Giga Consciousness-Coma Science Group ; CHU de Liège - Centre du Cerveau
Disciplines :
Neurosciences & behavior
Author, co-author :
Candia-Rivera, Diego ✱
Annen, Jitka ✱; Université de Liège - ULiège > GIGA Consciousness - Coma Science Group ; CHU Liège - Central University Hospital of Liege > Centre du Cerveau
Gosseries, Olivia ; Université de Liège - ULiège > GIGA Consciousness - Coma Science Group
Martial, Charlotte ; Université de Liège - ULiège > GIGA Consciousness - Coma Science Group
THIBAUT, Aurore ; Centre Hospitalier Universitaire de Liège - CHU > Autres Services Médicaux > Service de médecine de l'appareil locomoteur
LAUREYS, Steven ✱; Université de Liège - ULiège > GIGA Consciousness - Coma Science Group
Tallon-Baudry, C ✱
✱ These authors have contributed equally to this work.
Language :
English
Title :
Neural responses to heartbeats detect residual signs of consciousness during resting state in post-comatose patients
Publication date :
2021
Journal title :
Journal of Neuroscience
ISSN :
0270-6474
eISSN :
1529-2401
Publisher :
Society for Neuroscience, United States - District of Columbia
Al E, Iliopoulos F, Forschack N, Nierhaus T, Grund M, Motyka P, Gaebler M, Nikulin VV, Villringer A (2020) Heart-brain interactions shape somatosensory perception and evoked potentials. Proc Natl Acad Sci U S A 117:10575-10584.
Andrews-Hanna JR, Reidler JS, Sepulcre J, Poulin R, Buckner RL (2010) Functional-anatomic fractionation of the brain's default network. Neuron 65:550-562.
Azzalini D, Rebollo I, Tallon-Baudry C (2019) Visceral signals shape brain dynamics and cognition. Trends Cogn Sci 23:488-509.
Babo-Rebelo M, Richter CG, Tallon-Baudry C (2016a) Neural responses to heartbeats in the default network encode the self in spontaneous thoughts. J Neurosci 36:7829-7840.
Babo-Rebelo M, Wolpert N, Adam C, Hasboun D, Tallon-Baudry C (2016b) Is the cardiac monitoring function related to the self in both the default network and right anterior insula? Philos Trans R Soc Lond B Biol Sci 371:20160004.
Babo-Rebelo M, Buot A, Tallon-Baudry C (2019) Neural responses to heartbeats distinguish self fromother during imagination. Neuroimage 191:10-20.
Bayne T, Hohwy J, Owen AM (2017) Reforming the taxonomy in disorders of consciousness. Ann Neurol 82:866-872.
Blanke O, Metzinger T (2009) Full-body illusions and minimal phenomenal selfhood. Trends Cogn Sci 13:7-13.
Block N (2005) Two neural correlates of consciousness. Trends Cogn Sci 9:46-52.
Bodart O, Gosseries O, Wannez S, Thibaut A, Annen J, Boly M, Rosanova M, Casali AG, Casarotto S, Tononi G, Massimini M, Laureys S (2017) Measures of metabolism and complexity in the brain of patients with disorders of consciousness. Neuroimage 14:354-362.
Breiman L (2001) Random forests. Mach Learn 45:5-32.
Candia-Rivera D, Catrambone V, Valenza G (2020a)Methodological considerations on EEG electrical reference: A functional brain-heart interplay study. 42nd Annual International Conference of the IEEE Engineering in Medicine & Biology Society (EMBC), 20-24, July, Montreal, QC, Canada.
Candia-Rivera D, Catrambone V, Valenza G (2020b) The role of EEG electrical reference in the assessment of Functional brain-heart interplay: a preliminary study. 11th Conference of the European Study Group on Cardiovascular Oscillations (ESGCO), 15 July, Pisa, Italy.
Casali AG, Gosseries O, Rosanova M, Boly M, Sarasso S, Casali KR, Casarotto S, Bruno M-A, Laureys S, Tononi G, Massimini M (2013) A theoretically based index of consciousness independent of sensory processing and behavior. Sci Transl Med 5:198ra105.
Casarotto S, Comanducci A, Rosanova M, Sarasso S, Fecchio M, Napolitani M, Pigorini A, Casali AG, Trimarchi PD, Boly M, Gosseries O, Bodart O, Curto F, Landi C, Mariotti M, Devalle G, Laureys S, Tononi G, Massimini M (2016) Stratification of unresponsive patients by an independently validated index of brain complexity. Ann Neurol 80:718-729.
Chalmers DJ (1995) Facing up to the problem of consciousness. J Conscious Stud 2:200-219.
Combrisson E, Jerbi K (2015) Exceeding chance level by chance: the caveat of theoretical chance levels in brain signal classification and statistical assessment of decoding accuracy. J Neurosci Methods 250:126-136.
Cruse D, Chennu S, Chatelle C, Bekinschtein TA, Fernández-Espejo D, Pickard JD, Laureys S, Owen AM (2011) Bedside detection of awareness in the vegetative state: a cohort study. Lancet 378:2088-2094.
Di Perri C, Bahri MA, Amico E, Thibaut A, Heine L, Antonopoulos G, Charland-Verville V, Wannez S, Gomez F, Hustinx R, Tshibanda L, Demertzi A, Soddu A, Laureys S (2016) Neural correlates of consciousness in patients who have emerged from a minimally conscious state: a cross-sectional multimodal imaging study. Lancet Neurol 15:830-842.
Dirlich G, Vogl L, Plaschke M, Strian F (1997) Cardiac field effects on the EEG. Electroencephalogr Clin Neurophysiol 102:307-315.
Engemann DA, 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 JD (2018) Robust EEG-based cross-site and cross-protocol classification of states of consciousness. Brain 141:3179-3192.
Frässle S, Sommer J, Jansen A, Naber M, Einhäuser W (2014) Binocular rivalry: frontal activity relates to introspection and action but not to perception. J Neurosci 34:1738-1747.
Giacino JT, Ashwal S, Childs N, Cranford R, Jennett B, Katz DI, Kelly JP, Rosenberg JH, Whyte J, Zafonte RD, Zasler ND (2002) The minimally conscious state: definition and diagnostic criteria. Neurology 58:349-353.
Giacino JT, Kalmar K, Whyte J (2004) The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil 85:2020-2029.
Giacino JT, Katz DI, Schiff ND, Whyte J, Ashman EJ, Ashwal S, Barbano R, Hammond FM, Laureys S, Ling GSF, Nakase-Richardson R, Seel RT, Yablon S, Getchius TSD, Gronseth GS, Armstrong MJ (2018) Practice guideline update recommendations summary: disorders of consciousness: Report of the Guideline Development, Dissemination, and Implementation Subcommittee of the American Academy of Neurology; the American Congress of Rehabilitation Medicine; and the National Institute on Disability, Independent Living, and Rehabilitation Research. Arch Phys Med Rehabil 99:1699-1709.
Gosseries O, Zasler ND, Laureys S (2014) Recent advances in disorders of consciousness: focus on the diagnosis. Brain Injury 28:1141-1150.
Haxby JV, Grady CL, Horwitz B, Ungerleider LG, Mishkin M, Carson RE, Herscovitch P, Schapiro MB, Rapoport SI (1991) Dissociation of object and spatial visual processing pathways in human extrastriate cortex. Proc Natl Acad Sci U S A 88:1621-1625.
Jung T-P, Humphries C, Lee T-W, Makeig S, McKeown MJ, Iragui V, Sejnowski TJ (1998) Extended ICA removes artifacts from electroence phalographic recordings. In: Advances in neural information processing systems (Jordan MI, Kearns MJ, Solla SA, eds), pp 894-900. Cambridge, MA:MIT.
Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17:4302-4311.
Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773-795.
Kern M, Aertsen A, Schulze-Bonhage A, Ball T (2013) Heart cycle-related effects on event-related potentials, spectral power changes, and connectivity patterns in the human ECoG. Neuroimage 81:178-190.
Kondziella D, Bender A, Diserens K, van Erp W, Estraneo A, Formisano R, Laureys S, Naccache L, Ozturk S, Rohaut B, Sitt JD, Stender J, Tiainen M, Rossetti AO, Gosseries O, Chatelle C (2020) European Academy of Neurology guideline on the diagnosis of coma and other disorders of consciousness. Eur J Neurol 27:741-756.
Laureys S, Owen AM, Schiff ND (2004) Brain function in coma, vegetative state, and related disorders. Lancet Neurol 3:537-546.
Laureys S, Celesia GG, Cohadon F, Lavrijsen J, León-Carrión J, Sannita WG, Sazbon L, Schmutzhard E, von Wild KR, Zeman A, Dolce G (2010) Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med 8:68.
Leo A, Naro A, Cannavò A, Pisani LR, Bruno R, Salviera C, Bramanti P, Calabrò RS (2016) Could autonomic system assessment be helpful in disorders of consciousness diagnosis? A neurophysiological study. Exp Brain Res 234:2189-2199.
Luu P, Ferree TC (2000) Determination of the geodesic sensor nets' average electrode positions and their 10-10 international equivalents. Eugene, OR: Electrical Geodesics.
Mishkin M, Ungerleider LG, Macko KA (1983) Object vision and spatial vision: two cortical pathways. Trends Neurosci 6:414-417.
Nakayama N, Okumura A, Shinoda J, Nakashima T, Iwama T (2006) Relationship between regional cerebral metabolism and consciousness disturbance in traumatic diffuse brain injury without large focal lesions: an FDG-PET study with statistical parametric mapping analysis. J Neurol Neurosurg Psychiatry 77:856-862.
Ojala M, Garriga GC (2010) Permutation tests for studying classifier performance. JMach Learn Res 11:1833-1863.
Oostenveld R, Fries P, Maris E, Schoffelen J-M (2011) Field Trip: open source software for advanced analysis of MEG. Comput Intell Neurosci 2011:156869.
Pal M (2005) Random forest classifier for remote sensing classification. Int J Remote Sens 26:217-222.
Park H-D, Tallon-Baudry C (2014) The neural subjective frame: from bodily signals to perceptual consciousness. Philos Trans R Soc Lond B Biol Sci 369:20130208.
Park H-D, Correia S, Ducorps A, Tallon-Baudry C (2014) Spontaneous fluctuations in neural responses to heartbeats predict visual detection. Nat Neurosci 17:612-618.
Park H-D, Bernasconi F, Bello-Ruiz J, Pfeiffer C, Salomon R, Blanke O (2016) Transient modulations of neural responses to heartbeats covary with bodily self-consciousness. J Neurosci 36:8453-8460.
Park H-D, Bernasconi F, Salomon R, Tallon-Baudry C, Spinelli L, Seeck M, Schaller K, Blanke O (2018) Neural sources and underlying mechanisms of neural responses to heartbeats, and their role in bodily self-consciousness: an intracranial EEG study. Cereb Cortex 28:2351-2364.
Raimondo F, Rohaut B, Demertzi A, Valente M, Engemann DA, Salti M, Fernandez Slezak D, Naccache L, Sitt JD (2017) Brain-heart interactions reveal consciousness in noncommunicating patients. Ann Neurol 82:578-591.
Riganello F, Chatelle C, Schnakers C, Laureys S (2018a) Heart rate variability as an indicator of nociceptive pain in disorders of consciousness? J Pain Symptom Manage 57:47-56.
Riganello F, Larroque SK, Bahri MA, Heine L, Martial C, Carrière M, Charland-Verville V, Aubinet C, Vanhaudenhuyse A, Chatelle C, Laureys S, Di PC (2018b) A heartbeat away from consciousness: heart rate variability entropy can discriminate disorders of consciousness and is correlated with resting-state fMRI brain connectivity of the central autonomic network. Front Neurol 9:769.
Rouder JN, Speckman PL, Sun D, Morey RD, Iverson G (2009) Bayesian t tests for accepting and rejecting the null hypothesis. Psychon Bull Rev 16:225-237.
Rudolf J, Ghaemi M, Ghaemi M, Haupt WF, Szelies B, Heiss WD (1999) Cerebral glucose metabolism in acute and persistent vegetative state. J Neurosurg Anesthesiol 11:17-24.
Schandry R, Sparrer B, Weitkunat R (1986) From the heart to the brain: a study of heartbeat contingent scalp potentials. Int J Neurosci 30:261-275.
Schiff ND (2015) Cognitive motor dissociation following severe brain injuries. JAMA Neurol 72:1413-1415.
Sel A, Azevedo RT, Tsakiris M (2017) Heartfelt self: cardio-visual integration affects self-face recognition and interoceptive cortical processing. Cereb Cortex 27:5144-5155.
Sergent C, Faugeras F, Rohaut B, Perrin F, Valente M, Tallon-Baudry C, Cohen L, Naccache L (2017) Multidimensional cognitive evaluation of patients with disorders of consciousness using EEG: a proof of concept study. Neuroimage Clin 13:455-469.
Sitt JD, King J-R, El Karoui I, Rohaut B, Faugeras F, Gramfort A, Cohen L, Sigman M, Dehaene S, Naccache L (2014) Large scale screening of neural signatures of consciousness in patients in a vegetative or minimally conscious state. Brain 137:2258-2270.
Song M, Yang Y, He J, Yang Z, Yu S, Xie Q, Xia X, Dang Y, Zhang Q, Wu X, Cui Y, Hou B, Yu R, Xu R, Jiang T (2018) Prognostication of chronic disorders of consciousness using brain functional networks and clinical characteristics. eLife 7:e36173.
Sperry R (1984) Consciousness, personal identity and the divided brain. Neuropsychologia 22:661-673.
Stender J, Gosseries O, Bruno M-A, Charland-Verville V, Vanhaudenhuyse A, Demertzi A, Chatelle C, Thonnard M, Thibaut A, Heine L, Soddu A, Boly M, Schnakers C, Gjedde A, Laureys S (2014) Diagnostic precision of PET imaging and functional MRI in disorders of consciousness: a clinical validation study. Lancet 384:514-522.
Stender J, Kupers R, Rodell A, Thibaut A, Chatelle C, Bruno M-A, Gejl M, Bernard C, Hustinx R, Laureys S, Gjedde A (2015) Quantitative rates of brain glucose metabolism distinguish minimally conscious from vegetative state patients. J Cereb Blood Flow Metab 35:58-65.
Steyerberg EW, Uno H, Ioannidis JPA, Calster B van, Ukaegbu C, Dhingra T, Syngal S, Kastrinos F (2018) Poor performance of clinical prediction models: the harmof commonly appliedmethods. JClin Epidemiol 98:133-143.
Strobl C, Boulesteix A-L, Kneib T, Augustin T, Zeileis A (2008) Conditional variable importance for random forests. BMC Bioinformatics 9:307.
Tallon-Baudry C, Campana F, Park H-D, Babo-Rebelo M (2018) The neural monitoring of visceral inputs, rather than attention, accounts for firstperson perspective in conscious vision. Cortex 102:139-149.
Task Force of the European Society of Cardiology the North American Society of Pacing (1996) Heart rate variability: standards of measurement, physiological interpretation, and clinical use. Circulation 93:1043-1065.
Thayer JF, Peasley C, Muth ER (1996) Estimation of respiratory frequency from autoregressive spectral analysis of heart period. Biomed Sci Instrum 32:93-99.
Thibaut A, Bruno M-A, Chatelle C, Gosseries O, Vanhaudenhuyse A, Demertzi A, Schnakers C, Thonnard M, Charland-Verville V, Bernard C, Bahri M, Phillips C, Boly M, Hustinx R, Laureys S (2012) Metabolic activity in external and internal awareness networks in severely brain-damaged patients. J Rehabil Med 44:487-494.
Tobaldini E, Toschi-Dias E, Trimarchi PD, Brena N, Comanducci A, Casarotto S, Montano N, Devalle G (2018) Cardiac autonomic responses to nociceptive stimuli in patients with chronic disorders of consciousness. Clin Neurophysiol 129:1083-1089.
Tommasino C, Grana C, Lucignani G, Torri G, Fazio F (1995) Regional cerebral metabolism of glucose in comatose and vegetative state patients. J Neurosurg Anesthesiol 7:109-116.
Tsuchiya N, Wilke M, Frässle S, Lamme VAF (2015) No-report paradigms: extracting the true neural correlates of consciousness. Trends Cogn Sci 19:757-770.
Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNIMRI single-subject brain. Neuro Image 15:273-289.
van Veluw SJ, Chance SA (2014) Differentiating between self and others: an ALE meta-analysis of fMRI studies of self-recognition and theory of mind. Brain Imaging Behav 8:24-38.
Verikas A, Gelzinis A, Bacauskiene M (2011) Mining data with random forests: a survey and results of new tests. Pattern Recognit 44:330-349.
Wannez S, Heine L, Thonnard M, Gosseries O, Laureys S (2017) The repetition of behavioral assessments in diagnosis of disorders of consciousness. Ann Neurol 81:883-889.
Woo C-W, Chang LJ, Lindquist MA, Wager TD (2017) Building better biomarkers: brain models in translational neuroimaging. Nat Neurosci 20:365-377.
Yarkoni T, Poldrack RA, Nichols TE, Van Essen DC, Wager TD (2011) Large-scale automated synthesis of human functional neuroimaging data. Nat Methods 8:665-670.
