Advertisement

What Can We Learn About Brain Functions from Sleep EEG? Insights from Sleep of DOC Patients

  • Malgorzata Wislowska
  • Manuel SchabusEmail author
Chapter

Abstract

Disorder of Consciousness (DOC) patients are often reported to have alterations in sleep architecture and sleep-specific graphoelements. The reappearance of non-REM oscillatory patterns such as sleep spindles has been associated with diagnosis and presumably prognosis.

The study of sleep is of particular interest in DOC research as it might allow identifying lesioned neuronal tissue linked to specific sleep graphoelements. The presence of REM, for example, may reflect residual functioning of brainstem nuclei including pons and adjacent portions of the midbrain. On the other hand, the absence of circadian functioning, or sleep-wake cycles, has been associated with brainstem dysfunction and might be informative for hypothalamic and SCN alterations. Interestingly, the systematic work on sleep and circadian functioning in the various DOC states is still scarce. Most strikingly, there are no accepted criteria which allow to reliably classify sleep stages in these patients. In addition, there is very little knowledge whether sleep in DOC is still under normal circadian and homeostatic control. Without a doubt, studying sleep in DOC is a challenging endeavor, and long-term polysomnography (PSG) of DOC patients is difficult for many reasons, among which are ubiquitous artifacts present in the data recordings or PSG alterations which often come with pharmacological treatment.

Altogether, the characterization of sleep and its relationships with arousal, homeostasis, and circadian rhythmicity is, in our view, essential in order to better understand the various DOC states and might offer complementary diagnostic and prognostic information or even guide the direction of future treatment attempts.

Keywords

Polysomnography (PSG) Electroencephalography (EEG) Circadian rhythm Sleep Disorders of consciousness (DOC) Coma Unresponsive wakefulness state (UWS) Minimally conscious state (MCS) Locked-in syndrome (LIS) 

References

  1. 1.
    Giacino JT, Ashwal S, Childs N, Cranford R, Jennett B, Katz DI, et al. The minimally conscious state: definition and diagnostic criteria. Neurology. 2002;58(3):349–53.CrossRefPubMedGoogle Scholar
  2. 2.
    Brenner RP. The interpretation of the EEG in stupor and coma. Neurologist. 2005;11(5):271–84.CrossRefPubMedGoogle Scholar
  3. 3.
    Hansotia P, Gottschalk P, Green P, Zais D. Spindle coma: incidence, clinicopathologic correlates, and prognostic value. Neurology. 1981;31(1):83–7.CrossRefPubMedGoogle Scholar
  4. 4.
    Monti MM, Laureys S, Owen AM. The vegetative state. BMJ. 2010;341:c3765.CrossRefPubMedGoogle Scholar
  5. 5.
    Bruno M-A, Gosseries O, Ledoux D, Hustinx R, Laureys S. Assessment of consciousness with electrophysiological and neurological imaging techniques. Curr Opin Crit Care. 2011;17(2):146–51.CrossRefPubMedGoogle Scholar
  6. 6.
    Berry R, Brooks R, Gamaldo C. The AASM Manual for the scoring of sleep and associated events: rules, terminology and technical specifications. Version 2.0. Darien: American Academy of Sleep Medicine; 2012.Google Scholar
  7. 7.
    Cologan V, Schabus M, Ledoux D, Moonen G, Maquet P, Laureys S. Sleep in disorders of consciousness. Sleep Med Rev. 2010;14(2):97–105.CrossRefPubMedGoogle Scholar
  8. 8.
    Bekinschtein T, Cologan V, Dahmen B, Golombek D. You are only coming through in waves: wakefulness variability and assessment in patients with impaired consciousness. Prog Brain Res. 2009;177:171–89.CrossRefPubMedGoogle Scholar
  9. 9.
    Schabus M, Hödlmoser K, Gruber G, Sauter C, Anderer P, Klösch G, et al. Sleep spindle-related activity in the human EEG and its relation to general cognitive and learning abilities. Eur J Neurosci. 2006;23(7):1738–46.CrossRefPubMedGoogle Scholar
  10. 10.
    Bodizs R, Kis T, Lazar AS, Havran L, Rigo P, Clemens Z, et al. Prediction of general mental ability based on neural oscillation measures of sleep. J Sleep Res. 2005;14(3):285–92.CrossRefPubMedGoogle Scholar
  11. 11.
    Dang-Vu TT, Schabus M, Desseilles M, Albouy G, Boly M, Darsaud A, et al. Spontaneous neural activity during human slow wave sleep. Proc Natl Acad Sci U S A. 2008;105(39):15160–5.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Cologan V, Drouot X, Parapatics S, Delorme A, Gruber G, Moonen G, et al. Sleep in the unresponsive wakefulness syndrome and minimally conscious state. J Neurotrauma. 2013;30(5):339–46.CrossRefPubMedGoogle Scholar
  13. 13.
    Mundigler G, Delle-Karth G, Koreny M, Zehetgruber M, Steindl-Munda P, Marktl W, et al. Impaired circadian rhythm of melatonin secretion in sedated critically ill patients with severe sepsis. Crit Care Med. 2002;30(3):536–40.CrossRefPubMedGoogle Scholar
  14. 14.
    Guaraldi P, Sancisi E, La Morgia C, Calandra-Buonaura G, Carelli V, Cameli O, et al. Nocturnal melatonin regulation in post-traumatic vegetative state: a possible role for melatonin supplementation? Chronobiol Int. 2014;31(5):741–5.CrossRefPubMedGoogle Scholar
  15. 15.
    De Weer AS, Da Ros M, Berre J, Melot C, Goldman S, Peigneux P. Environmental influences on activity patterns in altered states of consciousness. Eur J Neurol. 2011;18(12):432–4.Google Scholar
  16. 16.
    Cruse D, Thibaut A, Demertzi A, Nantes JC, Bruno M-A, Gosseries O, et al. Actigraphy assessments of circadian sleep-wake cycles in the Vegetative and Minimally Conscious States. BMC Med. 2013;11(1):18.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Isono M, Wakabayashi Y, Fujiki MM, Kamida T, Kobayashi H. Sleep cycle in patients in a state of permanent unconsciousness. Brain Inj. 2002;16(8):705–12.CrossRefPubMedGoogle Scholar
  18. 18.
    de Biase S, Gigli GL, Lorenzut S, Bianconi C, Sfreddo P, Rossato G, et al. The importance of polysomnography in the evaluation of prolonged disorders of consciousness: sleep recordings more adequately correlate than stimulus-related evoked potentials with patients’ clinical status. Sleep Med. 2014;15(4):393–400.CrossRefPubMedGoogle Scholar
  19. 19.
    Pattoneri P, Tirabassi G, Pela G, Astorri E, Mazzucchi A, Borghetti A. Circadian blood pressure and heart rate changes in patients in a persistent vegetative state after traumatic brain injury. J Clin Hypertens (Greenwich). 2005;7(12):734–9.CrossRefGoogle Scholar
  20. 20.
    Fukudome Y, Abe I, Saku Y, Matsumura K, Sadoshima S, Utunomiya H, et al. Circadian blood pressure in patients in a persistent vegetative state. Am J Phys. 1996;270(5 Pt 2):R1109–14.Google Scholar
  21. 21.
    Bekinschtein TA, Golombek DA, Simonetta SH, Coleman MR, Manes FF. Circadian rhythms in the vegetative state. Brain Inj. 2009;23(11):915–9.CrossRefPubMedGoogle Scholar
  22. 22.
    Parthasarathy S, Tobin MJ. Sleep in the intensive care unit. Intensive Care Med. 2004;30(2):197–206.CrossRefPubMedGoogle Scholar
  23. 23.
    Chatrian GE, White Jr LE, Daly D. Electroencephalographic patterns resembling those of sleep in certain comatose states after injuries to the head. Electroencephalogr Clin Neurophysiol. 1963;15:272–80.CrossRefPubMedGoogle Scholar
  24. 24.
    Oksenberg A, Gordon C, Arons E, Sazbon L. Phasic activities of rapid eye movement sleep in vegetative state patients. Sleep. 2001;24(6):703–6.CrossRefPubMedGoogle Scholar
  25. 25.
    Valente M, Placidi F, Oliveira AJ, Bigagli A, Morghen I, Proietti R, et al. Sleep organization pattern as a prognostic marker at the subacute stage of post-traumatic coma. Clin Neurophysiol. 2002;113(11):1798–805.CrossRefPubMedGoogle Scholar
  26. 26.
    Ouellet MC, Savard J, Morin CM. Insomnia following traumatic brain injury: a review. Neurorehabil Neural Repair. 2004;18(4):187–98.CrossRefPubMedGoogle Scholar
  27. 27.
    Evans BM. What does brain damage tell us about the mechanisms of sleep? J R Soc Med. 2002;95(12):591–7.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Giubilei F, Formisano R, Fiorini M, Vitale A, Faroni J, Toni D, et al. Sleep abnormalities in traumatic apallic syndrome. J Neurol Neurosurg Psychiatry. 1995;58(4):484–6.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    D’Aleo G, Bramanti P, Silvestri R, Saltuari L, Gerstenbrand F, Di Perri R. Sleep spindles in the initial stages of the vegetative state. Ital J Neurol Sci. 1994;15(7):347–51.CrossRefPubMedGoogle Scholar
  30. 30.
    D’Aleo G, Saltuari L, Gerstenbrand F, Bramanti P. Sleep in the last remission stages of vegetative state of traumatic nature. Funct Neurol. 1994;9(4):189–92.PubMedGoogle Scholar
  31. 31.
    Landsness E, Bruno MA, Noirhomme Q, Riedner B, Gosseries O, Schnakers C, et al. Electrophysiological correlates of behavioural changes in vigilance in vegetative state and minimally conscious state. Brain. 2011;134(Pt 8):2222–32.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Aricò I, Naro A, Pisani LR, Leo A, Muscarà N, De Salvo S, et al. Could combined sleep and pain evaluation be useful in the diagnosis of disorders of consciousness (DOC)? Preliminary findings. Brain Inj. 2016;30(2):159–63.CrossRefPubMedGoogle Scholar
  33. 33.
    Malinowska U, Chatelle C, Bruno M-A, Noirhomme Q, Laureys S, Durka PJ. Electroencephalographic profiles for differentiation of disorders of consciousness. Biomed Eng Online. 2013;12(1):109.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Forgacs PB, Conte MM, Fridman EA, Voss HU, Victor JD, Schiff ND. Preservation of electroencephalographic organization in patients with impaired consciousness and imaging-based evidence of command-following. Ann Neurol. 2014;76(6):869–79.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Kang X, Li L, Wei D, Xu X, Zhao R, Jing Y, et al. Development of a simple score to predict outcome for unresponsive wakefulness syndrome. Crit Care. 2014;18:R37.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Oksenberg A, Soroker N, Solzi P, Reider-Groswasser I. Polysomnography in locked-in syndrome. Electroencephalogr Clin Neurophysiol. 1991;78(4):314–7.CrossRefPubMedGoogle Scholar
  37. 37.
    Guilleminault C, Cathala JP, Castaigne P. Effects of 5-hydroxytryptophan on sleep of a patient with a brain-stem lesion. Electroencephalogr Clin Neurophysiol. 1973;34(2):177–84.CrossRefPubMedGoogle Scholar
  38. 38.
    Markand ON, Dyken ML. Sleep abnormalities in patients with brain stem lesions. Neurology. 1976;26(8):769–76.CrossRefPubMedGoogle Scholar
  39. 39.
    Cummings JL, Greenberg R. Sleep patterns in the “locked-in” syndrome. Electroencephalogr Clin Neurophysiol. 1977;43(2):270–1.CrossRefPubMedGoogle Scholar
  40. 40.
    Freemon FR, Salinas-Garcia RF, Ward JW. Sleep patterns in a patient with a brain stem infarction involving the raphe nucleus. Electroencephalogr Clin Neurophysiol. 1974;36(6):657–60.CrossRefPubMedGoogle Scholar
  41. 41.
    Autret A, Laffont F, de Toffol B, Cathala HP. A syndrome of REM and non-REM sleep reduction and lateral gaze paresis after medial tegmental pontine stroke. Computed tomographic scans and anatomical correlations in four patients. Arch Neurol. 1988;45(11):1236–42.CrossRefPubMedGoogle Scholar
  42. 42.
    Tamura K, Karacan I, Williams RL, Meyer JS. Disturbances of the sleep-waking cycle in patients with vascular brain stem lesions. Clin Electroencephalogr. 1983;14(1):35–46.CrossRefPubMedGoogle Scholar
  43. 43.
    Lavie P, Pratt H, Scharf B, Peled R, Brown J. Localized pontine lesion: nearly total absence of REM sleep. Neurology. 1984;34(1):118–20.CrossRefPubMedGoogle Scholar
  44. 44.
    Cabello B, Thille A-W, Mancebo J. Sommeil en réanimation. Réanimation. 2007;16(1):61–6.CrossRefGoogle Scholar
  45. 45.
    Diekelmann S, Born J. The memory function of sleep. Nat Rev Neurosci. 2010;11(2):114–26.PubMedGoogle Scholar
  46. 46.
    Hobson JA. Sleep is of the brain, by the brain and for the brain. Nature. 2005;437(7063):1254–6.CrossRefPubMedGoogle Scholar
  47. 47.
    Sejnowski TJ, Destexhe A. Why do we sleep? Brain Res. 2000;886(1–2):208–23.CrossRefPubMedGoogle Scholar
  48. 48.
    Morawska MM, Büchele F, Moreira CG, Imbach LL, Noain D, Baumann CR. Sleep modulation alleviates axonal damage and cognitive decline after rodent traumatic brain injury. J Neurosci. 2016;36(12):3422–9.CrossRefPubMedGoogle Scholar
  49. 49.
    George B, Landau-Ferey J. Twelve months’ follow-up by night sleep EEG after recovery from severe head trauma. Neurochirurgia (Stuttg). 1986;29(2):45–7.Google Scholar
  50. 50.
    Keshavan MS, Channabasavanna SM, Reddy GN. Post-traumatic psychiatric disturbances: patterns and predictors of outcome. Br J Psychiatry. 1981;138:157–60.CrossRefPubMedGoogle Scholar
  51. 51.
    Cohen M, Oksenberg A, Snir D, Stern MJ, Groswasser Z. Temporally related changes of sleep complaints in traumatic brain injured patients. J Neurol Neurosurg Psychiatry. 1992;55(4):313–5.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Clinchot DM, Bogner J, Mysiw WJ, Fugate L, Corrigan J. Defining sleep disturbance after brain injury. Am J Phys Med Rehabil. 1998;77(4):291–5.CrossRefPubMedGoogle Scholar
  53. 53.
    Fichtenberg NL, Zafonte RD, Putnam S, Mann NR, Millard AE. Insomnia in a post-acute brain injury sample. Brain Inj. 2002;16(3):197–206.CrossRefPubMedGoogle Scholar
  54. 54.
    Guilleminault C, Yuen KM, Gulevich MG, Karadeniz D, Leger D, Philip P. Hypersomnia after head-neck trauma: a medicolegal dilemma. Neurology. 2000;54(3):653–9.CrossRefPubMedGoogle Scholar
  55. 55.
    Masel BE, Scheibel RS, Kimbark T, Kuna ST. Excessive daytime sleepiness in adults with brain injuries. Arch Phys Med Rehabil. 2001;82(11):1526–32.CrossRefPubMedGoogle Scholar
  56. 56.
    Ouellet MC, Morin CM. Subjective and objective measures of insomnia in the context of traumatic brain injury: a preliminary study. Sleep Med. 2006;7(6):486–97.CrossRefPubMedGoogle Scholar
  57. 57.
    Ouellet MC, Beaulieu-Bonneau S, Morin CM. Insomnia in patients with traumatic brain injury: frequency, characteristics, and risk factors. J Head Trauma Rehabil. 2006;21(3):199–212.CrossRefPubMedGoogle Scholar
  58. 58.
    Hoedlmoser K, Dang-Vu TT, Desseilles M, Schabus M. Non-pharmacological alternatives for the treatment of insomnia—instrumental EEG conditioning, a new alternative? In: Soriento YE, editor. Melatonin, sleep and insomnia. New York: Nova Science; 2011.Google Scholar
  59. 59.
    Schabus M, Heib DP, Lechinger J, Griessenberger H, Klimesch W, Pawlizki A, et al. Enhancing sleep quality and memory in insomnia using instrumental sensorimotor rhythm conditioning. Biol Psychol. 2014;95:126–34.CrossRefPubMedGoogle Scholar
  60. 60.
    Massengale JP. The role of nursing practice in promoting sleep during brain injury rehabilitation hospitalization. Minneapolis: Walden University; 2015.Google Scholar
  61. 61.
    Bergamasco B, Bergamini L, Doriguzzi T, Sacerdote I. The sleep cycle in coma: prognostic value. Electroencephalogr Clin Neurophysiol. 1968;25(1):87.PubMedGoogle Scholar
  62. 62.
    Ron S, Algom D, Hary D, Cohen M. Time-related changes in the distribution of sleep stages in brain injured patients. Electroencephalogr Clin Neurophysiol. 1980;48(4):432–41.CrossRefPubMedGoogle Scholar
  63. 63.
    Evans BM, Bartlett JR. Prediction of outcome in severe head injury based on recognition of sleep related activity in the polygraphic electroencephalogram. J Neurol Neurosurg Psychiatry. 1995;59(1):17–25.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Arnaldi D, Terzaghi M, Cremascoli R, De Carli F, Maggioni G, Pistarini C, et al. The prognostic value of sleep patterns in disorders of consciousness in the sub-acute phase. Clin Neurophysiol. 2016;127(2):1445–51.CrossRefPubMedGoogle Scholar
  65. 65.
    Sebastiano DR, Panzica F, Visani E, Rotondi F, Scaioli V, Leonardi M, et al. Significance of multiple neurophysiological measures in patients with chronic disorders of consciousness. Clin Neurophysiol. 2015;126(3):558–64.CrossRefGoogle Scholar
  66. 66.
    Avantaggiato P, Molteni E, Formica F, Gigli GL, Valente M, Lorenzut S, et al. Polysomnographic sleep patterns in children and adolescents in unresponsive wakefulness syndrome. J Head Trauma Rehabil. 2015;30(5):334–46.CrossRefPubMedGoogle Scholar
  67. 67.
    Schabus M, Dang-Vu TT, Albouy G, Balteau E, Boly M, Carrier J, et al. Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc Natl Acad Sci U S A. 2007;104(32):13164–9.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Britt Jr CW, Raso E, Gerson LP. Spindle coma, secondary to primary traumatic midbrain hemorrhage. Electroencephalogr Clin Neurophysiol. 1980;49(3–4):406–8.CrossRefPubMedGoogle Scholar
  69. 69.
    Britt Jr CW. Nontraumatic “spindle coma”: clinical, EEG, and prognostic features. Neurology. 1981;31(4):393–7.CrossRefPubMedGoogle Scholar
  70. 70.
    Seet RC, Lim EC, Wilder-Smith EP. Spindle coma from acute midbrain infarction. Neurology. 2005;64(12):2159–60.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  1. 1.Laboratory for Sleep, Cognition and Consciousness Research, Department of PsychologyUniversity of SalzburgSalzburgAustria
  2. 2.Centre for Cognitive Neuroscience Salzburg (CCNS)SalzburgAustria

Personalised recommendations