Artículo

Engemann, D.A.; Raimondo, F.; King, J.-R.; Rohaut, B.; Louppe, G.; Faugeras, F.; Annen, J.; Cassol, H.; Gosseries, O.; Fernandez-Slezak, D.; Laureys, S.; Naccache, L.; Dehaene, S.; Sitt, J.D. "Robust EEG-based cross-site and cross-protocol classification of states of consciousness" (2018) Brain. 141(11):3179-3192
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Determining the state of consciousness in patients with disorders of consciousness is a challenging practical and theoretical problem. Recent findings suggest that multiple markers of brain activity extracted from the EEG may index the state of consciousness in the human brain. Furthermore, machine learning has been found to optimize their capacity to discriminate different states of consciousness in clinical practice. However, it is unknown how dependable these EEG markers are in the face of signal variability because of different EEG configurations, EEG protocols and subpopulations from different centres encountered in practice. In this study we analysed 327 recordings of patients with disorders of consciousness (148 unresponsive wakefulness syndrome and 179 minimally conscious state) and 66 healthy controls obtained in two independent research centres (Paris Pitié-Salpêtrière and Liège). We first show that a non-parametric classifier based on ensembles of decision trees provides robust out-of-sample performance on unseen data with a predictive area under the curve (AUC) of ∼0.77 that was only marginally affected when using alternative EEG configurations (different numbers and positions of sensors, numbers of epochs, average AUC = 0.750 ± 0.014). In a second step, we observed that classifiers based on multiple as well as single EEG features generalize to recordings obtained from different patient cohorts, EEG protocols and different centres. However, the multivariate model always performed best with a predictive AUC of 0.73 for generalization from Paris 1 to Paris 2 datasets, and an AUC of 0.78 from Paris to Liège datasets. Using simulations, we subsequently demonstrate that multivariate pattern classification has a decisive performance advantage over univariate classification as the stability of EEG features decreases, as different EEG configurations are used for feature-extraction or as noise is added. Moreover, we show that the generalization performance from Paris to Liège remains stable even if up to 20% of the diagnostic labels are randomly flipped. Finally, consistent with recent literature, analysis of the learned decision rules of our classifier suggested that markers related to dynamic fluctuations in theta and alpha frequency bands carried independent information and were most influential. Our findings demonstrate that EEG markers of consciousness can be reliably, economically and automatically identified with machine learning in various clinical and acquisition contexts. © The Author(s) (2018). Published by Oxford University Press on behalf of the Guarantors of Brain.

Registro:

Documento: Artículo
Título:Robust EEG-based cross-site and cross-protocol classification of states of consciousness
Autor:Engemann, D.A.; Raimondo, F.; King, J.-R.; Rohaut, B.; Louppe, G.; Faugeras, F.; Annen, J.; Cassol, H.; Gosseries, O.; Fernandez-Slezak, D.; Laureys, S.; Naccache, L.; Dehaene, S.; Sitt, J.D.
Filiación:Parietal Project-team, INRIA Saclay - Île de France, France
Cognitive Neuroimaging Unit, Université Paris-Saclay, NeuroSpin Center, Gif sur Yvette, France
Inserm U 1127, Institut du Cerveau et de la Moelle Épinière, ICM, Paris, France
Laboratorio de Inteligencia Artificial Aplicada, Departamento de Computación FCEyN, UBA, Argentina
CONICET - Universidad de Buenos Aires, Instituto de Investigación en Ciencias de la Computación, Ciudad Autónoma de Buenos Aires, Godoy Cruz, 2290, Argentina
Sorbonne Universités, UPMC Université Paris 06, Faculté de Médecine Pitié-Salpêtrière, Paris, France
New York University, 6 Washington Place, New York, NY, United States
Frankfurt Institute for Advanced Studies, Frankfurt, Germany
Department of Neurology, Columbia University, New York, NY, United States
Coma Science Group, GIGA Consciousness, University and University Hospital of Liège, Liège, Belgium
Collège de France, Paris, France
Palabras clave:biomarker; diagnosis; disorders of consciousness; electroencephalography; machine learning; adult; alpha rhythm; area under the curve; Article; clinical protocol; consciousness; controlled study; decision tree; disease classification; electroencephalography; female; human; major clinical study; male; middle aged; minimally conscious state; priority journal; theta rhythm; wakefulness
Año:2018
Volumen:141
Número:11
Página de inicio:3179
Página de fin:3192
DOI: http://dx.doi.org/10.1093/brain/awy251
Título revista:Brain
Título revista abreviado:Brain
ISSN:00068950
CODEN:BRAIA
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00068950_v141_n11_p3179_Engemann

Referencias:

  • Axmacher, N., Henseler, M.M., Jensen, O., Weinreich, I., Elger, C.E., Fell, J., Cross-frequency coupling supports multi-item working memory in the human hippocampus (2010) Proc Natl Acad Sci USA, 107, pp. 3228-3233
  • Bayne, T., Hohwy, J., Owen, A.M., Are there levels of consciousness? (2016) Trends Cogn Sci, 20, pp. 405-413
  • Bekinschtein, T.A., Dehaene, S., Rohaut, B., Tadel, F., Cohen, L., Naccache, L., Neural signature of the conscious processing of auditory regularities (2009) Proc Natl Acad Sci USA, 106, pp. 1672-1677
  • Bruno, M.A., Vanhaudenhuyse, A., Thibaut, A., Moonen, G., Laureys, S., From unresponsive wakefulness to minimally conscious PLUS and functional locked-in syndromes: Recent advances in our understanding of disorders of consciousness (2011) J Neurol, 258, pp. 1373-1384
  • Bzdok, D., Engemann, D.-A., Grisel, O., Varoquaux, G., Thirion, B., Prediction and inference diverge in biomedicine: Simulations and real-world data (2018) BioRxiv
  • Casali, A.G., Gosseries, O., Rosanova, M., Boly, M., Sarasso, S., Casali, K.R., A theoretically based index of consciousness independent of sensory processing and behavior (2013) Sci Transl Med, 5, p. 198ra105
  • Chang, H.Y., Nuyten, D.S.A., Sneddon, J.B., Hastie, T., Tibshirani, R., Sørlie, T., Robustness, scalability, and integration of a wound-response gene expression signature in predicting breast cancer survival (2005) Proc Natl Acad Sci USA, 102, pp. 3738-3743
  • Chennu, S., Annen, J., Wannez, S., Thibaut, A., Chatelle, C., Cassol, H., Brain networks predict metabolism, diagnosis and prognosis at the bedside in disorders of consciousness (2017) Brain, 140, pp. 2120-2132
  • Claassen, J., Velazquez, A., Meyers, E., Witsch, J., Falo, M.C., Park, S., Bedside quantitative electroencephalography improves assessment of consciousness in comatose subarachnoid hemorrhage patients (2016) Ann Neurol, 80, pp. 541-553
  • Cruse, D., Chennu, S., Chatelle, C., Bekinschtein, T.A., Fernández-Espejo, D., Pickard, J.D., Bedside detection of awareness in the vegetative state: A cohort study (2012) Lancet, 378, pp. 2088-2094
  • Curley, W.H., Forgacs, P.B., Voss, H.U., Conte, M.M., Schiff, N.D., Characterization of EEG signals revealing covert cognition in the injured brain (2018) Brain, 141, pp. 1404-1421
  • Dehaene, S., Changeux, J.-P., Naccache, L., Sackur, J., Sergent, C., Conscious, preconscious, and subliminal processing: A testable taxonomy (2006) Trends Cogn Sci, 10, pp. 204-211
  • Dehaene, S., Naccache, L., Towards a cognitive neuroscience of consciousness: Basic evidence and a workspace framework (2001) Cognition, 79, pp. 1-37
  • Demertzi, A., Antonopoulos, G., Heine, L., Voss, H.U., Crone, J.S., De Los Angeles, C., Intrinsic functional connectivity differentiates minimally conscious from unresponsive patients (2015) Brain, 138, pp. 2619-2631
  • Demertzi, A., Gomez, F., Crone, J.S., Vanhaudenhuyse, A., Tshibanda, L., Noirhomme, Q., Multiple fMRI system-level baseline connectivity is disrupted in patients with consciousness alterations (2014) Cortex, 52, pp. 35-46
  • Donchin, E., Coles, M.G.H., Is the P300 component a manifestation of context updating (1988) Behav Brain Sci, 11, pp. 357-427
  • Efron, B., Tibshirani, R., (1993) An Introduction to the Bootstrap, , New York, NY: Chapman & Hall
  • Emmons, W.H., Simon, C.W., EEG, consciousness, and sleep (1956) Science, 124, pp. 1066-1069
  • Engemann, D., Raimondo, F., King, J.-R., Jas, M., Gramfort, A., Dehaene, S., Automated measurement and prediction of consciousness in vegetative and minimally conscious patients (2015) ICML Workshop on Statistics, Machine Learning and Neuroscience, , Lille, France; 2015
  • Faugeras, F., Rohaut, B., Valente, M., Sitt, J., Demeret, S., Bolgert, F., Survival and consciousness recovery are better in the minimally conscious state than in the vegetative state (2018) Brain Inj, 32, pp. 72-77
  • Geurts, P., Ernst, D., Wehenkel, L., Extremely randomized trees (2006) Machine Learning, 63, p. 3. , Springer/Kluwer Academic Publishers
  • Giacino, J.T., Ashwal, S., Childs, N., Cranford, R., Jennett, B., Katz, D.I., The minimally conscious state definition and diagnostic criteria (2002) Neurology, 58, pp. 349-353
  • Giacino, J.T., Kalmar, K., Whyte, J., The JFK Coma Recovery Scale- Revised: Measurement characteristics and diagnostic utility11No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon (2004) Arch Phys Med Rehabil, 85, pp. 2020-2029
  • Goldfine, A.M., Victor, J.D., Conte, M.M., Bardin, J.C., Schiff, N.D., Determination of awareness in patients with severe brain injury using EEG power spectral analysis (2011) Clin Neurophysiol, 122, pp. 2157-2168
  • Gosseries, O., Zasler, N.D., Laureys, S., Recent advances in disorders of consciousness: Focus on the diagnosis (2014) Brain Inj, 28, pp. 1141-1150
  • Gramfort, A., Luessi, M., Larson, E., Engemann, D., Strohmeier, D., Brodbeck, C., MNE software for processing MEG and EEG data (2014) Neuroimage, 86, pp. 446-460
  • Iotzov, I., Fidali, B.C., Petroni, A., Conte, M.M., Schiff, N.D., Parra, L.C., Divergent neural responses to narrative speech in disorders of consciousness (2017) Ann Clin Transl Neurol, 4, pp. 784-792
  • Jas, M., Engemann, D.A., Bekhti, Y., Raimondo, F., Gramfort, A., Autoreject: Automated artifact rejection for MEG and EEG data (2017) Neuroimage, 159, pp. 417-429
  • Jennett, B., Plum, F., Persistent vegetative state after brain damage: A syndrome in search of a name (1972) Lancet, 299, pp. 734-737
  • King, J.-R., Sitt, J.D., Faugeras, F., Rohaut, B., ElkI, E., Cohen, L., Information sharing in the brain indexes consciousness in noncommunicative patients (2013) Curr Biol, 23, pp. 1914-1919
  • King, J.R., Faugeras, F., Gramfort, A., Schurger, A., El Karoui, I., Sitt, J.D., Single-trial decoding of auditory novelty responses facilitates the detection of residual consciousness (2013) Neuroimage, 83, pp. 726-738
  • Laureys, S., Celesia, G.G., Cohadon, F., Lavrijsen, J., JoséL-C, Sannita, W.G., Unresponsive wakefulness syndrome: A new name for the vegetative state or apallic syndrome (2010) BMC Med, 8, p. 68
  • Lo, A., Chernoff, H., Zheng, T., Lo, S.-H., Why significant variables aren't automatically good predictors (2015) Pro. Natl Acad Sci USA, 112, pp. 13892-13897
  • Louppe, G., Wehenkel, L., Sutera, A., Geurts, P., Understanding variable importances in forests of randomized trees (2013) Advances in Neural Information Processing Systems, 26, pp. 431-439. , In: Burges CJC, Bottou L, Welling M, Ghahramani Z, Weinberger KQ, editors., (NIPS).Lake Tahoe: Curran Associates, Inc
  • Louppe, G., (2014) Understanding Random Forests: From Theory to Practice, , PhD thesis. University of Liège, Faculty of Applied Sciences, Department of Electrical Engineering & Computer Science
  • Luauté, J., Maucort-Boulch, D., Tell, L., Quelard, F., Sarraf, T., Iwaz, J., Long-term outcomes of chronic minimally conscious and vegetative states (2010) Neurology, 75, pp. 246-252
  • Lulé, D., Noirhomme, Q., Kleih, S.C., Chatelle, C., Halder, S., Demertzi, A., Probing command following in patients with disorders of consciousness using a brain-computer interface (2013) Clin Neurophysiol, 124, pp. 101-106
  • Monti, M.M., Vanhaudenhuyse, A., Coleman, M.R., Boly, M., Pickard, J.D., Tshibanda, L., Willful modulation of brain activity in disorders of consciousness (2010) N Engl J.Med, 362, pp. 579-589
  • Naccache, L., Minimally conscious state or cortically mediated state? (2018) Brain, 141, pp. 949-960
  • Naci, L., Monti, M.M., Cruse, D., Kübler, A., Sorger, B., Goebel, R., Brain-computer interfaces for communication with nonresponsive patients (2012) Ann Neurol, 72, pp. 312-323
  • Owen, A.M., Coleman, M.R., Boly, M., Davis, M.H., Laureys, S., Pickard, J.D., Detecting awareness in the vegetative state (2006) Science, 313, p. 1402
  • Pedregosa, F., Varoquaux, G., Gramfort, A., Michel, V., Thirion, B., Grisel, O., Scikit-learn: Machine learning in python (2011) J Mach Learn Res, 12, pp. 2825-2830
  • Phillips, C.L., Bruno, M.-A., Maquet, P., Boly, M., Noirhomme, Q., Schnakers, C., "Relevance vector machine'' consciousness classifier applied to cerebral metabolism of vegetative and locked-in patients (2011) Neuroimage, 56, pp. 797-808
  • Pins, D., The neural correlates of conscious vision (2003) Cereb Cortex, 13, pp. 461-474
  • Polich, J., Updating P300: An integrative theory of P3a and P3b (2007) Clin Neurophysiol, 118, pp. 2128-2148
  • Purdon, P.L., Pierce, E.T., Mukamel, E.A., Prerau, M.J., Walsh, J.L., Wong, K.F.K., Electroencephalogram signatures of loss and recovery of consciousness from propofol (2013) Proc Natl Acad Sci USA, 110, pp. E1142-E1151
  • Rohaut, B., Claassen, J., Decision making in perceived devastating brain injury: A call to explore the impact of cognitive biases (2018) Br J Anaesth, 120, pp. 5-9
  • Rohaut, B., Raimondo, F., Galanaud, D., Valente, M., Sitt, J.D., Naccache, L., Probing consciousness in a sensory-disconnected paralyzed patient (2017) Brain Inj, 31, pp. 1398-1403
  • Rosenberg, G.A., Johnson, S.F., Brenner, R.P., Recovery of cognition after prolonged vegetative state (1977) Ann Neurol, 2, pp. 167-168
  • Sadaghiani, S., Kleinschmidt, A., Brain networks and/-oscillations: Structural and functional foundations of cognitive control (2016) Trends Cogn Sci, 20, pp. 805-817
  • Saeb, S., Lonini, L., Jayaraman, A., Mohr, D.C., Kording, K.P., The need to approximate the use-case in clinical machine learning (2017) Gigascience, 6, pp. 1-9
  • Schiff, N.D., Recovery of consciousness after brain injury: A mesocircuit hypothesis (2010) Trends Neurosci, 33, pp. 1-9
  • Schiff, N.D., Cognitive motor dissociation following severe brain injuries (2015) JAMA Neurol, 72, pp. 1413-1415
  • Schiff, N.D., Nauvel, T., Victor, J.D., Large-scale brain dynamics in disorders of consciousness (2014) Curr Opin Neurobiol, 25, pp. 7-14
  • Schnakers, C., Vanhaudenhuyse, A., Giacino, J., Ventura, M., Boly, M., Majerus, S., Diagnostic accuracy of the vegetative and minimally conscious state: Clinical consensus versus standardized neurobehavioral assessment (2009) BMC Neurol, 9, p. 35
  • Sergent, C., Baillet, S., Dehaene, S., Timing of the brain events underlying access to consciousness during the attentional blink (2005) Nat Neurosci, 8, pp. 1391-1400
  • Sergent, C., Faugeras, F., Rohaut, B., Perrin, F., Valente, M., Tallon-Baudry, C., Multidimensional cognitive evaluation of patients with disorders of consciousness using EEG: A proof of concept study (2017) Neuroimage Clin, 13, pp. 455-469
  • Sitt, J.D., King, J.-R., El Karoui, I., Rohaut, B., Faugeras, F., Gramfort, A., Large scale screening of neural signatures of consciousness in patients in a vegetative or minimally conscious state (2014) Brain, 137, pp. 2258-2270
  • Stender, J., Gosseries, O., Bruno, M.-A., Charland-Verville, V., Vanhaudenhuyse, A., Demertzi, A., Diagnostic precision of PET imaging and functional MRI in disorders of consciousness: A clinical validation study (2014) Lancet, 384, pp. 514-522
  • Tononi, G., Edelman, G.M., Consciousness and complexity (1998) Science, 282, pp. 1846-1851
  • Varoquaux, G., Cross-validation failure: Small sample sizes lead to large error bars (2018) Neuroimage, 180, pp. 68-77
  • Varoquaux, G., Raamana, P.R., Engemann, D.A., Hoyos-Idrobo, A., Schwartz, Y., Thirion, B., Assessing and tuning brain decoders: Cross-validation, caveats, and guidelines (2016) Neuroimage
  • Victor, J.D., Drover, J.D., Conte, M.M., Schiff, N.D., Mean-field modeling of thalamocortical dynamics and a model-driven approach to EEG analysis (2011) Proc Natl Acad Sci USA, 108, pp. 15631-15638
  • Wannez, S., Heine, L., Thonnard, M., Gosseries, O., Laureys, S., The repetition of behavioral assessments in diagnosis of disorders of consciousness (2017) Ann Neurol, 81, pp. 883-889. , Coma Science Group Collaborators
  • Williams, S.T., Conte, M.M., Goldfine, A.M., Noirhomme, Q., Gosseries, O., Thonnard, M., Common resting brain dynamics indicate a possible mechanism underlying zolpidem response in severe brain injury (2013) Elife, 2, p. e01157
  • Woo, C.-W., Chang, L.J., Lindquist, M.A., Wager, T.D., Building better biomarkers: Brain models in translational neuroimaging (2017) Nat Neurosci, 20, pp. 365-377

Citas:

---------- APA ----------
Engemann, D.A., Raimondo, F., King, J.-R., Rohaut, B., Louppe, G., Faugeras, F., Annen, J.,..., Sitt, J.D. (2018) . Robust EEG-based cross-site and cross-protocol classification of states of consciousness. Brain, 141(11), 3179-3192.
http://dx.doi.org/10.1093/brain/awy251
---------- CHICAGO ----------
Engemann, D.A., Raimondo, F., King, J.-R., Rohaut, B., Louppe, G., Faugeras, F., et al. "Robust EEG-based cross-site and cross-protocol classification of states of consciousness" . Brain 141, no. 11 (2018) : 3179-3192.
http://dx.doi.org/10.1093/brain/awy251
---------- MLA ----------
Engemann, D.A., Raimondo, F., King, J.-R., Rohaut, B., Louppe, G., Faugeras, F., et al. "Robust EEG-based cross-site and cross-protocol classification of states of consciousness" . Brain, vol. 141, no. 11, 2018, pp. 3179-3192.
http://dx.doi.org/10.1093/brain/awy251
---------- VANCOUVER ----------
Engemann, D.A., Raimondo, F., King, J.-R., Rohaut, B., Louppe, G., Faugeras, F., et al. Robust EEG-based cross-site and cross-protocol classification of states of consciousness. Brain. 2018;141(11):3179-3192.
http://dx.doi.org/10.1093/brain/awy251