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24-h polysomnographic recordings and electrophysiological spectral analyses from a cohort of patients with chronic disorders of consciousness

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Abstract

Fourteen patients with severe brain injuries and chronic disorders of consciousness underwent polysomnographic recordings for a 24-h period. Their electrophysiological data were scored using a modified sleep staging system employed in a previous study of similar patients (J Head Trauma Rehabil 30:334–346, 2015). In addition to sleep scoring, the patients’ data were compared with a sample of approximately age-matched healthy volunteers in the spectral domain. All patients demonstrated some form of a sleep–wake cycle; however, the integrity of normal sleep features was remarkably heterogenous across individuals, and in some cases, sleep was significantly impoverished. In three patients, these cycles were biphasic and comprised of only alternating periods of wakefulness and sleep-like electrophysiological activity. Two patients demonstrated a sleep–wake cycle that included all sleep stages aside from non-REM stage 3, and another two patients demonstrated a sleep–wake cycle that included all sleep stages aside from REM sleep. The remaining seven patients, which included patients diagnosed as being in a minimally conscious state and patients diagnosed as being in a vegetative state (unresponsive wakefulness syndrome), demonstrated full sleep architecture, including k-complexes, REMs, and slow wave sleep. However, three of the patients with full sleep architecture did not generate sleep spindles. Altogether, these findings highlight the heterogeneity of brain function among patients with disorders of consciousness, regardless of their diagnostic category. Polysomnography is a useful tool to complement other behavioural and physiological assessments that characterize the abilities of each patient.

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References

  1. Bernat JL (2006) Chronic disorders of consciousness. Lancet 367:1181–1192. https://doi.org/10.1016/S0140-6736(06)68508-5

    Article  PubMed  Google Scholar 

  2. Laureys S, Celesia GG, Cohadon F et al (2010) Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med 8:68. https://doi.org/10.1186/1741-7015-8-68

    Article  PubMed  PubMed Central  Google Scholar 

  3. Giacino JT, Ashwal S, Childs NL et al (2002) The minimally conscious state: definition and diagnostic criteria. Neurology 58:349–353. https://doi.org/10.1212/WNL.58.3.349

    Article  PubMed  Google Scholar 

  4. Moruzzi G, Magoun HW (1949) Brain stem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol 1:455–473

    Article  CAS  Google Scholar 

  5. Plum F, Posner JB (1972) The diagnosis of stupor and coma. Contemp Neurol Ser 10:1–286

    CAS  PubMed  Google Scholar 

  6. Tononi G (2012) Integrated information theory of consciousness: an updated account. Arch Ital Biol 150:293–329. https://doi.org/10.4449/aib.v149i5.1388

    Article  CAS  PubMed  Google Scholar 

  7. Hobson JA (2009) REM sleep and dreaming: towards a theory of protoconsciousness. Nat Rev Neurosci 10:803–813. https://doi.org/10.1038/nrn2716

    Article  CAS  PubMed  Google Scholar 

  8. Brown RE, Basheer R, McKenna JT et al (2012) Control of sleep and wakefulness. Physiol Rev 92:1087–1187. https://doi.org/10.1152/physrev.00032.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Parvizi J, Damasio AR (2003) Neuroanatomical correlates of brainstem coma. Brain 126:1524–1536. https://doi.org/10.1093/brain/awg166

    Article  Google Scholar 

  10. Koch C, Massimini M, Boly M, Tononi G (2016) Neural correlates of consciousness: progress and problems. Nat Rev Neurosci 17:307–321. https://doi.org/10.1038/nrn.2016.22

    Article  CAS  PubMed  Google Scholar 

  11. Siclari F, Larocque JJ, Postle BR, Tononi G (2013) Assessing sleep consciousness within subjects using a serial awakening paradigm. Front Psychol 4:542. https://doi.org/10.3389/fpsyg.2013.00542

    Article  PubMed  PubMed Central  Google Scholar 

  12. Hobson JA, Pace-Schott EF (2002) The cognitive neuroscience of sleep: neuronal systems, consciousness and learning. Nat Rev Neurosci 3:679–693. https://doi.org/10.1038/nrn915

    Article  CAS  Google Scholar 

  13. Chaput J-P (2014) Sleep patterns, diet quality and energy balance. Physiol Behav 134:86–91. https://doi.org/10.1016/j.physbeh.2013.09.006

    Article  CAS  PubMed  Google Scholar 

  14. Sofi F, Cesari F, Casini A et al (2012) Insomnia and risk of cardiovascular disease: a meta-analysis. Eur J Prev Cardiol 21:57–64. https://doi.org/10.1177/2047487312460020

    Article  PubMed  Google Scholar 

  15. Tsuno N, Besset A, Ritchie K (2005) Sleep and depression. J Clin Psychiatry 66:1254–1269. https://doi.org/10.4088/JCP.v66n1008

    Article  PubMed  Google Scholar 

  16. De Biase S, Gigli GL, Lorenzut S et al (2014) 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 15:393–400. https://doi.org/10.1016/j.sleep.2013.09.026

    Article  PubMed  Google Scholar 

  17. Landsness E, Bruno M-A, Noirhomme Q et al (2011) Electrophysiological correlates of behavioural changes in vigilance in vegetative state and minimally conscious state. Brain 134:2222–2232. https://doi.org/10.1093/brain/awr152

    Article  PubMed  PubMed Central  Google Scholar 

  18. Wislowska M, Del Giudice R, Lechinger J et al (2017) Night and day variations of sleep in patients with disorders of consciousness. Sci Rep 7:1–11. https://doi.org/10.1038/s41598-017-00323-4

    Article  CAS  Google Scholar 

  19. Rossi Sebastiano D, Panzica F, Visani E et al (2015) Significance of multiple neurophysiological measures in patients with chronic disorders of consciousness. Clin Neurophysiol 126:558–564. https://doi.org/10.1016/j.clinph.2014.07.004

    Article  PubMed  Google Scholar 

  20. Mouthon A-L, van Hedel HJA, Meyer-Heim A et al (2016) High-density electroencephalographic recordings during sleep in children with disorders of consciousness. NeuroImage Clin 11:468–475. https://doi.org/10.1016/j.nicl.2016.03.012

    Article  PubMed  PubMed Central  Google Scholar 

  21. Lanteri P, Corica A, Bianconi C et al (2010) Sleep homeostasis in the vegetative and minimally conscious states. J Psychophysiol 24:120–124. https://doi.org/10.1027/0269-8803/a000022

    Article  Google Scholar 

  22. Matsumoto M, Sugama J, Nemoto T et al (2015) The nature of sleep in 10 bedridden elderly patients with disorders of consciousness in a Japanese hospital. Biol Res Nurs 17:13–20. https://doi.org/10.1177/1099800414523118

    Article  PubMed  Google Scholar 

  23. Rossi Sebastiano D, Visani E, Panzica F et al (2018) Sleep patterns associated with the severity of impairment in a large cohort of patients with chronic disorders of consciousness. Clin Neurophysiol 129:687–693. https://doi.org/10.1016/j.clinph.2017.12.012

    Article  PubMed  Google Scholar 

  24. Matsumoto M, Sugama J, Okuwa M et al (2013) Non-invasive monitoring of core body temperature rhythms over 72 h in 10 bedridden elderly patients with disorders of consciousness in a Japanese hospital: a pilot study. Arch Gerontol Geriatr 57:428–432. https://doi.org/10.1016/j.archger.2013.05.009

    Article  PubMed  Google Scholar 

  25. Blume C, Lechinger J, Santhi N et al (2017) Significance of circadian rhythms in severely brain-injured patients. Neurology 88:1933–1941. https://doi.org/10.1212/WNL.0000000000003942

    Article  PubMed  PubMed Central  Google Scholar 

  26. Cruse D, Thibaut A, Demertzi A et al (2013) Actigraphy assessments of circadian sleep–wake cycles in the vegetative and minimally conscious states. BMC Med 11:18. https://doi.org/10.1186/1741-7015-11-18

    Article  PubMed  PubMed Central  Google Scholar 

  27. Bekinschtein TA, Golombek DA, Simonetta SH et al (2009) Circadian rhythms in the vegetative state. Brain Inj 23:915–919. https://doi.org/10.1080/02699050903283197

    Article  CAS  PubMed  Google Scholar 

  28. Cologan V, Schabus M, Ledoux D et al (2010) Sleep in disorders of consciousness. Sleep Med Rev 14:97–105. https://doi.org/10.1016/j.smrv.2009.04.003

    Article  PubMed  Google Scholar 

  29. Chéliout-Heraut F, Rubinsztajn R, Ioos C, Estournet B (2001) Prognostic value of evoked potentials and sleep recordings in the prolonged comatose state of children. Preliminary data. Neurophysiol Clin 31:283–292. https://doi.org/10.1016/S0987-7053(01)00270-2

    Article  PubMed  Google Scholar 

  30. Arnaldi D, Terzaghi M, Cremascoli R et al (2016) The prognostic value of sleep patterns in disorders of consciousness in the sub-acute phase. Clin Neurophysiol 127:1445–1451. https://doi.org/10.1016/j.clinph.2015.10.042

    Article  PubMed  Google Scholar 

  31. Wielek T, Lechinger J, Wislowska M et al (2018) Sleep in patients with disorders of consciousness characterized by means of machine learning. PLoS ONE 13:1–14. https://doi.org/10.1371/journal.pone.0190458

    Article  CAS  Google Scholar 

  32. Malinowska CC, Bruno M-A et al (2013) Electroencephalographic profiles for differentiation of disorders of consciousness. Biomed Eng Online 12:109. https://doi.org/10.1186/1475-925X-12-109

    Article  PubMed  PubMed Central  Google Scholar 

  33. Avantaggiato P, Molteni E, Formica F et al (2015) Polysomnographic sleep patterns in children and adolescents in unresponsive wakefulness syndrome. J Head Trauma Rehabil 30:334–346. https://doi.org/10.1097/HTR.0000000000000122

    Article  PubMed  Google Scholar 

  34. Cornelissen L, Kim SE, Purdon PL et al (2015) Age-dependent electroencephalogram (EEG) patterns during sevoflurane general anesthesia in infants. Elife 4:e06513. https://doi.org/10.7554/eLife.06513

    Article  PubMed  PubMed Central  Google Scholar 

  35. Akeju O, Pavone KJ, Thum JA et al (2015) Age-dependency of sevoflurane-induced electroencephalogram dynamics in children. Br J Anaesth 115:i66–i76. https://doi.org/10.1093/bja/aev114

    Article  PubMed  PubMed Central  Google Scholar 

  36. Purdon PL, Pavone KJ, Akeju O et al (2015) The ageing brain: age-dependent changes in the electroencephalogram during propofol and sevofluranegeneral anaesthesia. Br J Anaesth 115:i46–i57. https://doi.org/10.1093/bja/aev213

    Article  PubMed  PubMed Central  Google Scholar 

  37. Kalmar K, Giacino JT (2005) The JFK coma recovery scale—revised. Neuropsychol Rehabil 15:454–460. https://doi.org/10.1080/09602010443000425

    Article  PubMed  Google Scholar 

  38. Iber C, Ancoli-Israel S, Chesson AL, Quan SF (2007) The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications. Westchester, IL

  39. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21. https://doi.org/10.1016/j.jneumeth.2003.10.009

    Article  PubMed  Google Scholar 

  40. Oostenveld R, Fries P, Maris E, Schoffelen J-M (2011) FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:156869. https://doi.org/10.1155/2011/156869

    Article  PubMed  Google Scholar 

  41. Duclos C, Dumont M, Arbour C et al (2017) Parallel recovery of consciousness and sleep in acute traumatic brain injury. Neurology 88:268–275. https://doi.org/10.1212/WNL.0000000000003508

    Article  PubMed  PubMed Central  Google Scholar 

  42. Pavlov YG, Gais S, Müller F et al (2017) Night sleep in patients with vegetative state. J Sleep Res 26:629–640. https://doi.org/10.1111/jsr.12524

    Article  PubMed  Google Scholar 

  43. Patterson JR, Grabois M (1986) Locked-in syndrome: a review of 139 cases. Stroke 17:758–764. https://doi.org/10.1161/01.str.17.4.758

    Article  CAS  PubMed  Google Scholar 

  44. Cummings JL, Greenberg R (1977) Sleep patterns in the ‘locked-in’ syndrome. Electroencephalogr Clin Neurophysiol 43:270–271. https://doi.org/10.1016/0013-4694(77)90134-1

    Article  CAS  PubMed  Google Scholar 

  45. Lu J, Sherman D, Devor M, Saper CB (2006) A putative flip-flop switch for control of REM sleep. Nature 441:589–594. https://doi.org/10.1038/nature04767

    Article  CAS  Google Scholar 

  46. Tononi G, Cirelli C (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10:49–62. https://doi.org/10.1016/j.smrv.2005.05.002

    Article  PubMed  Google Scholar 

  47. Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11:114–126. https://doi.org/10.1038/nrn2762

    Article  CAS  PubMed  Google Scholar 

  48. Rossi Sebastiano D, Franceschetti S (2018) A response to: “Sleep and circadian rhythms in severely brain-injured patients—a comment”. Clin Neurophysiol 129:1788. https://doi.org/10.1016/j.clinph.2018.04.744

    Article  PubMed  Google Scholar 

  49. Roehrs T, Roth T (2010) Drug-related sleep stage changes: functional significance and clinical relevance. Sleep Med Clin 5:559–570. https://doi.org/10.1016/j.jsmc.2010.08.002

    Article  PubMed  PubMed Central  Google Scholar 

  50. Bazil CW, Castro LHM, Walczak TS (2000) Reduction of rapid eye movement sleep by diurnal and nocturnal seizures in temporal lobe epilepsy. Arch Neurol 57:363–368. https://doi.org/10.1001/archneur.57.3.363

    Article  CAS  PubMed  Google Scholar 

  51. Miller LA, Ricci M, van Schalkwijk FJ et al (2016) Determining the relationship between sleep architecture, seizure variables and memory in patients with focal epilepsy. Behav Neurosci 130:316–324

    Article  Google Scholar 

  52. Jouvet M (1962) Recherches sur les structures nerveuses et les me´canismes responsables des diffe´rentes phases du sommeil physiologique. Arch Ital Biol 100:125–206

    CAS  PubMed  Google Scholar 

  53. Weber F, Chung S, Beier KT et al (2015) Control of REM sleep by ventral medulla GABAergic neurons. Nature 526:435–438. https://doi.org/10.1038/nature14979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Born J, Gais S (2000) REM sleep deprivation: the wrong paradigm leading to wrong conclusions. Behav Brain Sci 23:912–913. https://doi.org/10.1017/S0140525X00264029

    Article  Google Scholar 

  55. Krause AJ, Ben SE, Mander BA et al (2017) The sleep-deprived human brain. Nat Rev Neurosci 18:404–418. https://doi.org/10.1038/nrn.2017.55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Magidov E, Hayat H, Sharon O et al (2018) Near-total absence of REM sleep co-occurring with normal cognition: an update of the 1984 paper. Sleep Med 52:134–137. https://doi.org/10.1016/j.sleep.2018.09.003

    Article  PubMed  Google Scholar 

  57. Vertes RP, Eastman KE (2000) The case against memory consolidation in REM sleep. Behav Brain Sci 23:867–876. https://doi.org/10.1017/S0140525X00004003

    Article  CAS  PubMed  Google Scholar 

  58. De Gennaro L, Ferrara M, Bertini M (2001) The boundary between wakefulness and sleep: quantitative electroencephalographic changes during the sleep onset period. Neuroscience 107:1–11. https://doi.org/10.1016/S0306-4522(01)00309-8

    Article  PubMed  Google Scholar 

  59. Fernández-Espejo D, Bekinschtein TA, Monti MM et al (2011) Diffusion weighted imaging distinguishes the vegetative state from the minimally conscious state. Neuroimage 54:103–112. https://doi.org/10.1016/j.neuroimage.2010.08.035

    Article  PubMed  Google Scholar 

  60. Lutkenhoff ES, Chiang J, Tshibanda L et al (2015) Thalamic and extrathalamic mechanisms of consciousness after severe brain injury. Ann Neurol 78:68–76. https://doi.org/10.1002/ana.24423

    Article  PubMed  Google Scholar 

  61. Magrassi L, Zippo AG, Azzalin A et al (2018) Single unit activities recorded in the thalamus and the overlying parietal cortex of subjects affected by disorders of consciousness. PLoS ONE 13:1–17. https://doi.org/10.1371/journal.pone.0205967

    Article  CAS  Google Scholar 

  62. Schabus M, Wislowska M, Angerer M, Blume C (2018) Sleep and circadian rhythms in severely brain-injured patients—a comment. Clin Neurophysiol 129:1788. https://doi.org/10.1016/j.clinph.2018.04.744

    Article  Google Scholar 

  63. Bixler EO, Rhodes JM (1968) Spindle activity during sleep in cultural-familial mild retardates. Psychophysiology 5:212

    Google Scholar 

  64. Gibbs EL, Gibbs FA (1962) Extreme spindles: correlation of electroencephalographic sleep pattern with mental retardation. Science 138:1106–1107. https://doi.org/10.1126/science.138.3545.1106

    Article  CAS  PubMed  Google Scholar 

  65. Fogel SM, Smith CT (2011) The function of the sleep spindle: a physiological index of intelligence and a mechanism for sleep-dependent memory consolidation. Neurosci Biobehav Rev 35:1154–1165

    Article  Google Scholar 

  66. Fang Z, Sergeeva V, Ray LB et al (2017) Sleep spindles and intellectual ability: epiphenomenon or directly related? J Cogn Neurosci 29:167–182

    Article  Google Scholar 

  67. Fang Z, Ray LB, Owen AM, Fogel SM (2019) Brain activation time-locked to sleep spindles associated with human cognitive abilities. Front Neurosci 13:46

    Article  Google Scholar 

  68. Fang Z, Ray LB, Houldin E et al (2020) Sleep spindle-dependent functional connectivity correlates with cognitive abilities. J Cogn Neurosci 32:446–466

    Article  Google Scholar 

  69. Bódizs R, Kis T, Lázár AS et al (2005) Prediction of general mental ability based on neural oscillation measures of sleep. J Sleep Res 14:285–292

    Article  Google Scholar 

  70. Ulrich D (2016) Sleep spindles as facilitators of memory formation and learning. Neural Plast 2016:1796715

    Article  Google Scholar 

  71. Cologan V, Drouot X, Parapatics S et al (2013) Sleep in the unresponsive wakefulness syndrome and minimally conscious state. J Neurotrauma 30:339–346. https://doi.org/10.1089/neu.2012.2654

    Article  PubMed  Google Scholar 

  72. Rechtschaffen A, Kales A (1968) A manual of standardized terminology, techniques, and scoring system for sleep stages of human subjects. Washingt. Public Heal. Serv

  73. Kotchoubey B, Pavlov YG (2018) Approaches to sleep in severely brain damaged patients: opposite or complementary? Reply to “sleep and circadian rhythms in severely brain-injured patients—a comment”. Clin Neurophysiol 129:1785–1787. https://doi.org/10.1016/j.clinph.2018.03.049

    Article  PubMed  Google Scholar 

  74. Kotchoubey B, Pavlov YG (2018) Machine learning versus human expertise: the case of sleep stage classification in disorders of consciousness. Response to Wislowska et al. Clin Neurophysiol 129:2682–2683. https://doi.org/10.1016/j.clinph.2018.09.020

    Article  PubMed  Google Scholar 

  75. Wislowska M, Blume C, Angerer M et al (2018) Approaches to sleep in severely brain damaged patients—further comments and replies to Kotchoubey & Pavlov. Clin Neurophysiol 129:2680–2681. https://doi.org/10.1016/j.clinph.2018.08.029

    Article  CAS  PubMed  Google Scholar 

  76. Kotchoubey B, Pavlov YG (2018) Sleep patterns open the window into disorders of consciousness. Clin Neurophysiol 129:668–669. https://doi.org/10.1016/j.clinph.2018.01.006

    Article  CAS  PubMed  Google Scholar 

  77. Canadian Institutes of Health Research, Natural Sciences and Engineering Research Council of Canada, Social Sciences and Humanities Research Council (2018) Tri-Council Policy Statement: Ethical Conduct for Research Involving Humans

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Funding

RMG was supported by a Vanier Canada Graduate Scholarship from the Natural Sciences and Engineering Research Council of Canada.

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Authors and Affiliations

  1. The Brain and Mind Institute, Western University, London, Canada

    Raechelle M. Gibson, Geoffrey Laforge & Adrian M. Owen

  2. Department of Psychology, Western University, London, Canada

    Raechelle M. Gibson, Geoffrey Laforge & Adrian M. Owen

  3. Sleep Research Unit, The Royal’s Institute of Mental Health Research, Ottawa, Canada

    Laura B. Ray & Stuart M. Fogel

  4. Department of Physiology and Pharmacology, Western University, London, Canada

    Adrian M. Owen

  5. School of Psychology, University of Ottawa, Ottawa, Canada

    Stuart M. Fogel

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  1. Raechelle M. Gibson
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  2. Laura B. Ray
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  3. Geoffrey Laforge
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  4. Adrian M. Owen
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  5. Stuart M. Fogel
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Contributions

Conceptualization: RMG, AMO, SMF; methodology: RMG, LBR, SMF; formal analysis and investigation: RMG, LBR, GL, SMF; writing, first draft: RMG; writing, reviewing and editing: RMG, LBR, GL, AMO, SMF; funding acquisition: AMO; supervision: AMO, SMF.

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Correspondence to Stuart M. Fogel.

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The authors declare that they have no conflict of interest.

Ethical approval

Both the patient and control studies were approved by the appropriate local ethics committee at Western University (London, Canada) and have therefore been performed in accordance with the ethical standards laid down in the Canadian Tri-Council Policy Statement: Ethical Conduct for Research Involving Humans 2 [77]. For the control studies, all participants gave their informed consent prior to their inclusion in the study. For the behaviourally non-responsive patients, each patient’s designated substitute decision-maker gave their informed consent prior to the patient’s inclusion in the study.

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Gibson, R.M., Ray, L.B., Laforge, G. et al. 24-h polysomnographic recordings and electrophysiological spectral analyses from a cohort of patients with chronic disorders of consciousness. J Neurol 267, 3650–3663 (2020). https://doi.org/10.1007/s00415-020-10076-2

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