Prognostic Use of Cognitive Event-Related Potentials in Acute Consciousness Impairment

  • Chapter
  • First Online:
Clinical Neurophysiology in Disorders of Consciousness

Abstract

Electroencephalography (EEG) provides a powerful tool for evaluating the extent of intact cognitive functions in comatose patients at the bedside, mostly by recording responses to sensory stimuli, exemplified by the so-called event-related potentials (ERPs). Different ERP paradigms are informative of various levels of cognitive functions, ranging from basic auditory processing and auditory discrimination (i.e., mismatch negativity (MMN)) to novelty detection and detection of complex sound sequences. Among them, the MMN paradigm has proven especially useful, as the presence of an MMN response has been repeatedly associated with a favorable clinical prognosis. The high predictive power of MMN is basically driven by the absence of such a response in patients who fail to regain consciousness, mainly assessed several weeks or months after coma onset. However, the use of this paradigm in clinical routine has been limited so far, possibly due to the difficulty of assessing the presence of an MMN at the level of single patients. Multivariate EEG decoding methods provide a powerful tool for quantifying the degree of auditory discrimination, at the single-patient level with minimal a priori inclusion criteria, with very promising results in terms of prognostication of awakening. Moreover, recent evidence in patients in acute postanoxic coma treated with therapeutic hypothermia shows that auditory discrimination might still be intact during the first days of coma, irrespective of patients’ outcome. Here, we propose a general framework for assessing the degree of auditory discrimination over time, as a process that degenerates in non-survivors and that improves in patients who eventually awake.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
EUR 29.95
Price includes VAT (Thailand)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
EUR 67.40
Price includes VAT (Thailand)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
EUR 79.99
Price excludes VAT (Thailand)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Amantini A, Carrai R, Fossi S, Pinto F, Grippo A (2011) The role of early electroclinical assessment in improving the evaluation of patients with disorders of consciousness. Funct Neurol 26:7–14

    PubMed Central  PubMed  Google Scholar 

  • Bekinschtein TA, Dehaene S, Rohaut B, Tadel F, Cohen L, Naccache L (2009) Neural signature of the conscious processing of auditory regularities. Proc Natl Acad Sci U S A 106:1672–1677

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bernard SA, Gray TW, Buist MD, Jones BM, Silvester W, Gutteridge G, Smith K (2002) Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N Engl J Med 346:557–563

    Article  PubMed  Google Scholar 

  • Blankertz B, Lemm S, Treder M, Haufe S, Muller KR (2011) Single-trial analysis and classification of ERP components – a tutorial. Neuroimage 56:814–825

    Article  PubMed  Google Scholar 

  • Boly M, Garrido MI, Gosseries O, Bruno MA, Boveroux P, Schnakers C, Massimini M, Litvak V, Laureys S, Friston K (2011) Preserved feedforward but impaired top-down processes in the vegetative state. Science 332:858–862

    Article  CAS  PubMed  Google Scholar 

  • Boly M, Seth AK, Wilke M, Ingmundson P, Baars B, Laureys S, Edelman DB, Tsuchiya N (2013) Consciousness in humans and non-human animals: recent advances and future directions. Front Psychol 4:625

    Article  PubMed Central  PubMed  Google Scholar 

  • Bourdaud N, Chavarriaga R, Galan F, Millan Jdel R (2008) Characterizing the EEG correlates of exploratory behavior. IEEE Trans Neural Syst Rehabil Eng 16:549–556

    Article  PubMed  Google Scholar 

  • Bouwes A, Binnekade JM, Zandstra DF, Koelman JH, van Schaik IN, Hijdra A, Horn J (2009) Somatosensory evoked potentials during mild hypothermia after cardiopulmonary resuscitation. Neurology 73:1457–1461

    Article  CAS  PubMed  Google Scholar 

  • Chennu S, Bekinschtein TA (2012) Arousal modulates auditory attention and awareness: insights from sleep, sedation, and disorders of consciousness. Front Psychol 3:65

    Article  PubMed Central  PubMed  Google Scholar 

  • Choi HA, Badjatia N, Mayer SA (2012) Hypothermia for acute brain injury – mechanisms and practical aspects. Nat Rev Neurol 8:214–222

    CAS  PubMed  Google Scholar 

  • Cruse D, Chennu S, Chatelle C, Bekinschtein TA, Fernandez-Espejo D, Pickard JD, Laureys S, Owen AM (2011) Bedside detection of awareness in the vegetative state: a cohort study. Lancet 378:2088–2094

    Article  PubMed  Google Scholar 

  • Daltrozzo J, Wioland N, Mutschler V, Lutun P, Calon B, Meyer A, Pottecher T, Lang S, Jaeger A, Kotchoubey B (2009) Cortical information processing in coma. Cogn Behav Neurol 22:53–62

    Article  PubMed  Google Scholar 

  • De Lucia M, Constantinescu I, Sterpenich V, Pourtois G, Seeck M, Schwartz S (2011) Decoding sequence learning from single-trial intracranial EEG in humans. PLoS One 6:e28630

    Article  PubMed Central  PubMed  Google Scholar 

  • De Lucia M, Tzovara A, Bernasconi F, Spierer L, Murray MM (2012) Auditory perceptual decision-making based on semantic categorization of environmental sounds. Neuroimage 60:1704–1715

    Article  PubMed  Google Scholar 

  • De Vos M, Thorne JD, Yovel G, Debener S (2012) Let's face it, from trial to trial: comparing procedures for N170 single-trial estimation. Neuroimage 63:1196–1202

    Article  PubMed  Google Scholar 

  • Faugeras F, Rohaut B, Weiss N, Bekinschtein T, Galanaud D, Puybasset L, Bolgert F, Sergent C, Cohen L, Dehaene S, Naccache L (2012) Event related potentials elicited by violations of auditory regularities in patients with impaired consciousness. Neuropsychologia 50:403–418

    Article  PubMed  Google Scholar 

  • Fischer C, Morlet D, Bouchet P, Luaute J, Jourdan C, Salord F (1999) Mismatch negativity and late auditory evoked potentials in comatose patients. Clin Neurophysiol 110:1601–1610

    Article  CAS  PubMed  Google Scholar 

  • Fischer C, Luaute J, Adeleine P, Morlet D (2004) Predictive value of sensory and cognitive evoked potentials for awakening from coma. Neurology 63:669–673

    Article  PubMed  Google Scholar 

  • Fischer C, Dailler F, Morlet D (2008) Novelty P3 elicited by the subject’s own name in comatose patients. Clin Neurophysiol 119:2224–2230

    Article  PubMed  Google Scholar 

  • Fischer C, Luaute J, Morlet D (2010) Event-related potentials (MMN and novelty P3) in permanent vegetative or minimally conscious states. Clin Neurophysiol 121:1032–1042

    Article  PubMed  Google Scholar 

  • Friedman D, Cycowicz YM, Gaeta H (2001) The novelty P3: an event-related brain potential (ERP) sign of the brain’s evaluation of novelty. Neurosci Biobehav Rev 25:355–373

    Article  CAS  PubMed  Google Scholar 

  • Garrido MI, Kilner JM, Stephan KE, Friston KJ (2009) The mismatch negativity: a review of underlying mechanisms. Clin Neurophysiol 120:453–463

    Article  PubMed Central  PubMed  Google Scholar 

  • Gendo A, Kramer L, Hafner M, Funk GC, Zauner C, Sterz F, Holzer M, Bauer E, Madl C (2001) Time-dependency of sensory evoked potentials in comatose cardiac arrest survivors. Intensive Care Med 27:1305–1311

    Article  CAS  PubMed  Google Scholar 

  • Hausfeld L, De Martino F, Bonte M, Formisano E (2012) Pattern analysis of EEG responses to speech and voice: influence of feature grou**. Neuroimage 59:3641–3651

    Article  PubMed  Google Scholar 

  • Heine L, Soddu A, Gomez F, Vanhaudenhuyse A, Tshibanda L, Thonnard M, Charland-Verville V, Kirsch M, Laureys S, Demertzi A (2012) Resting state networks and consciousness: alterations of multiple resting state network connectivity in physiological, pharmacological, and pathological consciousness States. Front Psychol 3:295

    Article  PubMed Central  PubMed  Google Scholar 

  • Hillyard SA, Hink RF, Schwent VL, Picton TW (1973) Electrical signs of selective attention in the human brain. Science 182:177–180

    Article  CAS  PubMed  Google Scholar 

  • Holeckova I, Fischer C, Morlet D, Delpuech C, Costes N, Mauguiere F (2008) Subject’s own name as a novel in a MMN design: a combined ERP and PET study. Brain Res 1189:152–165

    Article  CAS  PubMed  Google Scholar 

  • Kane NM, Curry SH, Butler SR, Cummins BH (1993) Electrophysiological indicator of awakening from coma. Lancet 341:688

    Article  CAS  PubMed  Google Scholar 

  • King JR, Faugeras F, Gramfort A, Schurger A, El Karoui I, Sitt JD, Rohaut B, Wacongne C, Labyt E, Bekinschtein T, Cohen L, Naccache L, Dehaene S (2013) Single-trial decoding of auditory novelty responses facilitates the detection of residual consciousness. Neuroimage 83:726–738

    Article  CAS  PubMed  Google Scholar 

  • Koelsch S, Heinke W, Sammler D, Olthoff D (2006) Auditory processing during deep propofol sedation and recovery from unconsciousness. Clin Neurophysiol 117:1746–1759

    Article  CAS  PubMed  Google Scholar 

  • Kotchoubey B, Lang S, Mezger G, Schmalohr D, Schneck M, Semmler A, Bostanov V, Birbaumer N (2005) Information processing in severe disorders of consciousness: vegetative state and minimally conscious state. Clin Neurophysiol 116:2441–2453

    Article  CAS  PubMed  Google Scholar 

  • Kriegeskorte N, Simmons WK, Bellgowan PS, Baker CI (2009) Circular analysis in systems neuroscience: the dangers of double dip**. Nat Neurosci 12:535–540

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kutas M, Hillyard SA (1980) Reading senseless sentences: brain potentials reflect semantic incongruity. Science 207:203–205

    Article  CAS  PubMed  Google Scholar 

  • Laureys S, Owen AM, Schiff ND (2004) Brain function in coma, vegetative state, and related disorders. Lancet Neurol 3:537–546

    Article  PubMed  Google Scholar 

  • Lechinger J, Bothe K, Pichler G, Michitsch G, Donis J, Klimesch W, Schabus M (2013) CRS-R score in disorders of consciousness is strongly related to spectral EEG at rest. J Neurol 260:2348–2356

    Article  PubMed  Google Scholar 

  • Lemm S, Blankertz B, Dickhaus T, Muller KR (2011) Introduction to machine learning for brain imaging. Neuroimage 56:387–399

    Article  PubMed  Google Scholar 

  • Lew HL, Poole JH, Castaneda A, Salerno RM, Gray M (2006) Prognostic value of evoked and event-related potentials in moderate to severe brain injury. J Head Trauma Rehabil 21:350–360

    Article  PubMed  Google Scholar 

  • Luaute J, Fischer C, Adeleine P, Morlet D, Tell L, Boisson D (2005) Late auditory and event-related potentials can be useful to predict good functional outcome after coma. Arch Phys Med Rehabil 86:917–923

    Article  PubMed  Google Scholar 

  • Madhok J, Wu D, **ong W, Geocadin RG, Jia X (2012) Hypothermia amplifies somatosensory-evoked potentials in uninjured rats. J Neurosurg Anesthesiol 24:197–202

    Article  PubMed Central  PubMed  Google Scholar 

  • Murphy B, Poesio M, Bovolo F, Bruzzone L, Dalponte M, Lakany H (2011) EEG decoding of semantic category reveals distributed representations for single concepts. Brain Lang 117:12–22

    Article  PubMed  Google Scholar 

  • Murray MM, Brunet D, Michel CM (2008) Topographic ERP analyses: a step-by-step tutorial review. Brain Topogr 20:249–264

    Article  PubMed  Google Scholar 

  • Naatanen R, Picton T (1987) The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. Psychophysiology 24:375–425

    Article  CAS  PubMed  Google Scholar 

  • Naatanen R, Gaillard AW, Mantysalo S (1978) Early selective-attention effect on evoked potential reinterpreted. Acta Psychol (Amst) 42:313–329

    Article  CAS  Google Scholar 

  • Naccache L, Puybasset L, Gaillard R, Serve E, Willer JC (2005) Auditory mismatch negativity is a good predictor of awakening in comatose patients: a fast and reliable procedure. Clin Neurophysiol 116:988–989

    Article  PubMed  Google Scholar 

  • Neumann N, Kotchoubey B (2004) Assessment of cognitive functions in severely paralysed and severely brain-damaged patients: neuropsychological and electrophysiological methods. Brain Res Brain Res Protoc 14:25–36

    Article  PubMed  Google Scholar 

  • Oddo M, Schaller MD, Feihl F, Ribordy V, Liaudet L (2006) From evidence to clinical practice: effective implementation of therapeutic hypothermia to improve patient outcome after cardiac arrest. Crit Care Med 34:1865–1873

    PubMed  Google Scholar 

  • Owen AM, Coleman MR, Boly M, Davis MH, Laureys S, Pickard JD (2006) Detecting awareness in the vegetative state. Science 313:1402

    Article  CAS  PubMed  Google Scholar 

  • Pereira F, Mitchell T, Botvinick M (2009) Machine learning classifiers and fMRI: a tutorial overview. Neuroimage 45:S199–S209

    Article  PubMed Central  PubMed  Google Scholar 

  • Perrin F, Garcia-Larrea L (2003) Modulation of the N400 potential during auditory phonological/semantic interaction. Brain Res Cogn Brain Res 17:36–47

    Article  PubMed  Google Scholar 

  • Philiastides MG, Sajda P (2006) Temporal characterization of the neural correlates of perceptual decision making in the human brain. Cereb Cortex 16:509–518

    Article  PubMed  Google Scholar 

  • Pratt H, Berlad I, Lavie P (1999) ‘Oddball’ event-related potentials and information processing during REM and non-REM sleep. Clin Neurophysiol 110:53–61

    Article  CAS  PubMed  Google Scholar 

  • Robinson LR, Micklesen PJ, Tirschwell DL, Lew HL (2003) Predictive value of somatosensory evoked potentials for awakening from coma. Crit Care Med 31:960–967

    Article  PubMed  Google Scholar 

  • Rossetti AO, Oddo M, Logroscino G, Kaplan PW (2010) Prognostication after cardiac arrest and hypothermia: a prospective study. Ann Neurol 67:301–307

    PubMed  Google Scholar 

  • Ruby P, Caclin A, Boulet S, Delpuech C, Morlet D (2008) Odd sound processing in the slee** brain. J Cogn Neurosci 20:296–311

    Article  PubMed  Google Scholar 

  • Schoenle PW, Witzke W (2004) How vegetative is the vegetative state? Preserved semantic processing in VS patients–evidence from N 400 event-related potentials. NeuroRehabilitation 19:329–334

    PubMed  Google Scholar 

  • Sculthorpe LD, Ouellet DR, Campbell KB (2009) MMN elicitation during natural sleep to violations of an auditory pattern. Brain Res 1290:52–62

    Article  CAS  PubMed  Google Scholar 

  • Signorino M, D’Acunto S, Angeleri F, Pietropaoli P (1995) Eliciting P300 in comatose patients. Lancet 345:255–256

    Article  CAS  PubMed  Google Scholar 

  • Simanova I, van Gerven M, Oostenveld R, Hagoort P (2010) Identifying object categories from event-related EEG: toward decoding of conceptual representations. PLoS One 5:e14465

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Staeren N, Renvall H, De Martino F, Goebel R, Formisano E (2009) Sound categories are represented as distributed patterns in the human auditory cortex. Curr Biol 19:498–502

    Article  CAS  PubMed  Google Scholar 

  • Sutton S, Braren M, Zubin J, John ER (1965) Evoked-potential correlates of stimulus uncertainty. Science 150:1187–1188

    Article  CAS  PubMed  Google Scholar 

  • Tzovara A, Murray MM, Michel CM, De Lucia M (2012a) A tutorial review of electrical neuroimaging from group-average to single-trial event-related potentials. Dev Neuropsychol 37:518–544

    Article  PubMed  Google Scholar 

  • Tzovara A, Murray MM, Plomp G, Herzog MH, Michel CM, De Lucia M (2012b) Decoding stimulus-related information from single-trial EEG responses based on voltage topographies. Pattern Recognition 45:2109–2122

    Article  Google Scholar 

  • Tzovara A, Rossetti AO, Spierer L, Grivel J, Murray MM, Oddo M, De Lucia M (2013) Progression of auditory discrimination based on neural decoding predicts awakening from coma. Brain 136:81–89

    Article  PubMed  Google Scholar 

  • Weil RS, Rees G (2010) Decoding the neural correlates of consciousness. Curr Opin Neurol 23:649–655

    Article  PubMed  Google Scholar 

  • Wijnen VJ, van Boxtel GJ, Eilander HJ, de Gelder B (2007) Mismatch negativity predicts recovery from the vegetative state. Clin Neurophysiol 118:597–605

    Article  CAS  PubMed  Google Scholar 

  • Wu D, **ong W, Jia X, Geocadin RG, Thakor NV (2012) Short- and long-latency somatosensory neuronal responses reveal selective brain injury and effect of hypothermia in global hypoxic ischemia. J Neurophysiol 107:1164–1171

    Article  PubMed Central  PubMed  Google Scholar 

  • Zandbergen EG, de Haan RJ, Stoutenbeek CP, Koelman JH, Hijdra A (1998) Systematic review of early prediction of poor outcome in anoxic-ischaemic coma. Lancet 352:1808–1812

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marzia De Lucia PhD .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer-Verlag Wien

About this chapter

Cite this chapter

De Lucia, M., Tzovara, A. (2015). Prognostic Use of Cognitive Event-Related Potentials in Acute Consciousness Impairment. In: Rossetti, A., Laureys, S. (eds) Clinical Neurophysiology in Disorders of Consciousness. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1634-0_7

Download citation

  • DOI: https://doi.org/10.1007/978-3-7091-1634-0_7

  • Published:

  • Publisher Name: Springer, Vienna

  • Print ISBN: 978-3-7091-1633-3

  • Online ISBN: 978-3-7091-1634-0

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Navigation