Skip to main content

Stability of auditory event-related potentials in coma research

An Erratum to this article was published on 17 April 2015

Abstract

Patients with unresponsive wakefulness syndrome (UWS) or in minimally conscious state (MCS) after brain injury show significant fluctuations in their behavioural abilities over time. As the importance of event-related potentials (ERPs) in the detection of traces of consciousness increases, we investigated the retest reliability of ERPs with repeated tests at four different time points. Twelve healthy controls and 12 inpatients (8 UWS, 4 MCS; 6 traumatic, 6 non-traumatic) were tested twice a day (morning, afternoon) for 2 days with an auditory oddball task. ERPs were recorded with a 256-channel-EEG system, and correlated with behavioural test scores in the Coma Recovery Scale-revised (CRS-R). The number of identifiable P300 responses varied between zero and four in both groups. Reliabilities varied between Krippendorff’s α = 0.43 for within-day comparison, and α = 0.25 for between-day comparison in the patient group. Retest reliability was strong for the CRS-R scores for all comparisons (α = 0.83–0.95). The stability of auditory information processing in patients with disorders of consciousness is the basis for other, even more demanding tasks and cognitive potentials. The relatively low ERP-retest reliability suggests that it is necessary to perform repeated tests, especially when probing for consciousness with ERPs. A single negative ERP test result may be mistaken for proof that a UWS patient truly is unresponsive.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Guldenmund P, Stender J, Heine L, Laureys S (2012) Mindsight: diagnostics in disorders of consciousness. Crit Care Res Pract 2012:624724. doi:10.1155/2012/624724

    PubMed Central  CAS  PubMed  Google Scholar 

  2. Giacino JT, Fins JJ, Laureys S, Schiff ND (2014) Disorders of consciousness after acquired brain injury: the state of the science. Nat Rev Neurol 10(2):99–114. doi:10.1038/nrneurol.2013.279

    Article  PubMed  Google Scholar 

  3. 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(3):349–353

    Article  PubMed  Google Scholar 

  4. Andrews K, Murphy L, Munday R, Littlewood C (1996) Misdiagnosis of the vegetative state: retrospective study in a rehabilitation unit. Br Med J 313:13–16

    CAS  Article  Google Scholar 

  5. Giacino JT, Kalmar K, Whyte J (2004) The JFK coma recovery scale-revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil 85(12):2020–2029

    Article  PubMed  Google Scholar 

  6. Schnakers C, Giacino J, Kalmar K, Piret S, Lopez E, Boly M, Malone R, Laureys S (2006) Does the FOUR score correctly diagnose the vegetative and minimally conscious states. Ann Neurol 60(6):744–745

    Article  PubMed  Google Scholar 

  7. Schnakers C, Majerus S, Giacino J, Vanhaudenhuyse A, Bruno MA, Boly M, Moonen G, Damas P, Lambermont B, Lamy M, Damas F, Ventura M, Laureys S (2008) A French validation study of the coma recovery scale-revised (CRSR). Brain Inj 22(10):786–792

    Article  PubMed  Google Scholar 

  8. Vanhaudenhuyse A, Noirhomme Q, Tshibanda LJ, Bruno MA, Boveroux P, Schnakers C, Soddu A, Perlbarg V, Ledoux D, Brichant JF, Moonen G, Maquet P, Greicius MD, Laureys S, Boly M (2010) Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain 133(Pt 1):161–171. doi:10.1093/brain/awp313

    PubMed Central  Article  PubMed  Google Scholar 

  9. Qin P, Di H, Liu Y, Yu S, Gong Q, Duncan N, Weng X, Laureys S, Northoff G (2010) Anterior cingulate activity and the self in disorders of consciousness. Hum Brain Mapp 31(12):1993–2002. doi:10.1002/hbm.20989

    Article  PubMed  Google Scholar 

  10. Bekinschtein TA, Manes FF, Villarreal M, Owen AM, Della-Maggiore V (2011) Functional imaging reveals movement preparatory activity in the vegetative state. Front Hum Neurosci 5:5. doi:10.3389/fnhum.2011.00005

    PubMed Central  Article  PubMed  Google Scholar 

  11. Fischer C, Luaute J, Morlet D (2010) Event-related potentials (MMN and novelty P3) in permanent vegetative or minimally conscious states. Clin Neurophysiol 121(7):1032–1042. doi:10.1016/j.clinph.2010.02.005

    Article  PubMed  Google Scholar 

  12. Donchin E, Karis D, Bashore TR, Coles MGH, Gratton G (1986) Cognitivepsychophysiology and human information processing. In: Coles MGH, Donchin E, Porges SW (eds) Psychophysiology: systems, processes, and applications. Guildford, New York, pp 244–267

    Google Scholar 

  13. Luauté 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 

  14. Cavinato M, Freo U, Ori C, Zorzi M, Tonin P, Piccione F, Merico A (2009) Post-acute P300 predicts recovery of consciousness from traumatic vegetative state. Brain 23:973–980

    Google Scholar 

  15. Risetti M, Formisano R, Toppi J, Quitadamo LR, Bianchi L, Astolfi L, Cincotti F, Mattia D (2013) On ERPs detection in disorders of consciousness rehabilitation. Front Hum Neurosci 7:775

    PubMed Central  Article  PubMed  Google Scholar 

  16. Lulé D, Noirhomme Q, Kleih SC, Chatelle C, Halder S, Demertzi A, Bruno MA, Gosseries O, Vanhaudenhuyse A, Schnakers C, Thonnard M, Soddu A, Kübler A, Laureys S (2013) Probing command following in patients with disorders of consciousness using a brain-computer interface. Clin Neurophysiol 124(1):101–106

    Article  PubMed  Google Scholar 

  17. Cavinato M, Volpato C, Silvoni S, Sacchetto M, Merico A, Piccione F (2011) Event-related brain potential modulation in patients with severe brain damage. Clin Neurophysiol 122(4):719–724. doi:10.1016/j.clinph.2010.08.024

    CAS  Article  PubMed  Google Scholar 

  18. Schnakers C, Perrin F, Schabus M, Majerus S, Ledoux D, Damas P, Boly M, Vanhaudenhuyse A, Bruno MA, Moonen G, Laureys S (2008) Voluntary brain processing in disorders of consciousness. Neurology 71(20):1614–1620. doi:10.1212/01.wnl.0000334754.15330.69

    CAS  Article  PubMed  Google Scholar 

  19. Pritchard WS (1981) Psychophysiology of P300. Psychol Bull 89(3):506–540

    CAS  Article  PubMed  Google Scholar 

  20. Johnson R Jr (1986) A triarchic model of P300 amplitude. Psychophysiology 23(4):367–384

    Article  PubMed  Google Scholar 

  21. Bekinschtein TA, Golombek DA, Simonetta SH, Coleman MR, Manes FF (2009) Circadian rhythms in the vegetative state. Brain Inj 23(11):915–919. doi:10.1080/02699050903283197

    CAS  Article  PubMed  Google Scholar 

  22. Cruse D, Thibaut A, Demertzi A, Nantes JC, Bruno MA, Gosseries O, Vanhaudenhuyse A, Bekinschtein TA, Owen AM, Laureys S (2013) Actigraphy assessments of circadian sleep-wake cycles in the vegetative and minimally conscious states. BMC Med 11:18. doi:10.1186/1741-7015-11-18

    PubMed Central  Article  PubMed  Google Scholar 

  23. Grill E, Klein AM, Howell K, Arndt M, Bodrozic L, Herzog J, Jox R, Koenig E, Mansmann U, Müller F, Müller T, Dennis N, Schaupp M, Straube A, Bender A (2013) Design of the prospective german registry of outcome in patients with severe disorders of consciousness after acute brain injury. Arch Phys Med Rehabil 94(10):1870–1876

    Article  PubMed  Google Scholar 

  24. Lehmann D, Skrandies W (1980) Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroencephalogr Clin Neurophysiol 48(6):609–621

    CAS  Article  PubMed  Google Scholar 

  25. Esser SK, Huber R, Massimini M, Peterson MJ, Ferrarelli F, Tononi G (2006) A direct demonstration of cortical LTP in humans: a combined TMS/EEG study. Brain Res Bull 69(1):86–94. doi:10.1016/j.brainresbull.2005.11.003

    CAS  Article  PubMed  Google Scholar 

  26. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15(1):1–25

    Article  PubMed  Google Scholar 

  27. Maris E, Oostenveld R (2007) Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods 164(1):177–190. doi:10.1016/j.jneumeth.2007.03.024

    Article  PubMed  Google Scholar 

  28. Oostenveld R, Fries P, Maris E, Schoffelen JM (2011) FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:9

    Article  Google Scholar 

  29. Pinheiro J, Bates D, DebRoy S, Sarker D, R Development Core Team (2013) nlme: linear and nonlinear mixed effects models. R package version 3.1–111

  30. Krippendorff K (2011) Computing Krippendorff’s alpha-reliability. Retrieved from http://repository.upenn.edu/asc_papers/43

  31. Walhovd KB, Fjell AM (2002) One-year test-retest reliability of auditory ERPs in young and old adults. Int J Psychophysiol 46(1):29–40

    Article  PubMed  Google Scholar 

  32. Cassidy SM, Robertson IH, O’Connell RG (2012) Retest reliability of event-related potentials: evidence from a variety of paradigms. Psychophysiology 49(5):659–664. doi:10.1111/j.1469-8986.2011.01349.x

    Article  PubMed  Google Scholar 

  33. Duncan-Johnson CC, Donchin E (1977) On quantifying surprise: the variation of event-related potentials with subjective probability. Psychophysiology 14(5):456–467

    CAS  Article  PubMed  Google Scholar 

  34. 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(9809):2088–2094. doi:10.1016/S0140-6736(11)61224-5

    Article  PubMed  Google Scholar 

Download references

Conflicts of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Ethical standard

This study has been approved by the ethics committee of the University of Munich and has, therefore, been performed in the accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Barbara Schorr.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Schorr, B., Schlee, W., Arndt, M. et al. Stability of auditory event-related potentials in coma research. J Neurol 262, 307–315 (2015). https://doi.org/10.1007/s00415-014-7561-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-014-7561-y

Keywords

  • Disorders of consciousness
  • Minimally conscious state
  • Unresponsive wakefulness syndrome
  • P300
  • ERPs
  • EEG