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Nonlinear dynamics captures brain states at different levels of consciousness in patients anesthetized with propofol


Autoři: Sarah L. Eagleman aff001;  Divya Chander aff002;  Christina Reynolds aff003;  Nicholas T. Ouellette aff005;  M. Bruce MacIver aff001
Působiště autorů: Department of Anesthesiology, Perioperative and Pain Medicine, Stanford University School of Medicine, Stanford, California, United States of America aff001;  Department of Medicine, Stanford University School of Medicine, Stanford, California, United States of America aff002;  Department of Neurology, Oregon Health Sciences University, Portland, Oregon, United States of America aff003;  National Radio Astronomy Observatory, Charlottesville, VA, United States of America aff004;  Department of Civil and Environmental Engineering, Stanford University, Stanford, California, United States of America aff005
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223921

Souhrn

The information processing capability of the brain decreases during unconscious states. Capturing this decrease during anesthesia-induced unconsciousness has been attempted using standard spectral analyses as these correlate relatively well with breakdowns in corticothalamic networks. Much of this work has involved the use of propofol to perturb brain activity, as it is one of the most widely used anesthetics for routine surgical anesthesia. Propofol administration alone produces EEG spectral characteristics similar to most hypnotics; however, inter-individual and drug variation render spectral measures inconsistent. Complexity measures of EEG signals could offer better measures to distinguish brain states, because brain activity exhibits nonlinear behavior at several scales during transitions of consciousness. We tested the potential of complexity analyses from nonlinear dynamics to identify loss and recovery of consciousness at clinically relevant timepoints. Patients undergoing propofol general anesthesia for various surgical procedures were identified as having changes in states of consciousness by the loss and recovery of response to verbal stimuli after induction and upon cessation of anesthesia, respectively. We demonstrate that nonlinear dynamics analyses showed more significant differences between consciousness states than spectral measures. Notably, attractors in conscious and anesthesia-induced unconscious states exhibited significantly different shapes. These shapes have implications for network connectivity, information processing, and the total number of states available to the brain at these different levels. They also reflect some of our general understanding of the network effects of consciousness in a way that spectral measures cannot. Thus, complexity measures could provide a universal means for reliably capturing depth of consciousness based on EEG changes at the beginning and end of anesthesia administration.

Klíčová slova:

Anesthesia – Anesthetics – Consciousness – Electroencephalography – Ellipses – Nonlinear dynamics – Surgical and invasive medical procedures – Syncope


Zdroje

1. Widman Schreiber, Rehberg Hoeft, Elger. Quantification of depth of anesthesia by nonlinear time series analysis of brain electrical activity. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 2000;62(4 Pt A):4898–903.

2. Walling PT, Hicks KN. Nonlinear changes in brain dynamics during emergence from sevoflurane anesthesia: preliminary exploration using new software. Anesthesiology. 2006;105(5):927–35. doi: 10.1097/00000542-200611000-00013 17065886

3. Watt RC, Hameroff SR. Phase space electroencephalography (EEG): A new mode of intraoperative EEG analysis. Int J Clin Monit Comput. 1988;5(1):3–13. 3351372

4. Ma Y, Shi W, Peng C-K, Yang AC. Nonlinear dynamical analysis of sleep electroencephalography using fractal and entropy approaches. Sleep Med Rev. 2018;37:85–93. doi: 10.1016/j.smrv.2017.01.003 28392169

5. Stam CJJ. Nonlinear dynamical analysis of EEG and MEG: Review of an emerging field. Clin Neurophysiol. 2005;116(10):2266–301. doi: 10.1016/j.clinph.2005.06.011 16115797

6. Wang DJJ, Jann K, Fan C, Qiao Y, Zang Y-F, Lu H, et al. Neurophysiological Basis of Multi-Scale Entropy of Brain Complexity and Its Relationship With Functional Connectivity. Front Neurosci. 2018;12:352. doi: 10.3389/fnins.2018.00352 29896081

7. Winters WD. Effects of Drugs on the Electrical Activity of the Brain: Anesthetics. Annu Rev Pharmacol Toxicol. 1976;16(1):413–26.

8. Billard V, Gambus PL, Chamoun N, Stanski DR, Shafer SL. A comparison of spectral edge, delta power, and bispectral index as EEG measures of alfentanil, propofol, and midazolam drug effect*. Clin Pharmacol Ther. 1997;61(1):45–58. doi: 10.1016/S0009-9236(97)90181-8 9024173

9. Rampil IJ. Monitoring depth of anesthesia. Curr Opin Anaesthesiol. 2001;14(6):649–53. 17019160

10. Purdon PL, Sampson A, Pavone KJ, Brown EN. Clinical Electroencephalography for Anesthesiologists Part I: Background and Basic Signatures. Anesthesiology. 2015;123(4):937–60. doi: 10.1097/ALN.0000000000000841 26275092

11. Ching S, Cimenser A, Purdon PL, Brown EN, Kopell NJ. Thalamocortical model for a propofol-induced -rhythm associated with loss of consciousness. Proc Natl Acad Sci. 2010;107(52):22665–70. doi: 10.1073/pnas.1017069108 21149695

12. Vijayan S, Ching S, Purdon PL, Brown EN, Kopell NJ. Thalamocortical mechanisms for the anteriorization of α rhythms during propofol-induced unconsciousness. J Neurosci. 2013;33(27).

13. Nishikawa K, MacIver MB. Membrane and Synaptic Actions of Halothane on Rat Hippocampal Pyramidal Neurons and Inhibitory Interneurons. J Neurosci. 2000;20(16):5915–23. 10934238

14. Lukatch HS, MacIver MB. Synaptic mechanisms of thiopental-induced alterations in synchronized cortical activity. Anesthesiology. 1996;84(6):1425–34. doi: 10.1097/00000542-199606000-00019 8669684

15. Nicoll RA, Eccles JC, Oshima T, Rubia F. Prolongation of hippocampal inhibitory postsynaptic potentials by barbiturates. Nature. 1975;258(5536):625–7. doi: 10.1038/258625a0 1207741

16. Chander D, García PS, MacColl JN, Illing S, Sleigh JW. Electroencephalographic Variation during End Maintenance and Emergence from Surgical Anesthesia. Rudolph U, editor. PLoS One. 2014;9(9):e106291. doi: 10.1371/journal.pone.0106291 25264892

17. Pilge S, Jordan D, Kreuzer M, Kochs EF, Schneider G. Burst suppression-MAC and burst suppression-CP50 as measures of cerebral effects of anaesthetics. Br J Anaesth. 2014;112(6):1067–74. doi: 10.1093/bja/aeu016 24658022

18. Stanski DR, Hudson RJ, Homer TD, Saidman LJ, Meathe E. Pharmacodynamic modeling of thiopental anesthesia. J Pharmacokinet Biopharm. 1984;12(2):223–40. 6491902

19. Friedman EB, Sun Y, Moore JT, Hung H-T, Meng QC, Perera P, et al. A Conserved Behavioral State Barrier Impedes Transitions between Anesthetic-Induced Unconsciousness and Wakefulness: Evidence for Neural Inertia. van Swinderen B, editor. PLoS One. 2010;5(7):e11903. doi: 10.1371/journal.pone.0011903 20689589

20. Tarnal V, Vlisides PE, Mashour GA. The Neurobiology of Anesthetic Emergence. J Neurosurg Anesthesiol. 2015;28(3):1.

21. Frank GB, Jhamandas K. Effects of drugs acting alone and in combination on the motor activity of intact mice. Br J Pharmacol. 1970;39(4):696–706. doi: 10.1111/j.1476-5381.1970.tb09895.x 4394969

22. MacIver MB, Bland BH. Chaos analysis of EEG during isoflurane-induced loss of righting in rats. Front Syst Neurosci. 2014;8:203. doi: 10.3389/fnsys.2014.00203 25360091

23. Eagleman SL, Drover CM, Drover DR, Ouellette NT, MacIver MB. Remifentanil and Nitrous Oxide Anesthesia Produces a Unique Pattern of EEG Activity During Loss and Recovery of Response. Front Hum Neurosci. 2018;12:173. doi: 10.3389/fnhum.2018.00173 29867405

24. Eagleman SL, Vaughn DA, Drover DR, Drover CM, Cohen MS, Ouellette NT, et al. Do Complexity Measures of Frontal EEG Distinguish Loss of Consciousness in Geriatric Patients Under Anesthesia? Front Neurosci. 2018;12:645. doi: 10.3389/fnins.2018.00645 30294254

25. Khachiyan LG. Polynomial algorithms in linear programming. USSR Comput Math Math Phys. 1980;20(1):53–72.

26. Casali AG, Gosseries O, Rosanova M, Boly M, Sarasso S, Casali KR, et al. A Theoretically Based Index of Consciousness Independent of Sensory Processing and Behavior. Sci Transl Med. 2013;5(198).

27. Sarasso S, Boly M, Napolitani M, Gosseries O, Charland-Verville V, Casarotto S, et al. Consciousness and Complexity during Unresponsiveness Induced by Propofol, Xenon, and Ketamine. Curr Biol CB. 2015;25(23):3099–105. doi: 10.1016/j.cub.2015.10.014 26752078

28. Rosanova M, Fecchio M, Casarotto S, Sarasso S, Casali AG, Pigorini A, et al. Sleep-like cortical OFF-periods disrupt causality and complexity in the brain of unresponsive wakefulness syndrome patients. Nat Commun. 2018;9(1):4427. doi: 10.1038/s41467-018-06871-1 30356042

29. Bodart O, Gosseries O, Wannez S, Thibaut A, Annen J, Boly M, et al. Measures of metabolism and complexity in the brain of patients with disorders of consciousness. NeuroImage Clin. 2017;14:354–62. doi: 10.1016/j.nicl.2017.02.002 28239544

30. Committee AH of DS and PP. American Society of Anesthesiologists Committee on Standards and Practice Parameters Standards for Basic Anesthetic Monitoring. 2015.

31. Mitra P, Bokil H. Observed brain dynamics. Oxford University Press; 2008. 381 p.

32. Purdon PL, Pierce ET, Mukamel EA, Prerau MJ, Walsh JL, Wong KFK, et al. Electroencephalogram signatures of loss and recovery of consciousness from propofol. Proc Natl Acad Sci. 2013;

33. Gugino LD, Chabot RJ, Prichep LS, John ER, Formanek V, Aglio LS. Quantitative EEG changes associated with loss and return of consciousness in healthy adult volunteers anaesthetized with propofol or sevoflurane. Br J Anaesth. 2001;87(3):421–8. doi: 10.1093/bja/87.3.421 11517126

34. Grassberger P, Procaccia I. Characterization of Strange Attractors. Phys Rev Lett. 1983;50(5):346–9.

35. Holm S. A Simple Sequentially Rejective Multiple Test Procedure [Internet]. Vol. 6, Scandinavian Journal of Statistics. WileyBoard of the Foundation of the Scandinavian Journal of Statistics; 1979. p. 65–70.

36. Breshears JD, Roland JL, Sharma M, Gaona CM, Freudenburg Z V, Tempelhoff R, et al. Stable and dynamic cortical electrophysiology of induction and emergence with propofol anesthesia. Proc Natl Acad Sci U S A. 2010;107(49):21170–5. doi: 10.1073/pnas.1011949107 21078987

37. Li X, Cui S, Voss LJ. Using permutation entropy to measure the electroencephalographic effects of sevoflurane. Anesthesiology. 2008;

38. Olofsen E, Sleigh JW, Dahan A. Permutation entropy of the electroencephalogram: A measure of anaesthetic drug effect. Br J Anaesth. 2008;

39. Su C, Liang Z, Li X, Li D, Li Y, Ursino M. A Comparison of Multiscale Permutation Entropy Measures in On-Line Depth of Anesthesia Monitoring. Hernandez Montoya AR, editor. PLoS One. 2016;11(10):e0164104. doi: 10.1371/journal.pone.0164104 27723803

40. Struys MM, De Smet T, Depoorter B, Versichelen LF, Mortier EP, Dumortier FJ, et al. Comparison of plasma compartment versus two methods for effect compartment—controlled target-controlled infusion for propofol. Anesthesiology. 2000;92(2):399–406. doi: 10.1097/00000542-200002000-00021 10691226

41. Greenblatt DJ, Ehrenberg BL, Culm KE, Scavone JM, Corbett KE, Friedman HL, et al. Kinetics and EEG Effects of Midazolam during and after 1-Minute, 1-Hour, and 3-Hour Intravenous Infusions. J Clin Pharmacol. 2004;44(6):605–11. doi: 10.1177/0091270004265368 15145968

42. Minto CF, Schnider TW, Egan TD, Youngs E, Lemmens HJ, Gambus PL, et al. Influence of age and gender on the pharmacokinetics and pharmacodynamics of remifentanil. I. Model development. Anesthesiology. 1997;86(1):10–23. doi: 10.1097/00000542-199701000-00004 9009935

43. Egan TD. Remifentanil pharmacokinetics and pharmacodynamics. A preliminary appraisal. Clin Pharmacokinet. 1995;29(2):80–94. doi: 10.2165/00003088-199529020-00003 7586903

44. Scott JC, Ponganis K V, Stanski DR. EEG quantitation of narcotic effect: the comparative pharmacodynamics of fentanyl and alfentanil. Anesthesiology. 1985;62(3):234–41. doi: 10.1097/00000542-198503000-00005 3919613

45. Rampil IJ, Kim JS, Lenhardt R, Negishi C, Sessler DI. Bispectral EEG index during nitrous oxide administration. Anesthesiology. 1998;89(3):671–7. doi: 10.1097/00000542-199809000-00017 9743404

46. Hirota K, Kubota T, Ishihara H, Matsuki A. The effects of nitrous oxide and ketamine on the bispectral index and 95% spectral edge frequency during propofol-fentanyl anaesthesia. Eur J Anaesthesiol. 1999;16(11):779–83. doi: 10.1046/j.1365-2346.1999.00585.x 10713872

47. Foster BL, Liley DTJ. Nitrous Oxide Paradoxically Modulates Slow Electroencephalogram Oscillations. Anesth Analg. 2011;113(4):758–65. doi: 10.1213/ANE.0b013e318227b688 21788312

48. Akeju O, Westover MB, Pavone KJ, Sampson AL, Hartnack KE, Brown EN, et al. Effects of Sevoflurane and Propofol on Frontal Electroencephalogram Power and Coherence. Anesthesiology. 2014;121(5):990–8. doi: 10.1097/ALN.0000000000000436 25233374

49. Feshchenko VA, Veselis RA, Reinsel RA. Propofol-Induced Alpha Rhythm. Neuropsychobiology. 2004;50(3):257–66. doi: 10.1159/000079981 15365226

50. Boly M, Moran R, Murphy M, Boveroux P, Bruno M-A, Noirhomme Q, et al. Connectivity Changes Underlying Spectral EEG Changes during Propofol-Induced Loss of Consciousness. J Neurosci. 2012;32(20):7082–90. doi: 10.1523/JNEUROSCI.3769-11.2012 22593076

51. Muthukumaraswamy SD. High-frequency brain activity and muscle artifacts in MEG/EEG: a review and recommendations. Front Hum Neurosci. 2013;7:138. doi: 10.3389/fnhum.2013.00138 23596409

52. Shackman AJ, McMenamin BW, Slagter HA, Maxwell JS, Greischar LL, Davidson RJ. Electromyogenic Artifacts and Electroencephalographic Inferences. Brain Topogr. 2009;22(1):7–12. doi: 10.1007/s10548-009-0079-4 19214730

53. Claus S, Velis D, Lopes da Silva FH, Viergever MA, Kalitzin S. High frequency spectral components after Secobarbital: The contribution of muscular origin-A study with MEG/EEG. Epilepsy Res. 2012;

54. Sleigh JW, Steyn-Ross DA, Steyn-Ross ML, Williams ML, Smith P. Comparison of changes in electroencephalographic measures during induction of general anaesthesia: influence of the gamma frequency band and electromyogram signal. Br J Anaesth. 2001;86(1):50–8. doi: 10.1093/bja/86.1.50 11575410

55. Egan TD, Minto CF, Hermann DJ, Barr J, Muir KT, Shafer SL. Remifentanil versus alfentanil: comparative pharmacokinetics and pharmacodynamics in healthy adult male volunteers. Anesthesiology. 1996;84(4):821–33. doi: 10.1097/00000542-199604000-00009 8638836

56. Egan TD, Lemmens HJ, Fiset P, Hermann DJ, Muir KT, Stanski DR, et al. The pharmacokinetics of the new short-acting opioid remifentanil (GI87084B) in healthy adult male volunteers. Anesthesiology. 1993;79(5):881–92. doi: 10.1097/00000542-199311000-00004 7902032

57. Mi W, Sakai T, Kudo T, Kudo M, Matsuki A. The interaction between fentanyl and propofol during emergence from anesthesia: monitoring with the EEG-Bispectral index. J Clin Anesth. 2003;15(2):103–7. doi: 10.1016/s0952-8180(02)00510-x 12719048

58. Veselis RA, Reinsel R, Marino P, Sommer S, Carlon GC. The effects of midazolam on the EEG during sedation of critically ill patients. Anaesthesia. 1993;48(6):463–70. doi: 10.1111/j.1365-2044.1993.tb07063.x 8322985

59. Kortelainen J, Koskinen M, Mustola S, Seppänen T. Effects of Remifentanil on the Spectrum and Quantitative Parameters of Electroencephalogram in Propofol Anesthesia. Anesthesiology. 2009;111(3):574–83. doi: 10.1097/ALN.0b013e3181af633c 19672187

60. Mazanikov M, Udd M, Kylänpää L, Lindström O, Aho P, Halttunen J, et al. Patient-controlled sedation with propofol and remifentanil for ERCP: a randomized, controlled study. Gastrointest Endosc. 2011;73(2):260–6. doi: 10.1016/j.gie.2010.10.005 21295639

61. Kortelainen J, Koskinen M, Mustola S, Seppänen T. Remifentanil Modifies the Relation of Electroencephalographic Spectral Changes and Clinical Endpoints in Propofol Anesthesia. Anesthesiology. 2008;109(2):198–205. doi: 10.1097/ALN.0b013e31817f5bfc 18648228

62. Kaka U, Hui Cheng C, Meng GY, Fakurazi S, Kaka A, Behan AA, et al. Electroencephalographic changes associated with antinociceptive actions of lidocaine, ketamine, meloxicam, and morphine administration in minimally anaesthetized dogs. Biomed Res Int. 2015;2015:305367. doi: 10.1155/2015/305367 25695060

63. Maher K, Reynolds C, Chander D. Drug Effects on the EEG under General Anesthesia. In: American Society of Anesthesiologists. Chicago, IL; 2016.

64. Lee H, Mashour GA, Noh G-J, Kim S, Lee U. Reconfiguration of network hub structure after propofol-induced unconsciousness. Anesthesiology. 2013;119(6):1347–59. doi: 10.1097/ALN.0b013e3182a8ec8c 24013572

65. Mashour GA, Hudetz AG. Neural Correlates of Unconsciousness in Large-Scale Brain Networks. Trends Neurosci. 2018;41(3):150–60. doi: 10.1016/j.tins.2018.01.003 29409683

66. Vlisides PE, Li D, Zierau M, Lapointe AP, Ip KI, McKinney AM, et al. Dynamic Cortical Connectivity during General Anesthesia in Surgical Patients. Anesthesiology. 2019;1.

67. Huang Z, Liu X, Mashour GA, Hudetz AG. Timescales of Intrinsic BOLD Signal Dynamics and Functional Connectivity in Pharmacologic and Neuropathologic States of Unconsciousness. J Neurosci. 2018;38(9):2304–17. doi: 10.1523/JNEUROSCI.2545-17.2018 29386261


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