Structural and functional basis of chronic disorders of consciousness

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Abstract

The problem of chronic disorders of consciousness (DOC) remains challenging due to increasing number of these patients and limited therapeutic options. Novel diagnostic approaches provided us with valuable insights into the mechanisms of DOC, such as structural and/or functional disconnection of elements of brain networks that are essential for information processing. Depending on the modality of the study, it may be represented as low-frequency EEG patterns, global or more localized decrease of cortical metabolism on PET scanning, abnormal connectivity structural or functional MRI, or low-differentiated/disintegrated TMSEEG responses. Deeper knowledge of nature of abnormalities underlying chronic DOC may improve accuracy of diagnosis and efficacy of treatment interventions, as well as bring us somewhat closer to the understanding the phenomenon of consciousness.

About the authors

Mikhail A. Piradov

Research Center of Neurology

Email: dmsergeev@yandex.ru
ORCID iD: 0000-0002-6338-0392

D. Sci. (Med), Prof., Full Member of RAS, Director, Research Center of Neurology

Russian Federation, 125367 Moscow, Volokolamskoye shosse, 80

Natalya A. Suponeva

Research Center of Neurology

Email: dmsergeev@yandex.ru
ORCID iD: 0000-0003-3956-6362

D. Sci. (Med.), Professor, Corresponding Member of the Russian Academy of Sciences, principal researcher, Department of neurorehabilitation and physiotherapy

Russian Federation, Moscow

Dmitry V. Sergeev

Research Center of Neurology

Author for correspondence.
Email: dmsergeev@yandex.ru
Russian Federation, Moscow

Alexander V. Chervyakov

Research Center of Neurology

Email: dmsergeev@yandex.ru
Russian Federation, Moscow

Yulia V. Ryabinkina

Research Center of Neurology

Email: dmsergeev@yandex.ru
ORCID iD: 0000-0001-8576-9983

D. Sci. (Med.), Head, Department of anesthesiology and intensive care

Russian Federation, Moscow

Dmitry O. Sinitsyn

Research Center of Neurology

Email: dmsergeev@yandex.ru
Russian Federation, Moscow

Alexandra G. Poydasheva

Research Center of Neurology

Email: dmsergeev@yandex.ru
ORCID iD: 0000-0003-1841-1177

junior researcher, neurologist, Department of neurorehabilitation and physiotherapy

Russian Federation, Moscow

Elena I. Kremneva

Research Center of Neurology

Email: dmsergeev@yandex.ru
Russian Federation, Moscow

Sofia N. Morozova

Research Center of Neurology

Email: dmsergeev@yandex.ru
Russian Federation, Moscow

Elizaveta G. Yazeva

Research Center of Neurology

Email: dmsergeev@yandex.ru
Russian Federation, Moscow

Liudmila A. Legostaeva

Research Center of Neurology

Email: dmsergeev@yandex.ru
Russian Federation, Moscow

References

  1. Rosenblath W. Uber einen bemerkenswerten Fall von Himerschutterrun (aus dem Landkrankenshaus Kassel). Arch Klin Med 1899; 64: 406–424.
  2. Kretschmer E. Das apallische Syndrom. Z ges Neurol Psychiat 1940; 169: 576–579. doi: 10.1007/BF02871384.
  3. Jennett B., Plum F. Persistent vegetative state after brain damage. A syndrome in search of a name. Lancet 1972; 1(7753): 734-7. PMID: 4111204.
  4. Giacino J.T., Ashwal S., Childs N. et al. The minimally conscious state: definition and diagnostic criteria. Neurology 2002; 58: 349-353. PMID: 11839831.
  5. Laureys S., Celesia G.G., Cohadon F. et al. Unresponsive wakefulness syndrome: A new name for the vegetative state or apallic syndrome. BMC Med 2010;8: 68. doi: 10.1186/1741-7015-8-68. PMID: 21040571.
  6. Giacino G.T., Katz D.I., Schiff N.D. et al. Practice guideline update recommendations summary: Disorders of consciousness. Neurology 2018; 91(10):450-460. doi: 10.1212/WNL.0000000000005926. PMID: 30089618.
  7. Giacino G.T., Katz D.I., Schiff N.D. et al. Comprehensive systematic review update summary: Disorders of consciousness. Neurology 2018; 91(10): 461-470. doi: 10.1212/WNL.0000000000005928. PMID: 30089617.
  8. Bruno M.A., Vanhaudenhuyse A., Thibaut A. et al. 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: 1373-1384. doi: 10.1007/s00415-011-6114-x. PMID: 21674197.
  9. Bruno M.A., Schnakers C., Boly M. et al. Subcategorizing the minimally conscious state based on cerebral metabolism PET studies. In: 19th Meeting of the European Neurological Society 2009.
  10. Edelman G.M., Tononi G. A Universe of Consciousness: How Matter Becomes Imagination. New York.: Basic Books, 2003. 274 p.
  11. Edlow B.L.; Haynes, R.L., Takahashi E. et al. Disconnection of the Ascending Arousal System in Traumatic Coma. J Neuropathol Exp Neurol 2013; 72: 505–523. doi: 10.1097/NEN.0b013e3182945bf6. PMID: 23656993.
  12. Sherer M., Nakase-Thompson R., Yablon S.A. et al. Multidimensional assessment of acute confusion after traumatic brain injury. Arch Phys Med Rehabil 2005; 86(5): 896–904. doi: 10.1016/j.apmr.2004.09.029. PMID: 1589533.
  13. Eapen B.C., Georgekutty J., Subbarao B. et al. Disorders of Consciousness. Phys Med Rehabil Clin N Am 2017; 28(2): 245–258. doi: 10.1016/j.pmr.2016.12.003. PMID: 28390511.
  14. Laureys S. The neural correlate of (un)awareness: lessons from the vegetative state. Trends Cogn Sci 2005; 9: 556-559. doi: 10.1016/j.tics.2005.10.010PMID: 16271507.
  15. Schnakers C., Laureys S. (Eds.) Coma and Disorders of Consciousness, 2nd edition. Springer eBooks, 2018. 276 p.
  16. Adams J.H., Graham D.I., Jennett B. The neuropathology of the vegetative state after an acute brain insult. Brain 2000; 123: 1327–1338. PMID: 10869046.
  17. Giacino J., Malone R. The vegetative and minimally conscious states. In: Handbook of Clinical Neurology, Vol. 90 (3rd series). Disorders of consciousness. G.B. Young, E.F. Wijdicks, (Eds). 773-786.
  18. Dougherty J.H., Rawlinson D.G., Levy D.E. et al. Hypoxicischemic brain injury and the vegetative state: clinical and neuropathologic correlation. Neurology 1981; 31: 991–997. PMID: 7196525.
  19. Kinney H.C., Korein J., Panigrahy A. et al. Neuropathological findings in the brain of Karen Ann Quinlan: the role of the thalamus in the persistent vegetative state. N Engl J Med 1994; 330: 1469–1475. DOI: 10.1056/ NEJM199405263302101. PMID: 8164698.
  20. Rosenblum W.I. Immediate, irreversible, posttraumatic coma: a review indicating that bilateral brainstem injury rather than widespread hemispheric damage is essential for its production. J Neuropathol Exp Neurol 2015, 274, 198–202. doi: 10.1097/NEN.0000000000000170. PMID: 25668566.
  21. Lutkenhoff E.S., Chiang J., Tshibanda L. et al. Thalamic and extrathalamic mechanisms of consciousness after severe brain injury. Ann Neurol 2015; 78(1):68-76. doi: 10.1002/ana.24423. PMID: 25893530.
  22. 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(1): 35. doi: 10.1186/1471-2377-9-35. PMID: 19622138.
  23. Legostayeva L. A., Mochalova E.G., Suponeva N.A. et al. [The complications of the clinical diagnosis of chronic impairment of consciousness and recommendations for the clinical and instrumental assessment of patients after they leave the coma].Anesteziologiya i reanimatologiya 2017; 6 (62): 449-456. (In Russ.).
  24. Fernandez-Espejo D., Junque C., Bernabeu M. et al. Reductions of thalamic volume and regional shape changes in the vegetative and the minimally conscious states. J Neurotrauma 2010; 27: 1187–1193. doi: 10.1089/neu.2010.1297.PMID: 20392136.
  25. Annen J., Frasso G., Crone J.S. et al. Regional brain volumetry and brain function in severely brain-injured patients. Ann Neurol 2018; 83(4): 842-853. doi: 10.1002/ana.25214. PMID: 29572926.
  26. Kampfl A., Schmutzhard E., Franz G. et al. Prediction of recovery from post-traumatic vegetative state with cerebral magnetic-resonance imaging. Lancet 1998; 351: 1763–67. doi: 10.1016/S0140-6736(97)10301-4. PMID: 9635948.
  27. Morozova S., Kremneva E., Sergeev D. et al. Conventional Structural Magnetic Resonance Imaging in Differentiating Chronic Disorders of Consciousness. Brain Sci 2018; 8(8): E144. doi: 10.3390/brainsci8080144. PMID: 30081605.
  28. Fernandez-Espejo D., Bekinschtein T., Monti M.M. et al. Diffusion weighted imaging distinguishes the vegetative state from the minimally conscious state. Neuroimage 2011; 54: 103–112. doi: 10.1016/j.neuroimage.2010.08.035. PMID: 20728553.
  29. Fernandez-Espejo D., Soddu A., Cruse D. et al. A role for the default mode network in the bases of disorders of consciousness. Ann Neurol 2012; 72: 335–343. doi: 10.1002/ana.23635. PMID: 23034909.
  30. Annen J., Heine L., Ziegler E. et al. Function-structure connectivity in patients with severe brain injury as measured by MRI-DWI and FDG-PET. Hum Brain Map 2016; 37(11): 3707-3720. doi: 10.1002/hbm.23269. PMID: 27273334.
  31. Jensen JH, Helpern JA. MRI quantification of non-Gaussian water diffusion by kurtosis analysis. NMR Biomed 2010; 23(7): 698–710. doi: 10.1002/nbm.1518. PMID: 20632416.
  32. De Volder, A.G., Goffinet, A.M., Bol, A. et al. Brain glucose metabolism in postanoxic syndrome. Positron emission tomographic study. Arch Neurol 1990;47: 197–204. PMID: 2302091.
  33. Stender J., Kupers R., Rodell A., et al. Quantitative rates of brain glucose metabolism distinguish minimally conscious from vegetative state patients. J Cereb Blood Flow Metab 2015; 35(1):58-65. doi: 10.1038/jcbfm.2014. PMID: 25294128.
  34. Laureys S., Lemaire C., Maquet P. et al. Cerebral metabolism during vegetative state and after recovery to consciousness. J Neurol Neurosurg Psychiatry 1999;67: 121. PMID: 10454871.
  35. Laureys S., Pellas F., Van Eeckhout P. et al. The locked-in syndrome: what is it like to be conscious but paralyzed and voiceless? Prog Brain Res 2005; 150: 495–511. doi: 10.1016/S0079-6123(05)50034-7. PMID: 16186044.
  36. Laureys S., Goldman S., Phillips C. et al. Impaired effective cortical connectivity in vegetative state. NeuroImage 1999; 9: 377–382. doi: 10.1006/nimg.1998.0414. PMID: 10191166.
  37. Lull N., Noé E., Lull J. et al. Voxel-based statistical analysis of thalamic glucose metabolism in traumatic brain injury: relationship with consciousness and cognition.
  38. Brain Inj 2010; 24: 1098–1107. doi: 10.3109/02699052.2010.494592 PMID: 20597637
  39. Vogt B.A., Laureys S. Posterior cingulate, precuneal and retrosplenial cortices: cytology and components of the neural network correlates of consciousness. Prog Brain Res 2005; 150 :205–217. doi: 10.1016/S0079-6123(05)50015-3. PMID: 16186025.
  40. Laureys S., Antoine S., Boly M. et al. Brain function in the vegetative state. Acta Neurol Belg 2002; 102(4): 177–185. PMID: 12534245.
  41. Laureys S. The neural correlate of (un)awareness: lessons from the vegetative state. Trends Cogn Sci 2005; 9(12): 556–559. doi: 10.1016/j.tics.2005.10.010. PMID: 16271507.
  42. The Neurology of Consciousness. 2nd Edition. Laureys S., Gosseries J., Tononi G. (eds). Academic Press, 2015. 488 p.
  43. Schiff ND. Recovery of consciousness after brain injury: a mesocircuit hypothesis. Trends Neurosci 2010; 33(1): 1–9. doi: 10.1016/j.tins.2009.11.002. PMID: 19954851.
  44. Laureys S., Faymonville M.E., Luxen A. et al. Restoration of thalamocortical connectivity after recovery from persistent vegetative state. Lancet 2000; 355:1790–1791. PMID: 10832834.
  45. Piradov M.A., Tanashyan M.M., Krotenkova M.V et al. [Advanced non-visualization technology] Annals of clinical and experimental neurology 2015; 9(4):11–18. (In Russ.)
  46. Bruno M.A., Boly M., Vanhaudenhuyse A. Functional neuroanatomy underlying the clinical subcategorization of minimally conscious state patients. J Neurol 2012 259:1087–1098. doi: 10.1007/s00415-011-6303-7. PMID: 22081100.
  47. Laureys S., Schiff N.D. Coma and consciousness: paradigms (re)framed by neuroimaging. Neuroimage 2012; 61: 478–491. doi: 10.1016/j.neuroimage. 2011.12.041. PMID: 22227888.
  48. Di H., Boly M., Weng X. et al. Neuroimaging activation studies in the vegetative state: predictors of recovery? Clin Med (Lond) 2008; 8(5): 502-507. PMID: 18975482.
  49. Monti M.M., Vanhaudenhuyse A., Coleman M.R. et al. Willful modulation of brain activity in disorders of consciousness. N Engl J Med 2010; 362: 579–589. doi: 10.1056/NEJMoa0905370. PMID: 20130250.
  50. Owen A.M., Coleman M.R., Boly M. et al. Detecting awareness in the vegetative state. Science 2006; 313 (5792): 1402. PMID: 16959998.
  51. Piradov M.A., Suponeva N.A., Seliverstov Yu.A. et al. [Possibilities of modern non-visualization methods in the study of spontaneous activity of the brain at rest] Nevrologicheskiy zhurnal 2016; 21(1): 4–12. (In Russ.)
  52. Guldenmund P., Vanhaudenhuyse A., Boly M. et al. A default mode of brain function in altered states of consciousness. Arch Ital Biol 2012; 150: 107–121. doi: 10.4449/aib.v150i2.1373. PMID: 23165872.
  53. Demertzi A., Soddu A., Laureys S. Consciousness supporting networks. Curr Opin Neurobiol 2013; 23: 239–244. doi: 10.1016/j.conb.2012.12.003.PMID: 23273731.
  54. Vanhaudenhuyse A., Noirhomme Q., Tshibanda L.J. et al. Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain 133, 161–171 (2010). doi: 10.1093/brain/awp313 PMID: 2003492.
  55. Demertzi, A., Antonopoulos, G., Heine, L. et al. Intrinsic functional connectivity differentiates minimally conscious from unresponsive patients. Brain 2015; 138(Pt 9): 2619–2631. doi: 10.1093/brain/awv169. PMID: 26117367.
  56. Rosazza C., Andronache A., Sattin D. et al. Multimodal study of default-mode network integrity in disorders of consciousness. Ann Neurol 2016; 79(5): 841–853. doi: 10.1002/ana.24634. PMID: 26970235.
  57. Vanhaudenhuyse A., Demertzi A., Schabus M. et al. Two Distinct Neuronal Networks Mediate the Awareness of Environment and of Self. J Cogn Neurosci 2011; 23(3): 570-578. doi: 10.1162/jocn.2010.21488. PMID: 20515407
  58. Boly M., Phillips C., Tshibanda L. et al. Intrinsic brain activity in altered states of consciousness: how conscious is the default mode of brain function? Ann N Y Acad Sci 2008; 1129:119–129. doi: 10.1196/annals.1417.015. PMID: 18591474.
  59. Thibaut A., Bruno M.A., Chatelle C. et al. Metabolic activity in external and internal awareness networks in severely brain-damaged patients. J Rehab Med 2012; 44(6): 487–494. doi: 10.2340/16501977-0940. PMID: 22366927.
  60. Demertzi A., Gomez F., Crone J. S. et al. Multiple fMRI system-level baseline connectivity is disrupted in patients with consciousness alterations. Cortex 2014; 52: 35–46. doi: 10.1016/j.cortex.2013.11.005. PMID: 24480455.
  61. Wu X., Zou Q., Hu J. et al. Intrinsic functional connectivity patterns predict onsciousness level and recovery outcome in acquired brain injury. J Neurosci 2015; 35(37): 12932–12946. doi: 10.1523/JNEUROSCI.0415-15.2015. PMID: 26377477.
  62. Sinitsyn D.O., Legostaeva L.A., Kremneva E.I. et al. Degrees of functional connectome abnormality in disorders of consciousness. Hum Brain Mapp 2018; 10: 1–12. doi: 10.1002/hbm.24050. PMID: 29575425.
  63. Giacino J.T., Fins J.J., Laureys S., Schiff N.D. Disorders of consciousness after acquired brain injury: the state of the science. Nat Rev Neurol 2014; 10(2): 99–114. doi: 10.1038/nrneurol.2013.279. PMID: 24468878.
  64. Gnezditskiy V.V., Piradov M.A. Neyrofiziologiya komy i narusheniya soznaniya (Analiz i interpretatsiya klinicheskikh nablyudeniy). [Neurophysiology of coma and impairment of consciousness (Analysis and interpretation of clinical observations)]. Ivanovo: PresSto; 2015 (In Russ.)
  65. Estraneo A., Loreto V., Guarino I. et al. Standard EEG in diagnostic process of prolonged disorders of consciousness. Clin Neurophysiol 2016; 127: 2379–2385. doi: 10.1016/j.clinph.2016.03.021. PMID: 27178856.
  66. Forgacs P.B., Conte M.M., Fridman E.A. et al. Preservation of electroencephalographic organization in patients with impaired consciousness and imaging-based evidence of command-following. Ann Neurol 2014; 76(6): 869–79. doi: 10.1002/ana.24283. PMID: 2527003.
  67. Cologan V., Drouot X., Parapatics S. et al. Sleep in the unresponsive wakefulness syndrome and minimally conscious state. J Neurotrauma 2013; 30: 339–346. doi: 10.1089/neu.2012.2654. PMID: 23121471.
  68. Landsness E., Bruno M.A., Noirhomme Q. et al. Electrophysiological correlates of behavioural changes in vigilance in vegetative state and minimally conscious state. Brain 2011; 134: 2222–2232. doi: 10.1093/brain/awr152. PMID: 21841201.
  69. Kotchoubey B., Lang S., Mezger G. et al. Information processing in severe disorders of consciousness: vegetative state and minimally conscious state. Clin Neurophysiol 2005; 116(10): 2441–2453. doi: 10.1016/j.clinph.2005.03.028. PMID: 16002333.
  70. Schnakers C., Perrin F., Schabus M. et al. Voluntary brain processing in disorders of consciousness. Neurology 2008; 71: 1614–1620. doi: 10.1212/01.wnl.0000334754.15330.69. PMID: 19001251.
  71. Chennu S., Finoia P., Kamau E. et al. Dissociable endogenous and exogenous attention in disorders of consciousness. Neuroimage Clin 2013; 3: 450–461.
  72. Faugeras F., Rohaut B., Weiss N. et al. Probing consciousness with event-related potentials in the vegetative state. Neurology 2011; 77(3): 264–268. doi: 10.1212/WNL.0b013e3182217ee8. PMID: 21593438.
  73. Ilmoniemi R.J., Kičić D. Methodology for combined TMS and EEG. Brain Topogr 2010; 22 (4): 233–248. PMID: 20012350.
  74. Chervyakov A.V., Piradov M.A., Savitskaya N.G. et al. [New step to personalized medicine. Transcranial Magnetic Stimulation Navigation System (NBS EXIMIA N・EXSTIM)] Annals of clinical and experimental neurology 2012; 6(3): 37-46. (In Russ.)
  75. Casali A.G., 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. doi: 10.1126/scitranslmed.3006294. PMID: 23946194.
  76. Sarasso S., Rosanova M., Casali A.G. et al. Quantifying Cortical EEG Responses to TMS in (un)consciousness. Clin EEG Neurosci 2014; 45 (1): 40–49. doi: 10.1177/1550059413513723. PMID: 24403317.
  77. Tononi G. Integrated information theory of consciousness: an updated account. Arch Ital Biol 2012; 150 (4): 293–329. PMID: 23802335.
  78. Casarotto S., Comanducci A., Rosanova M. et al. Stratification of unresponsive patients by an independently validated index of brain complexity. Ann Neurol 2016; 80(5): 718–729. doi: 10.1002/ana.24779. PMID: 27717082.
  79. Legostaeva L., Mochalova E., Poydasheva A. et al. Feasibility of individual diagnostic approach for patients with chronic disorders of counsciousness. Eur J Neurol 2017; 22 (S1): 147.
  80. Legostaeva L.A., Zmeykina E.A., Poydasheva A.G. et al. A new approach to the study of consciousness from the theory of integrated information point of view. Sovrem Tehnol v Med 2016; 8 (4): 251–258.
  81. Dehaene S., Changeux J.P. Experimental and theoretical approaches to conscious processing. Neuron. 2011;70(2): 200-27. doi: 10.1016/j.neuron. 2011.03.018. PMID: 21521609. doi: 10.1016/j.nicl.2013.10.008. PMID: 24273727.

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Copyright (c) 2018 Piradov M.A., Suponeva N.A., Sergeev D.V., Chervyakov A.V., Ryabinkina Y.V., Sinitsyn D.O., Poydasheva A.G., Kremneva E.I., Morozova S.N., Iazeva E.G., Legostaeva L.A.

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