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Semin Neurol 2022; 42(03): 299-308
DOI: 10.1055/a-1892-1715
Review Article

Uncovering Consciousness and Revealing the Preservation of Mental Life in Unresponsive Brain-Injured Patients

Lorina Naci
1   Trinity College Institute of Neuroscience, School of Psychology, Trinity College Dublin, Dublin, Ireland
2   Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland
,
Adrian M. Owen
3   Department of Physiology and Pharmacology, Western University, London, Canada
4   Department of Psychology, Western University, London, Canada
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Abstract

In the last few years, functional neuroimaging and electroencephalography-based techniques have been used to address one of the most complex and challenging questions in clinical medicine, that of detecting covert awareness in behaviorally unresponsive patients who have survived severe brain injuries. This is a very diverse population with a wide range of etiologies and comorbidities, as well as variable cognitive and behavioral abilities, which render accurate diagnosis extremely challenging. These studies have shown that some chronic behaviorally unresponsive patients harbor not only covert consciousness but also highly preserved levels of mental life. Building on this work, although in its infancy, the investigation of covert consciousness in acutely brain-injured patients could have profound implications for patient prognosis, treatment, and decisions regarding withdrawal of care. The body of evidence on covert awareness presents a moral imperative to redouble our efforts for improving the quality of life and standard of care for all brain-injured patients with disorders of consciousness.

Keywords

covert consciousness - brain injury - mental life


Publikationsverlauf

Accepted Manuscript online:
05. Juli 2022

Artikel online veröffentlicht:
13. September 2022

© 2022. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 Plum F, Posner JB. The Diagnosis of Stupor and Coma. 3rd ed. Philadelphia: Oxford University Press; 1980
    Google Scholar
  • 2 Laureys S, Owen AM, Schiff ND. Brain function in coma, vegetative state, and related disorders. Lancet Neurol 2004; 3 (09) 537-546
    CrossrefPubMedGoogle Scholar
  • 3 Owen AM, Coleman MR. Using neuroimaging to detect awareness in disorders of consciousness. Funct Neurol 2008; 23 (04) 189-194
    PubMedGoogle Scholar
  • 4 Laureys S, Celesia GG, Cohadon F. et al; European Task Force on Disorders of Consciousness. Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med 2010; 8: 68
    Google Scholar
  • 5 Peterson A, Norton L, Naci L, Owen AM, Weijer C. Toward a science of brain death. Am J Bioeth 2014; 14 (08) 29-31
    CrossrefPubMedGoogle Scholar
  • 6 Schnakers C, Vanhaudenhuyse A, Giacino J. et al. Diagnostic accuracy of the vegetative and minimally conscious state: clinical consensus versus standardized neurobehavioral assessment. BMC Neurol 2009; 9: 35
    Google Scholar
  • 7 Andrews K, Murphy L, Munday R, Littlewood C. Misdiagnosis of the vegetative state: retrospective study in a rehabilitation unit. BMJ 1996; 313 (7048): 13-16
    Google Scholar
  • 8 Naci L, Owen AM. Making every word count for nonresponsive patients. JAMA Neurol 2013; 70 (10) 1235-1241
    PubMedGoogle Scholar
  • 9 Fernández-Espejo D, Owen AM. Detecting awareness after severe brain injury. Nat Rev Neurosci 2013; 14 (11) 801-809
    CrossrefPubMedGoogle Scholar
  • 10 Bardin JC, Fins JJ, Katz DI. et al. Dissociations between behavioural and functional magnetic resonance imaging-based evaluations of cognitive function after brain injury. Brain 2011; 134 (Pt 3): 769-782
    CrossrefPubMedGoogle Scholar
  • 11 Goldfine AM, Victor JD, Conte MM, Bardin JC, Schiff ND. Determination of awareness in patients with severe brain injury using EEG power spectral analysis. Clin Neurophysiol 2011; 122 (11) 2157-2168
    CrossrefPubMedGoogle Scholar
  • 12 Cruse D, Chennu S, Chatelle C. et al. Bedside detection of awareness in the vegetative state: a cohort study. Lancet 2011; 378 (9809): 2088-2094
    CrossrefPubMedGoogle Scholar
  • 13 Cruse D, Chennu S, Fernández-Espejo D, Payne WL, Young GB, Owen AM. Detecting awareness in the vegetative state: electroencephalographic evidence for attempted movements to command. PLoS One 2012; 7 (11) e49933
    CrossrefPubMedGoogle Scholar
  • 14 Monti MM, Vanhaudenhuyse A, Coleman MR. et al. Willful modulation of brain activity in disorders of consciousness. N Engl J Med 2010; 362 (07) 579-589
    Google Scholar
  • 15 Owen AM, Coleman MR, Boly M, Davis MH, Laureys S, Pickard JD. Detecting awareness in the vegetative state. Science 2006; 313 (5792): 1402
    CrossrefPubMedGoogle Scholar
  • 16 Boly M, Coleman MR, Davis MH. et al. When thoughts become action: an fMRI paradigm to study volitional brain activity in non-communicative brain injured patients. Neuroimage 2007; 36 (03) 979-992
    CrossrefPubMedGoogle Scholar
  • 17 Owen AM, Coleman MR, Boly M. et al. Response to comments on “detecting awareness in the vegetative state”. Science 2007; 315 (5816): 1221-1
    CrossrefPubMedGoogle Scholar
  • 18 Monti MM, Coleman MR, Owen AM. Executive functions in the absence of behavior: functional imaging of the minimally conscious state. Prog Brain Res 2009; 177: 249-260
    CrossrefPubMedGoogle Scholar
  • 19 Naci L, Cusack R, Jia VZ, Owen AM. The brain's silent messenger: using selective attention to decode human thought for brain-based communication. J Neurosci 2013; 33 (22) 9385-9393
    CrossrefPubMedGoogle Scholar
  • 20 Bruno MA, 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. J Neurol 2011; 258 (07) 1373-1384
    CrossrefPubMedGoogle Scholar
  • 21 Cincotti F, Mattia D, Babiloni C. et al. The use of EEG modifications due to motor imagery for brain-computer interfaces. IEEE Trans Neural Syst Rehabil Eng 2003; 11 (02) 131-133
    CrossrefPubMedGoogle Scholar
  • 22 Wolpaw JR, McFarland DJ, Neat GW, Forneris CA. An EEG-based brain-computer interface for cursor control. Electroencephalogr Clin Neurophysiol 1991; 78 (03) 252-259
    CrossrefPubMedGoogle Scholar
  • 23 Cruse D, Chennu S, Chatelle C. et al. Relationship between etiology and covert cognition in the minimally conscious state. Neurology 2012; 78 (11) 816-822
    CrossrefPubMedGoogle Scholar
  • 24 Naci L, Haugg A, MacDonald A. et al. Functional diversity of brain networks supports consciousness and verbal intelligence. Sci Rep 2018; 8 (01) 13259
    CrossrefPubMedGoogle Scholar
  • 25 Naci L, Cusack R, Anello M, Owen AM. A common neural code for similar conscious experiences in different individuals. Proc Natl Acad Sci U S A 2014; 111 (39) 14277-14282
    CrossrefPubMedGoogle Scholar
  • 26 Curley WH, Forgacs PB, Voss HU, Conte MM, Schiff ND. Characterization of EEG signals revealing covert cognition in the injured brain. Brain 2018; 141 (05) 1404-1421
    CrossrefPubMedGoogle Scholar
  • 27 Edlow BL, Chatelle C, Spencer CA. et al. Early detection of consciousness in patients with acute severe traumatic brain injury. Brain 2017; 140 (09) 2399-2414
    Google Scholar
  • 28 Schiff ND. Cognitive motor dissociation following severe brain injuries. JAMA Neurol 2015; 72 (12) 1413-1415
    Google Scholar
  • 29 Rohaut B, Eliseyev A, Claassen J. Uncovering consciousness in unresponsive ICU patients: technical, medical and ethical considerations. Crit Care 2019; 23 (01) 78
    CrossrefPubMedGoogle Scholar
  • 30 Barbey AK, Colom R, Solomon J, Krueger F, Forbes C, Grafman J. An integrative architecture for general intelligence and executive function revealed by lesion mapping. Brain 2012; 135 (Pt 4): 1154-1164
    CrossrefPubMedGoogle Scholar
  • 31 Duncan J. The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour. Trends Cogn Sci 2010; 14 (04) 172-179
    CrossrefPubMedGoogle Scholar
  • 32 Robertson IH, Manly T, Andrade J, Baddeley BT, Yiend J. 'Oops!': performance correlates of everyday attentional failures in traumatic brain injured and normal subjects. Neuropsychologia 1997; 35 (06) 747-758
    CrossrefPubMedGoogle Scholar
  • 33 Giacino JT, Kalmar K, Whyte J. The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil 2004; 85 (12) 2020-2029
    PubMedGoogle Scholar
  • 34 Naci L, Sinai L, Owen AM. Detecting and interpreting conscious experiences in behaviorally non-responsive patients. Neuroimage 2017; 145 (Pt B): 304-313
    CrossrefPubMedGoogle Scholar
  • 35 Naci L, Graham M, Owen AM, Weijer C. Covert narrative capacity: a cross-section of the preserved mental life in patients thought to lack consciousness. Ann Clin Transl Neurol 2016; 1: 61-70
    PubMedGoogle Scholar
  • 36 Haugg A, Cusack R, Gonzalez-Lara LE, Sorger B, Owen AM, Naci L. Do patients thought to lack consciousness retain the capacity for internal as well as external awareness?. Front Neurol 2018; 9: 492
    CrossrefPubMedGoogle Scholar
  • 37 Sinai L, Owen AM, Naci L. Mapping preserved real-world cognition in severely brain-injured patients. Front Biosci 2017; 22 (05) 815-823
    CrossrefPubMedGoogle Scholar
  • 38 Owen AM, Naci L. Decoding thoughts in behaviorally non-responsive patients. In: Sinnott-Armstrong W. ed. Finding Consciousness. New York, NY: Oxford University Press; 2016: 100-121
    Google Scholar
  • 39 Owen AM, Naci L. Decoding thoughts in disorders of consciousness. In: Monti M, Sannita WG. eds. Brain Function and Responsiveness in Severe Disorders of Consciousness. Switzerland: Springer International; 2016: 67-80
    Google Scholar
  • 40 Guglielmo S. Moral judgment as information processing: an integrative review. Front Psychol 2015; 6: 1637
    CrossrefPubMedGoogle Scholar
  • 41 Lehne M, Koelsch S. Toward a general psychological model of tension and suspense. Front Psychol 2015; 6: 79
    CrossrefPubMedGoogle Scholar
  • 42 Peterson A, Cruse D, Naci L, Weijer C, Owen AM. Risk, diagnostic error, and the clinical science of consciousness. Neuroimage Clin 2015; 7: 588-597
    CrossrefPubMedGoogle Scholar
  • 43 Chung C, Pollock A, Campbell T, Durward B, Hagen S. Cognitive rehabilitation for executive dysfunction in adults with stroke or other adult nonprogressive acquired brain damage. Stroke 2013; 44 (07) e77-e78
    CrossrefPubMedGoogle Scholar
  • 44 Giacino JT, Ashwal S, Childs N. et al. The minimally conscious state: definition and diagnostic criteria. Neurology 2002; 58 (03) 349-353
    Google Scholar
  • 45 McDowell S, Whyte J, D'Esposito M. Working memory impairments in traumatic brain injury: evidence from a dual-task paradigm. Neuropsychologia 1997; 35 (10) 1341-1353
    CrossrefPubMedGoogle Scholar
  • 46 Kondziella D, Friberg CK, Frokjaer VG, Fabricius M, Møller K. Preserved consciousness in vegetative and minimal conscious states: systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 2016; 87 (05) 485-492
    CrossrefPubMedGoogle Scholar
  • 47 Gibson RM, Chennu S, Fernández-Espejo D, Naci L, Owen AM, Cruse D. Somatosensory attention identifies both overt and covert awareness in disorders of consciousness. Ann Neurol 2016; 80 (03) 412-423
    CrossrefPubMedGoogle Scholar
  • 48 Sanz LRD, Thibaut A, Edlow BL, Laureys S, Gosseries O. Update on neuroimaging in disorders of consciousness. Curr Opin Neurol 2021; 34 (04) 488-496
    CrossrefPubMedGoogle Scholar
  • 49 González-Lara L, Owen AM. Identifying covert cognition in disorders of consciousness. In: Schnakers C, Laureys S. eds. Coma and Disorders of Consciousness. Switzerland: Springer International Publishing; 2018: 77-96
    Google Scholar
  • 50 Beisteiner R, Klinger N, Höllinger I. et al. How much are clinical fMRI reports influenced by standard postprocessing methods? An investigation of normalization and region of interest effects in the medial temporal lobe. Hum Brain Mapp 2010; 31 (12) 1951-1966
    CrossrefPubMedGoogle Scholar
  • 51 Crinion J, Ashburner J, Leff A, Brett M, Price C, Friston K. Spatial normalization of lesioned brains: performance evaluation and impact on fMRI analyses. Neuroimage 2007; 37 (03) 866-875
    CrossrefPubMedGoogle Scholar
  • 52 Bekinschtein TA, Dehaene S, Rohaut B, Tadel F, Cohen L, Naccache L. Neural signature of the conscious processing of auditory regularities. Proc Natl Acad Sci U S A 2009; 106 (05) 1672-1677
    CrossrefPubMedGoogle Scholar
  • 53 Engemann DA, Raimondo F, King JR. et al. Robust EEG-based cross-site and cross-protocol classification of states of consciousness. Brain 2018; 141 (11) 3179-3192
    CrossrefPubMedGoogle Scholar
  • 54 Naccache L, King JR, Sitt J. et al. Neural detection of complex sound sequences or of statistical regularities in the absence of consciousness?. Brain 2015; 138 (Pt 12): e395
    CrossrefPubMedGoogle Scholar
  • 55 Casarotto S, Comanducci A, Rosanova M. et al. Stratification of unresponsive patients by an independently validated index of brain complexity. Ann Neurol 2016; 80 (05) 718-729
    CrossrefPubMedGoogle Scholar
  • 56 Casali AG, Gosseries O, Rosanova M. et al. A theoretically based index of consciousness independent of sensory processing and behavior. Sci Transl Med 2013; 5 (198) 198ra105
    CrossrefPubMedGoogle Scholar
  • 57 Weijer C, Bruni T, Gofton T. et al. Ethical considerations in functional magnetic resonance imaging research in acutely comatose patients. Brain 2016; 139 (Pt 1): 292-299
    CrossrefPubMedGoogle Scholar
  • 58 Claassen J, Velazquez A, Meyers E. et al. Bedside quantitative electroencephalography improves assessment of consciousness in comatose subarachnoid hemorrhage patients. Ann Neurol 2016; 80 (04) 541-553
    CrossrefPubMedGoogle Scholar
  • 59 Claassen J, Doyle K, Matory A. et al. Detection of brain activation in unresponsive patients with acute brain injury. N Engl J Med 2019; 380 (26) 2497-2505
    Google Scholar
  • 60 Wilson JTL, Pettigrew LEL, Teasdale GM. Structured interviews for the Glasgow Outcome Scale and the extended Glasgow Outcome Scale: guidelines for their use. J Neurotrauma 1998; 15 (08) 573-585
    CrossrefPubMedGoogle Scholar
  • 61 Sokoliuk R, Degano G, Banellis L. et al. Covert speech comprehensions predicts recovery from acute unresponsive states. Ann Neurol 2021; 89 (04) 646-656
    Google Scholar
  • 62 Guger C, Sorger B, Noirhomme Q. et al. Brain-computer interfaces for assessment and communication in disorders of consciousness. In: Emerging Theory and Practice in Neuroprosthetics. 2014:181–214. IGIGLOBAL Press, 2013
    Google Scholar
  • 63 Naccache L. Minimally conscious state or cortically mediated state?. Brain 2018; 141 (04) 949-960
    CrossrefPubMedGoogle Scholar
  • 64 Bayne T, Hohwy J, Owen AM. Reforming the taxonomy in disorders of consciousness. Ann Neurol 2017; 82 (06) 866-872
    CrossrefPubMedGoogle Scholar
  • 65 Bernat JL. Nosologic considerations in disorders of consciousness. Ann Neurol 2017; 82 (06) 863-865
    CrossrefPubMedGoogle Scholar
  • 66 Giacino JT, Katz DI, Schiff ND. et al. Practice guideline update recommendations summary: disorders of consciousness. Neurology 2018; 91 (10) 450-460
    Google Scholar
  • 67 Kondziella D, Bender A, Diserens K. et al; EAN Panel on Coma, Disorders of Consciousness. European Academy of Neurology guideline on the diagnosis of coma and other disorders of consciousness. Eur J Neurol 2020; 27 (05) 741-756
    Google Scholar
  • 68 Young M, Peterson AH. Neuroethics across the disorders of consciousness care continuum. Semin Neurol 2022; In press
    Google Scholar
  • 69 Young MJ, Bodien YG, Giacino JT. et al. The neuroethics of disorders of consciousness: a brief history of evolving ideas. Brain 2021; 144 (11) 3291-3310
    CrossrefPubMedGoogle Scholar
  • 70 Taylor N, Graham M, Delargy M, Naci L. Revealing memory during the vegetative state: implications for patient quality of life. Camb Q Healthc Ethics 2020; 29 (04) 501-510
    CrossrefPubMedGoogle Scholar
  • 71 Graham M, Weijer C, Cruse D. et al. An ethics of welfare for patients diagnosed as vegetative with covert awareness. AJOB Neurosci 2015; 6 (02) 31-41
    CrossrefPubMedGoogle Scholar
  • 72 Graham M, Naci L. Well-being after severe brain injury: What counts as good recovery?. Camb Q Healthc Ethics 2021; 30 (04) 613-622
    CrossrefPubMedGoogle Scholar
  • 73 Tung J, Speechley KN, Gofton T. et al. Towards the assessment of quality of life in patients with disorders of consciousness. Qual Life Res 2020; 29 (05) 1217-1227
    CrossrefPubMedGoogle Scholar
  • 74 Turgeon AF, Lauzier F, Simard JF. et al; Canadian Critical Care Trials Group. Mortality associated with withdrawal of life-sustaining therapy for patients with severe traumatic brain injury: a Canadian multicentre cohort study. CMAJ 2011; 183 (14) 1581-1588
    Google Scholar
  • 75 Graham M, Wallace E, Doherty C, McCann A, Naci L. From awareness to prognosis: Ethical implications of uncovering hidden awareness in behaviorally nonresponsive patients. Camb Q Healthc Ethics 2019; 28 (04) 616-631
    CrossrefPubMedGoogle Scholar
  • 76 Graham M, Doherty CP, Naci L. Using neuroimaging to detect covert awareness and determine prognosis of comatose patients: Informing surrogate decision makers of individual patient results. Semin Neurol 2018; 38 (05) 555-560
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 77 Naci L, Monti MM, Cruse D. et al. Brain-computer interfaces for communication with nonresponsive patients. Ann Neurol 2012; 72 (03) 312-323
    CrossrefPubMedGoogle Scholar