[en] Background: This review discusses the advantages of transcranial magnetic stimulation combined with high-density electroencephalography (TMS-hdEEG) over other current techniques of brain imaging. Methods and results: Its application was reviewed, focusing particularly on disorders of consciousness, in the perspective of recent theories of consciousness. Assessment of non-communicative patients with disorders of consciousness remains a clinical challenge and objective measures of the level of consciousness are still needed. Current theories suggest that a key requirement for consciousness is the brain’s capacity to rapidly integrate information across different specialized cortical areas. TMS-EEG allows the stimulation of any given cortical area and the recording of the immediate electrical cortical response. This technique has recently been successfully employed to measure changes in brain complexity under physiological, pharmacological and pathological conditions.
Conclusions: This suggests that TMS-EEG is a reliable tool to discriminate between conscious and unconscious patients at the single subject level. Future works are needed to validate and implement this technique as a clinical tool.
Research center :
GIGA CRC (Cyclotron Research Center) In vivo Imaging-Aging & Memory - ULiège
Disciplines :
Neurology
Author, co-author :
Napolitani, Martino ✱; Università degli Studi di Milano
Bodart, Olivier ✱; Université de Liège - ULiège > Centre de recherches du cyclotron
Canali, P.
Seregni, F.
Rosanova, Mario; Università degli Studi di Milano
Laureys, Steven ; Université de Liège - ULiège > Centre de recherches du cyclotron
Massimini, Marcello; Università degli Studi di Milano
Gosseries, Olivia ; Université de Liège - ULiège > Centre de recherches du cyclotron
✱ These authors have contributed equally to this work.
Language :
English
Title :
Transcranial magnetic stimulation combined with high density EEG in altered states of consciousness
Publication date :
September 2014
Journal title :
Brain Injury
ISSN :
0269-9052
eISSN :
1362-301X
Publisher :
Informa Healthcare, United Kingdom
Volume :
28
Issue :
9
Pages :
1180-1189
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Laureys S, Celesia GG, Cohadon F, Lavrijsen J, Leon-Carrion J, Sannita WG, Sazbon L, Schmutzhard E, von Wild KR, Zeman A, et al. Unresponsive wakefulness syndrome: A new name for the vegetative state or apallic syndrome. BMC Medicine 2010;8:68.
Giacino JT, Ashwal S, Childs N, Cranford R, Jennett B, Katz DI, Kelly JP, Rosenberg JH, Whyte J, Zafonte RD, et al. The minimally conscious state: Definition and diagnostic criteria. Neurology 2002; 58:349-353.
Schnakers C, Vanhaudenhuyse A, Giacino J, Ventura M, Boly M, Majerus S, Moonen G, Laureys S. Diagnostic accuracy of the vegetative and minimally conscious state: Clinical consensus versus standardized neurobehavioral assessment. BMC Neurology 2009;9: 35.
Giacino JT, Kalmar K, Whyte J. The JFK Coma Recovery Scale-Revised: Measurement characteristics and diagnostic utility. Archives of Physical Medicine and Rehabilitation 2004;85: 2020-2029.
Massimini M, Boly M, Casali A, Rosanova M, Tononi G. A perturbational approach for evaluating the brain's capacity for consciousness. Progress in Brain Research 2009;177:201-214.
Virtanen J, Ruohonen J, Naatanen R, Ilmoniemi RJ. Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation. Medical & Biological Engineering & Computing 1999;37:322-326.
Majerus S, Bruno MA, Schnakers C, Giacino JT, Laureys S. The problem of aphasia in the assessment of consciousness in braindamaged patients. Progress in Brain Research 2009;177:49-61.
Boly M, Coleman MR, Davis MH, Hampshire A, Bor D, Moonen G, Maquet PA, Pickard JD, Laureys S, Owen AM. When thoughts become action: An fMRI paradigm to study volitional brain activity in non-communicative brain injured patients. NeuroImage 2007;36:979-992.
Owen AM, Coleman MR, Boly M, Davis MH, Laureys S, Pickard JD. Using functional magnetic resonance imaging to detect covert awareness in the vegetative state. Archives of Neurology 2007;64:1098-1102.
Monti MM, Vanhaudenhuyse A, Coleman MR, Boly M, Pickard JD, Tshibanda L, Owen AM, Laureys S. Willful modulation of brain activity in disorders of consciousness. The New England Journal of Medicine 2010;362:579-589.
Bardin JC, Fins JJ, Katz DI, Hersh J, Heier LA, Tabelow K, Dyke JP, Ballon DJ, Schiff ND, Voss HU. Dissociations between behavioural and functional magnetic resonance imaging-based evaluations of cognitive function after brain injury. Brain 2011; 134:769-782.
Vogel D, Markl A, Yu T, Kotchoubey B, Lang S, Muller F. Can mental imagery functional magnetic resonance imaging predict recovery in patients with disorders of consciousness? Archives of Physical Medicine and Rehabilitation 2013;10:1891-1898.
Boly M, Faymonville ME, Peigneux P, Lambermont B, Damas P, Del Fiore G, Degueldre C, Franck G, Luxen A, Lamy M, et al. Auditory processing in severely brain injured patients: Differences between the minimally conscious state and the persistent vegetative state. Archives of Neurology 2004;61:233-238.
Schiff ND, Ribary U, Moreno DR, Beattie B, Kronberg E, Blasberg R, Giacino J, McCagg C, Fins JJ, Llinas R, et al. Residual cerebral activity and behavioural fragments can remain in the persistently vegetative brain. Brain 2002;125:1210-1234.
Laureys S, Faymonville ME, Peigneux P, Damas P, Lambermont B, Del Fiore G, Degueldre C, Aerts J, Luxen A, Franck G, et al. Cortical processing of noxious somatosensory stimuli in the persistent vegetative state. NeuroImage 2002;17:732-741.
Vanhaudenhuyse A, Noirhomme Q, Tshibanda LJ, Bruno MA, Boveroux P, Schnakers C, Soddu A, Perlbarg V, Ledoux D, Brichant JF, et al. Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain 2010;133:161-171.
Demertzi A, Gomez F, Crone JS, Vanhaudenhuyse A, Tshibanda L, Noirhomme Q, Thonnard M, Charland-Verville V, Kirsch M, Laureys S, et al. Multiple fMRI system-level baseline connectivity is disrupted in patients with consciousness alterations. Cortex; A Journal Devoted to the Study of the Nervous System and Behavior 2014;52:35-46.
Jox RJ, Bernat JL, Laureys S, Racine E. Disorders of consciousness: Responding to requests for novel diagnostic and therapeutic interventions. Lancet Neurology 2012;11:732-738.
Dehaene S, Changeux JP. Experimental and theoretical approaches to conscious processing. Neuron 2011;70:200-227.
Cruse D, Chennu S, Chatelle C, Bekinschtein TA, Fernandez-Espejo D, Pickard JD, Laureys S, Owen AM. Bedside detection of awareness in the vegetative state: A cohort study. Lancet 2011;378:2088-2094.
Schnakers C, Perrin F, Schabus M, Hustinx R, Majerus S, Moonen G, Boly M, Vanhaudenhuyse A, Bruno MA, Laureys S. Detecting consciousness in a total locked-in syndrome: An active event-related paradigm. Neurocase 2009;15:271-277.
Naci L, Monti MM, Cruse D, Kubler A, Sorger B, Goebel R, Kotchoubey B, Owen AM. Brain-computer interfaces for communication with nonresponsive patients. Annals of Neurology 2012; 72:312-323.
Myles PS, Leslie K, McNeil J, Forbes A, Chan MT. Bispectral index monitoring to prevent awareness during anaesthesia: The B-Aware randomised controlled trial. Lancet 2004;363:1757-1763.
Schnakers C, Ledoux D, Majerus S, Damas P, Damas F, Lambermont B, Lamy M, Boly M, Vanhaudenhuyse A, Moonen G, et al. Diagnostic and prognostic use of bispectral index in coma, vegetative state and related disorders. Brain Injury 2008;22:926-931.
Landsness E, Bruno MA, Noirhomme Q, Riedner B, Gosseries O, Schnakers C, Massimini M, Laureys S, Tononi G, Boly M. Electrophysiological correlates of behavioural changes in vigilance in vegetative state and minimally conscious state. Brain 2011;134: 2222-2232.
Gosseries O, Schnakers C, Ledoux D, Vanhaudenhuyse A, Bruno MA, Demertzi A, Noirhomme Q, Lehembre R, Damas P, Goldman S, et al. Automated EEG entropy measurements in coma, vegetative state/unresponsive wakefulness syndrome and minimally conscious state. Functional Neurology 2011;26:25-30.
Tononi G, Sporns O, Edelman GM. A measure for brain complexity: Relating functional segregation and integration in the nervous system. Proceedings of the National Academy of Sciences of the United States of America 1994;91:5033-5037.
Seth AK. Causal connectivity of evolved neural networks during behavior. Network 2005;16:35-54.
Granger CW. Investigating causal relations by Econometric Models and Cross-spectral Methods. Econometrica 1969;37:424-238.
Balduzzi D. Estimating integrated information with TMS pulses during wakefulness, sleep, and under anesthesia. Conference proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society. Conference 2011:4717-4720.
Roth BJ, Saypol JM, Hallett M, Cohen LG. A theoretical calculation of the electric field induced in the cortex during magnetic stimulation. Electroencephalography and Clinical Neurophysiology 1991;81:47-56.
Ruohonen J, Ilmoniemi RJ. Modeling of the stimulating field generation in TMS. Electroencephalography and Clinical Neurophysiology Supplement 1999;51:30-40.
Maccabee PJ, Amassian VE, Eberle LP, Cracco RQ. Magnetic coil stimulation of straight and bent amphibian and mammalian peripheral nerve in vitro: Locus of excitation. The Journal of Physiology 1993;460:201-219.
Friston KJ. Functional and effective connectivity: A review. Brain Connectivity 2011;1:13-36.
Massimini M, Ferrarelli F, Huber R, Esser SK, Singh H, Tononi G. Breakdown of cortical effective connectivity during sleep. Science 2005;309:2228-2232.
Ferrarelli F, Massimini M, Sarasso S, Casali A, Riedner BA, Angelini G, Tononi G, Pearce RA. Breakdown in cortical effective connectivity during midazolam-induced loss of consciousness. Proceedings of the National Academy of Sciences of the United States of America 2010;107:2681-2686.
Bonato C, Miniussi C, Rossini PM. Transcranial magnetic stimulation and cortical evoked potentials: A TMS/EEG co-registration study. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology 2006;117: 1699-1707.
Esser SK, Huber R, Massimini M, Peterson MJ, Ferrarelli F, Tononi G. A direct demonstration of cortical LTP in humans: A combined TMS/EEG study. Brain Research Bulletin 2006;69: 86-94.
Mutanen T, Maki H, Ilmoniemi RJ. The effect of stimulus parameters on TMS-EEG muscle artifacts. Brain Stimulation 2013;6:371-376.
Rosanova M, Gosseries O, Casarotto S, Boly M, Casali AG, Bruno MA, Mariotti M, Boveroux P, Tononi G, Laureys S, et al. Recovery of cortical effective connectivity and recovery of consciousness in vegetative patients. Brain 2012;135:1308-1320.
Casarotto S, Romero Lauro LJ, Bellina V, Casali AG, Rosanova M, Pigorini A, Defendi S, Mariotti M, Massimini M. EEG responses to TMS are sensitive to changes in the perturbation parameters and repeatable over time. PLoS One 2010;5:e10281.
Casali AG, Casarotto S, Rosanova M, Mariotti M, Massimini M. General indices to characterize the electrical response of the cerebral cortex to TMS. NeuroImage 2010;49:1459-1468.
Johnson JS, Kundu B, Casali AG, Postle BR. Task-dependent changes in cortical excitability and effective connectivity: A combined TMS-EEG study. Journal of Neurophysiology 2012; 107:2383-2392.
Kundu B, Sutterer DW, Emrich SM, Postle BR. Strengthened effective connectivity underlies transfer of working memory training to tests of short-term memory and attention. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2013;33:8705-8715.
Akaishi R, Morishima Y, Rajeswaren VP, Aoki S, Sakai K. Stimulation of the frontal eye field reveals persistent effective connectivity after controlled behavior. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2010;30:4295-4305.
Morishima Y, Akaishi R, Yamada Y, Okuda J, Toma K, Sakai K. Task-specific signal transmission from prefrontal cortex in visual selective attention. Nature Neuroscience 2009;12:85-91.
Nikulin VV, Kicic D, Kahkonen S, Ilmoniemi RJ. Modulation of electroencephalographic responses to transcranial magnetic stimulation: Evidence for changes in cortical excitability related to movement. The European Journal of Neuroscience 2003;18: 1206-1212.
Massimini M, Ferrarelli F, Murphy M, Huber R, Riedner B, Casarotto S, Tononi G. Cortical reactivity and effective connectivity during REM sleep in humans. Cognitive Neuroscience 2010;1: 176-183.
Rosanova M, Casali A, Bellina V, Resta F, Mariotti M, Massimini M. Natural frequencies of human corticothalamic circuits. The Journal of Neuroscience: The official Journal of the Society for Neuroscience 2009;29:7679-7685.
Huber R, Maki H, Rosanova M, Casarotto S, Canali P, Casali AG, Tononi G, Massimini M. Human cortical excitability increases with time awake. Cerebral Cortex 2013;23:332-338.
Mattavelli G, Rosanova M, Casali AG, Papagno C, Romero Lauro LJ. Top-down interference and cortical responsiveness in face processing: A TMS-EEG study. NeuroImage 2013;76: 24-32.
Kahkonen S, Wilenius J, Nikulin VV, Ollikainen M, Ilmoniemi RJ. Alcohol reduces prefrontal cortical excitability in humans: A combined TMS and EEG study. Neuropsychopharmacology 2003;28:747-754.
Hobson JA, Pace-Schott EF, Stickgold R. Dreaming and the brain: Toward a cognitive neuroscience of conscious states. Behav Brain Sci 2000;23:793-842.
Massimini M, Ferrarelli F, Esser SK, Riedner BA, Huber R, Murphy M, Peterson MJ, Tononi G. Triggering sleep slow waves by transcranial magnetic stimulation. Proceedings of the National Academy of Sciences of the United States of America 2007;104: 8496-8501.
Tanelian DL, Kosek P, Mody I, MacIver MB. The role of the GABAA receptor/chloride channel complex in anesthesia. Anesthesiology 1993;78:757-776.
Ragazzoni A, Pirulli C, Veniero D, Feurra M, Cincotta M, Giovannelli F, Chiaramonti R, Lino M, Rossi S, Miniussi C. Vegetative versus Minimally Conscious States: A study using TMS-EEG, sensory and event-related potentials. PLoS One 2013;8: e57069.
Tallus J, Lioumis P, Hamalainen H, Kahkonen S, Tenovuo O. TMS-EEG responses in recovered and symptomatic mild traumatic brain injury. Journal of Neurotrauma 2013;30:1270-1277.
Lapitskaya N, Gosseries O, De Pasqua V, Pedersen AR, Nielsen JF, de Noordhout AM, Laureys S. Abnormal corticospinal excitability in patients with disorders of consciousness. Brain Stimulation 2013; 6:590-597.
Ferrarelli F, Massimini M, Peterson MJ, Riedner BA, Lazar M, Murphy MJ, Huber R, Rosanova M, Alexander AL, Kalin N, et al. Reduced evoked gamma oscillations in the frontal cortex in schizophrenia patients: A TMS/EEG study. The American Journal of Psychiatry 2008;165:996-1005.
Frantseva M, Cui J, Farzan F, Chinta LV, Perez Velazquez JL, Daskalakis ZJ. Disrupted cortical conductivity in schizophrenia: TMS-EEG Study. Cerebral Cortex 2014;24:211-221.
Casarotto S, Maatta S, Herukka SK, Pigorini A, Napolitani M, Gosseries O, Niskanen E, Kononen M, Mervaala E, Rosanova M, et al. Transcranial magnetic stimulation-evoked EEG/cortical potentials in physiological and pathological aging. Neuroreport 2011;22:592-597.
Wassermann EM. Risk and safety of repetitive transcranial magnetic stimulation: Report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. Electroencephalography and Clinical Neurophysiology 1998;108:1-16.
Baars BJ. The conscious access hypothesis: Origins and recent evidence. Trends in Cognitive Sciences 2002;6:47-52.
Dehaene S, Naccache L. Towards a cognitive neuroscience of consciousness: Basic evidence and a workspace framework. Cognition 2001;79:1-37.
Tononi G. An information integration theory of consciousness. BMC Neuroscience 2004;5:42.
Mashour GA. Consciousness unbound: Toward a paradigm of general anesthesia. Anesthesiology 2004;100:428-433.
Ortinski P, Meador KJ. Neuronal mechanisms of conscious awareness. Archives of Neurology 2004;61:1017-1020.
Amting JM, Greening SG, Mitchell DG. Multiple mechanisms of consciousness: The neural correlates of emotional awareness. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2010;30:10039-10047.
McPherson A, Rojas L, Bauerschmidt A, Ezeani CC, Yang L, Motelow JE, Farooque P, Detyniecki K, Giacino JT, Blumenfeld H. Testing for minimal consciousness in complex partial and generalized tonic-clonic seizures. Epilepsia 2012;53: e180-e183.
Casali AJ, Gosseries O, Rosanova M, Boly M, Sarasso S, Casali KR, Casarotto S, Bruno M-A, Laureys S, Tononi G, Massimini M. A theoretically based index of consciousness independent of sensory processing and behavior. Science Translational Medicine 2013;5:198-105. doi: 10.1126/scitranslmed.3006294.
Giacino JT, Whyte J, Bagiella E, Kalmar K, Childs N, Khademi A, Eifert B, Long D, Katz DI, Cho S, et al. Placebo-controlled trial of amantadine for severe traumatic brain injury. The New England Journal of Medicine 2012;366:819-826.
Clauss R, Nel W. Drug induced arousal from the permanent vegetative state. NeuroRehabilitation 2006;21:23-28.
Fridman EA, Krimchansky BZ, Bonetto M, Galperin T, Gamzu ER, Leiguarda RC, Zafonte R. Continuous subcutaneous apomorphine for severe disorders of consciousness after traumatic brain injury. Brain Injury 2010;24:636-641.
Peters JC, Reithler J, Schuhmann T, de Graaf T, Uludag K, Goebel R, Sack AT. On the feasibility of concurrent human TMS-EEG-fMRI measurements. Journal of Neurophysiology 2013; 109:1214-1227.
Shimojima Y, Morita H, Nishikawa N, Kodaira M, Hashimoto T, Ikeda S. The safety of transcranial magnetic stimulation with deep brain stimulation instruments. Parkinsonism & Related Disorders 2010;16:127-131.
Sarasso S, Rosanova M, Casali AG, Casarotto S, Fecchio M, Boly M, Gosseries O, Tononi G, Laureys S, Massimini M. Quantifying cortical EEG responses to TMS in (un)consciousness. Clinical EEG and Neuroscience 2014;45:40-49. doi: 10.1177/1550059413513723.
