Neuroimaging of Consciousness in the Vegetative and Minimally Conscious States

Chapter

Abstract

Differentiating reflex from voluntary activity is one of the most challenging task facing clinicians involved in the care of patients presenting disorders of consciousness such as vegetative and minimally conscious states. Behavioral assessment is considered as the main way to detect signs of consciousness but may often be complicated by verbal and motor impairments. As misdiagnosis can lead to serious consequences, especially, in terms of pain treatment and end-of-life decision-making, objective paramedical tools have to be used to assess remnant brain functioning and detect brain activity linked to consciousness. We therefore here review the current state of clinical behavioral assessment and functional neuroimaging paradigms as these may offer complementary information to bedside examination findings.

Keywords

Glasgow Coma Scale Brain Death Vegetative State Conscious State White Matter Integrity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. American Congress of Rehabilitation Medicine (1995) Recommendations for use of uniform nomenclature pertinent to patients with severe alterations of consciousness. Arch Phys Med Rehabil 76:205–209CrossRefGoogle Scholar
  2. Andrews K, Murphy L, Munday R, Littlewood C (1996) Misdiagnosis of the vegetative state: ­retrospective study in a rehabilitation unit. BMJ 313(7048):13–16PubMedCrossRefGoogle Scholar
  3. Arthuis M, Valton L, Regis J, Chauvel P, Wendling F, Naccache L, Bernard C, Bartolomei F (2009) Impaired consciousness during temporal lobe seizures is related to increased long-distance cortical-subcortical synchronization. Brain 132:2091–2101PubMedCrossRefGoogle Scholar
  4. Bardin JC, Fins JJ, Katz DI, Hersh J, Heier LA, Tabelow K, Dyke JP, Ballon DJ, Schiff ND, Voss HU (2011) Dissociations between behavioural and functional magnetic resonance imaging-based evaluations of cognitive function after brain injury. Brain 134:769–782PubMedCrossRefGoogle Scholar
  5. Bauer G, Gerstenbrand F, Rumpl E (1979) Varieties of the locked-in syndrome. J Neurol 221(2):77–91PubMedCrossRefGoogle Scholar
  6. Boly M (2011) Measuring the fading consciousness in the human brain. Curr Opin Neurol 24:394–400PubMedCrossRefGoogle Scholar
  7. Boly M, Faymonville ME, Schnakers C, Peigneux P, Lambermont B, Phillips C, Lancellotti P, Luxen A, Lamy M, Moonen G et al (2008) Perception of pain in the minimally conscious state with PET activation: an observational study. Lancet Neurol 7:1013–1020PubMedCrossRefGoogle Scholar
  8. Boly M, Massimini M, Tononi G (2009a) Theoretical approaches to the diagnosis of altered states of consciousness. Prog Brain Res 177:383–398PubMedCrossRefGoogle Scholar
  9. Boly M, Tshibanda L, Vanhaudenhuyse A, Noirhomme Q, Schnakers C, Ledoux D, Boveroux P, Garweg C, Lambermont B, Phillips C et al (2009b) Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient. Hum Brain Mapp 30:2393–2400PubMedCrossRefGoogle Scholar
  10. Boveroux P, Vanhaudenhuyse A, Bruno MA, Noirhomme Q, Lauwick S, Luxen A, Degueldre C, Plenevaux A, Schnakers C, Phillips C et al (2010) Breakdown of within- and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness. Anesthesiology 113:1038–1053PubMedCrossRefGoogle Scholar
  11. Bruno MA, Gosseries O, Ledoux D, Hustinx R, Laureys S (2011) Assessment of consciousness with electrophysiological and neurological imaging techniques. Curr Opin Crit Care 17:146–151PubMedCrossRefGoogle Scholar
  12. Bruno M-A, Ledoux D, Vanhaudenhuyse A, Gosseries O, Thibaut A, Laureys S (2012a) Prognosis of patients with altered state of consciousness. In: Schnakers C, Laureys S (eds) Coma and disorders of consciousness. Springer, LondonGoogle Scholar
  13. Bruno MA, Majerus S, Boly M, Vanhaudenhuyse A, Schnakers C, Gosseries O, Boveroux P, Kirsch M, Demertzi A, Bernard C et al (2012b) Functional neuroanatomy underlying the clinical subcategorization of minimally conscious state patients. J Neurol 259(6):1087–1098PubMedCrossRefGoogle Scholar
  14. Buckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, Hedden T, Andrews-Hanna JR, Sperling RA, Johnson KA (2009) Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer’s disease. J Neurosci 29:1860–1873PubMedCrossRefGoogle Scholar
  15. Childs NL, Mercer WN, Childs HW (1993) Accuracy of diagnosis of persistent vegetative state. Neurology 43(8):1465–1467PubMedCrossRefGoogle Scholar
  16. Coleman MR, Davis MH, Rodd JM, Robson T, Ali A, Owen AM, Pickard JD (2009) Towards the routine use of brain imaging to aid the clinical diagnosis of disorders of consciousness. Brain 132:2541–2552PubMedCrossRefGoogle Scholar
  17. 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 378:2088–2094PubMedCrossRefGoogle Scholar
  18. Dehaene S, Changeux JP, Naccache L, Sackur J, Sergent C (2006) Conscious, preconscious, and subliminal processing: a testable taxonomy. Trends Cogn Sci 10:204–211PubMedCrossRefGoogle Scholar
  19. Di HB, Yu SM, Weng XC, Laureys S, Yu D, Li JQ, Qin PM, Zhu YH, Zhang SZ, Chen YZ (2007) Cerebral response to patient’s own name in the vegetative and minimally conscious states. Neurology 68:895–899PubMedCrossRefGoogle Scholar
  20. Fernandez-Espejo D, Bekinschtein T, Monti MM, Pickard JD, Junque C, Coleman MR, Owen AM (2011) Diffusion weighted imaging distinguishes the vegetative state from the minimally conscious state. Neuroimage 54:103–112PubMedCrossRefGoogle Scholar
  21. Fernandez-Espejo D, Junque C, Bernabeu M, Roig-Rovira T, Vendrell P, Mercader JM (2010) Reductions of thalamic volume and regional shape changes in the vegetative and the minimally conscious States. J Neurotrauma 27:1187–1193PubMedCrossRefGoogle Scholar
  22. Ferrarelli F, Massimini M, Sarasso S, Casali A, Riedner BA, Angelini G, Tononi G, Pearce RA (2010) Breakdown in cortical effective connectivity during midazolam-induced loss of consciousness. Proc Natl Acad Sci U S A 107:2681–2686PubMedCrossRefGoogle Scholar
  23. Fischer C, Luaute J, Morlet D (2010) Event-related potentials (MMN and novelty P3) in permanent vegetative or minimally conscious states. Clin Neurophysiol 121:1032–1042PubMedCrossRefGoogle Scholar
  24. Giacino JT, Ashwal S, Childs N, Cranford R, Jennett B, Katz DI, Kelly JP, Rosenberg JH, Whyte J, Zafonte RD et al (2002) The minimally conscious state: definition and diagnostic criteria. Neurology 58(3):349–353PubMedCrossRefGoogle Scholar
  25. Giacino J, Kalmar K, Whyte J (2004) The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil 85(12):2020–2029PubMedCrossRefGoogle Scholar
  26. Guye M, Regis J, Tamura M, Wendling F, McGonigal A, Chauvel P, Bartolomei F (2006) The role of corticothalamic coupling in human temporal lobe epilepsy. Brain 129:1917–1928PubMedCrossRefGoogle Scholar
  27. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6:e159PubMedCrossRefGoogle Scholar
  28. Jennett B (2005) 30 years of the vegetative state: clinical, ethical and legal problems. In: Laureys S (ed) The boundaries of consciousness: neurobiology and neuropathology. Elsevier, AmsterdamGoogle Scholar
  29. Laureys S, Celesia GG, Cohadon F, Lavrijsen J, Leon-Carrion 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 8:68PubMedCrossRefGoogle Scholar
  30. Laureys S (2005a) Science and society: death, unconsciousness and the brain. Nat Rev Neurosci 6(11):899–909PubMedCrossRefGoogle Scholar
  31. Laureys S, Pellas F, Van Eeckhout P, Ghorbel S, Schnakers C, Perrin F, Berré J, Faymonville ME, Pantke KH, Damas F et al (2005b) The locked-in syndrome: what is it like to be conscious but paralyzed and voiceless? Prog Brain Res 150:495–511PubMedCrossRefGoogle Scholar
  32. Luaute J, Maucort-Boulch D, Tell L, Quelard F, Sarraf T, Iwaz J, Boisson D, Fischer C (2010) Long-term outcomes of chronic minimally conscious and vegetative states. Neurology 75:246–252PubMedCrossRefGoogle Scholar
  33. Massimini M, Boly M, Casali A, Rosanova M, Tononi G (2009) A perturbational approach for evaluating the brain’s capacity for consciousness. Prog Brain Res 177:201–214PubMedCrossRefGoogle Scholar
  34. McNett M (2007) A review of the predictive ability of Glasgow Coma Scale scores in head-injured patients. J Neurosci Nurs 39(2):68–75PubMedCrossRefGoogle Scholar
  35. Monti MM, Vanhaudenhuyse A, Coleman MR, Boly M, Pickard JD, Tshibanda L, Owen AM, Laureys S (2010) Willful modulation of brain activity in disorders of consciousness. N Engl J Med 362:579–589PubMedCrossRefGoogle Scholar
  36. Nachev P, Hacker PM (2010) Covert cognition in the persistent vegetative state. Prog Neurobiol 91:68–76PubMedCrossRefGoogle Scholar
  37. Newcombe VF, Williams GB, Scoffings D, Cross J, Carpenter TA, Pickard JD, Menon DK (2010) Aetiological differences in neuroanatomy of the vegetative state: insights from diffusion tensor imaging and functional implications. J Neurol Neurosurg Psychiatry 81:552–561PubMedCrossRefGoogle Scholar
  38. Owen AM, Coleman MR, Boly M, Davis MH, Laureys S, Pickard JD (2006) Detecting awareness in the vegetative state. Science 313:1402PubMedCrossRefGoogle Scholar
  39. Perlbarg V, Puybasset L, Tollard E, Lehericy S, Benali H, Galanaud D (2009) Relation between brain lesion location and clinical outcome in patients with severe traumatic brain injury: a diffusion tensor imaging study using voxel-based approaches. Hum Brain Mapp 30:3924–3933PubMedCrossRefGoogle Scholar
  40. Phillips CL, Bruno MA, Maquet P, Boly M, Noirhomme Q, Schnakers C, Vanhaudenhuyse A, Bonjean M, Hustinx R, Moonen G et al (2011) “Relevance vector machine” consciousness classifier applied to cerebral metabolism of vegetative and locked-in patients. Neuroimage 56(2):797–808PubMedCrossRefGoogle Scholar
  41. Plum F, Posner JB (1966) The diagnosis of stupor and coma, 1st edn. Davis, PhiladelphiaGoogle Scholar
  42. 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 31:1993–2002PubMedCrossRefGoogle Scholar
  43. Rafii MS, Brewer JB (2010) Functional brain imaging in the clinical assessment of consciousness. PLoS Biol 8:1000548CrossRefGoogle Scholar
  44. Rodriguez Moreno D, Schiff ND, Giacino J, Kalmar K, Hirsch J (2010) A network approach to assessing cognition in disorders of consciousness. Neurology 75:1871–1878PubMedCrossRefGoogle Scholar
  45. Rosanova M, Gosseries O, Casarotto S, Boly M, Casali AG, Bruno MA, Mariotti M, Boveroux P, Tononi G, Laureys S, Massimini M (2012) Recovery of cortical effective connectivity and recovery of consciousness in vegetative patients. Brain 135:1308–1320PubMedCrossRefGoogle Scholar
  46. Schnakers C, Chatelle C, Demertzi A, Majerus S, Laureys S (2012) What about pain in disorders of consciousness? AAPS J 14(3):437–444PubMedCrossRefGoogle Scholar
  47. Schnakers C, Chatelle C, Vanhaudenhuyse A, Majerus S, Ledoux D, Boly M, Bruno MA, Boveroux P, Demertzi A, Moonen G et al (2010) The Nociception Coma Scale: a new tool to assess nociception in disorders of consciousness. Pain 148(2):215–219PubMedCrossRefGoogle Scholar
  48. Schnakers C, Perrin F, Schabus M, Hustinx R, Majerus S, Moonen G, Boly M, Vanhaudenhuyse A, Bruno MA, Laureys S (2009a) Detecting consciousness in a total locked-in syndrome: an active event-related paradigm. Neurocase 15:271–277PubMedCrossRefGoogle Scholar
  49. Schnakers C, Vanhaudenhuyse A, Giacino J, Ventura M, Boly M, Majerus S, Moonen G, Laureys S (2009b) Diagnostic accuracy of the vegetative and minimally conscious state: clinical consensus versus standardized neurobehavioral assessment. BMC Neurol 9:35PubMedCrossRefGoogle Scholar
  50. Seel RT, Sherer M, Whyte J, Katz DI, Giacino JT, Rosenbaum AM, Hammond FM, Kalmar K, Pape TL, Zafonte R et al (2010) Assessment scales for disorders of consciousness: evidence-based recommendations for clinical practice and research. Arch Phys Med Rehabil 91(12):1795–1813PubMedCrossRefGoogle Scholar
  51. Shiel A, Horn SA, Wilson BA, Watson MJ, Campbell MJ, McLellan DL (2000) The Wessex Head Injury Matrix (WHIM) main scale: a preliminary report on a scale to assess and monitor patient recovery after severe head injury. Clin Rehabil 14(4):408–416PubMedCrossRefGoogle Scholar
  52. Silva S, Alacoque X, Fourcade O, Samii K, Marque P, Woods R, Mazziotta J, Chollet F, Loubinoux I (2010) Wakefulness and loss of awareness: brain and brainstem interaction in the vegetative state. Neurology 74:313–320PubMedCrossRefGoogle Scholar
  53. Soddu A, Vanhaudenhuyse A, Bahri M, Bruno MA, Boly M, Demertzi A, Tshibanda L, Phillips C, Stanziano M, Ovadia S et al (2012) Identifying the default mode component in spatial IC analyses of patients with disorders of consciousness. Hum Brain Mapp 33:778–796PubMedCrossRefGoogle Scholar
  54. Teasdale G, Jennett B (1974) Assessment of coma and impaired consciousness. A practical scale. Lancet 2(7872):81–84PubMedCrossRefGoogle Scholar
  55. The Multi-Society Task Force on PVS (1994) Medical aspects of the persistent vegetative state (1). N Engl J Med 330(21):1499–1508CrossRefGoogle Scholar
  56. Tononi G (2008) Consciousness as integrated information: a provisional manifesto. Biol Bull 215:216–242PubMedCrossRefGoogle Scholar
  57. Vanhaudenhuyse A, Noirhomme Q, Tshibanda LJ, Bruno MA, Boveroux P, Schnakers C, Soddu A, Perlbarg V, Ledoux D, Brichant JF et al (2010) Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain 133:161–171PubMedCrossRefGoogle Scholar
  58. Wijdicks EF (2012) The transatlantic divide over brain death determination and the debate. Brain 135(4):1321–1331PubMedCrossRefGoogle Scholar
  59. Wijdicks EF, Bamlet WR, Maramattom BV, Manno EM, McClelland RL (2005) Validation of a new coma scale: the FOUR score. Ann Neurol 58(4):585–593PubMedCrossRefGoogle Scholar
  60. Working Party of the Royal College of Physicians (2003) The vegetative state: guidance on diagnosis and management. Clin Med 3(3):249–254CrossRefGoogle Scholar
  61. Zhou J, Liu X, Song W, Yang Y, Zhao Z, Ling F, Hudetz AG, Li SJ (2011) Specific and nonspecific thalamocortical functional connectivity in normal and vegetative states. Conscious Cogn 20:257–268PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Caroline Schnakers
    • 1
  • Steven Laureys
    • 1
  • Melanie Boly
    • 1
  1. 1.Cyclotron Research CentreUniversity of LiègeLiègeBelgium

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