Department of Neurophysiology, Hospital for Neurology and Neurosurgery, Hospices Civils de Lyon, Lyon, France.
Faculté de médecine Claude Bernard, Université de Lyon, Lyon, France.
Neuropain Team, Centre de Recherche en Neurosciences de Lyon, INSERM U1028, Lyon, France.

Hélène Bastuji (H)

Neuropain Team, Centre de Recherche en Neurosciences de Lyon, INSERM U1028, Lyon, France.
Functional Neurology Department and Sleep Center, Hospices Civils de Lyon, Lyon, France.

Jean Isnard (J)

Functional Neurology Department and Sleep Center, Hospices Civils de Lyon, Lyon, France.

Jean-Rémi King (JR)

Brain and Spine Institue, INSERM U1127, CNRS 7225, 47 boulevard de l'Hôpital, 75013, Paris, France.

Jacobo Sitt (J)

Brain and Spine Institue, INSERM U1127, CNRS 7225, 47 boulevard de l'Hôpital, 75013, Paris, France.

Lionel Naccache (L)

Brain and Spine Institue, INSERM U1127, CNRS 7225, 47 boulevard de l'Hôpital, 75013, Paris, France. lionel.naccache@gmail.com.
Sorbonne Université, Paris, France. lionel.naccache@gmail.com.
Department of Neurophysiology, Groupe Hospitalier Pitié-Salpêtrière, Assistance Publique Hôpitaux de Paris, Paris, France. lionel.naccache@gmail.com.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH