Age-dependent electroencephalogram (EEG) patterns during sevoflurane general anesthesia in infants
Laura Cornelissen, Seong-Eun Kim, Patrick L Purdon, Emery N Brown, Charles B Berde, Laura Cornelissen, Seong-Eun Kim, Patrick L Purdon, Emery N Brown, Charles B Berde
Abstract
Electroencephalogram (EEG) approaches may provide important information about developmental changes in brain-state dynamics during general anesthesia. We used multi-electrode EEG, analyzed with multitaper spectral methods and video recording of body movement to characterize the spatio-temporal dynamics of brain activity in 36 infants 0-6 months old when awake, and during maintenance of and emergence from sevoflurane general anesthesia. During maintenance: (1) slow-delta oscillations were present in all ages; (2) theta and alpha oscillations emerged around 4 months; (3) unlike adults, all infants lacked frontal alpha predominance and coherence. Alpha power was greatest during maintenance, compared to awake and emergence in infants at 4-6 months. During emergence, theta and alpha power decreased with decreasing sevoflurane concentration in infants at 4-6 months. These EEG dynamic differences are likely due to developmental factors including regional differences in synaptogenesis, glucose metabolism, and myelination across the cortex. We demonstrate the need to apply age-adjusted analytic approaches to develop neurophysiologic-based strategies for pediatric anesthetic state monitoring.
Keywords: EEG; alpha; anesthesia; computational biology; development; human; infant; neuroscience; sevoflurane; systems biology.
Conflict of interest statement
PLP: PLP has patents pending on brain monitoring during general anesthesia and sedation, and a patent licensing agreement with Masimo Corporation. Application Numbers: 20150080754, 20150011907, 20140323898, 20140323897, 20140316218, 20140316217, 20140187973, 20140180160, 20080306397.
ENB: ENB has patents pending on brain monitoring during general anesthesia and sedation, and a patent licensing agreement with Masimo Corporation. Application Numbers: 20150080754, 20150011907, 20140323898, 20140323897, 20140316218, 20140316217, 20140187973, 20140180160. ENB is a Reviewing Editor for eLife.
The other authors declare that no competing interests exist.
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References
- Akeju O, Loggia ML, Catana C, Pavone KJ, Vazquez R, Rhee J, Contreras Ramirez V, Chonde DB, Izquierdo-Garcia D, Arabasz G, Hsu S, Habeeb K, Hooker JM, Napadow V, Brown EN, Purdon PL. Disruption of thalamic functional connectivity is a neural correlate of dexmedetomidine-induced unconsciousness. eLife. 2014a;4:e04499. doi: 10.7554/eLife.04499.
- Akeju O, Pavone KJ, Westover MB, Vazquez R, Prerau MJ, Harrell PG, Hartnack KE, Rhee J, Sampson AL, Habeeb K, Gao L, Pierce ET, Walsh JL, Brown EN, Purdon PL. A comparison of propofol- and dexmedetomidine-induced electroencephalogram dynamics using spectral and coherence analysis. Anesthesiology. 2014b;121:978–989. doi: 10.1097/ALN.0000000000000419.
- Akeju O, Westover MB, Pavone KJ, Sampson AL, Hartnack KE, Brown EN, Purdon PL. Effects of sevoflurane and propofol on frontal electroencephalogram power and coherence. Anesthesiology. 2014c;121:990–998. doi: 10.1097/ALN.0000000000000436.
- Bokil H, Andrews P, Kulkarni JE, Mehta S, Mitra PP. Chronux: a platform for analyzing neural signals. Journal of Neuroscience Methods. 2010;192:146–151. doi: 10.1016/j.jneumeth.2010.06.020.
- Boly M, Moran R, Murphy M, Boveroux P, Bruno MA, Noirhomme Q, Ledoux D, Bonhomme V, Brichant JF, Tononi G, Laureys S, Friston K. Connectivity changes underlying spectral EEG changes during propofol-induced loss of consciousness. The Journal of Neuroscience. 2012;32:7082–7090. doi: 10.1523/JNEUROSCI.3769-11.2012.
- Boveroux P, Vanhaudenhuyse A, Bruno MA, Noirhomme Q, Lauwick S, Luxen A, Degueldre C, Plenevaux A, Schnakers C, Phillips C, Brichant JF, Bonhomme V, Maquet P, Greicius MD, Laureys S, Boly M. Breakdown of within- and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness. Anesthesiology. 2010;113:1038–1053. doi: 10.1097/ALN.0b013e3181f697f5.
- Breshears JD, Roland JL, Sharma M, Gaona CM, Freudenburg ZV, Tempelhoff R, Avidan MS, Leuthardt EC. Stable and dynamic cortical electrophysiology of induction and emergence with propofol anesthesia. Proceedings of the National Academy of Sciences of USA. 2010;107:21170–21175. doi: 10.1073/pnas.1011949107.
- Brody BA, Kinney HC, Kloman AS, Gilles FH. Sequence of central nervous system myelination in human Infancy. I. an autopsy atudy of myelination. Journal of Neuropathology and Experimental Neurology. 1987;46:283–301. doi: 10.1097/00005072-198705000-00005.
- Brown EN, Lydic R, Schiff ND. General anesthesia, sleep, and coma. The New England Journal of Medicine. 2010;363:2638–2650. doi: 10.1056/NEJMra0808281.
- Brown EN, Purdon PL, Van Dort CJ. General anesthesia and altered states of arousal: a systems neuroscience analysis. Annual Review of Neuroscience. 2011;34:601–628. doi: 10.1146/annurev-neuro-060909-153200.
- Brown EN, Solt K, Purdon PL, Akeju O. Miller's anesthesia. 8th Edition. Volume 1. Cambridge: Elsevier Health Sciences; 2015. Monitoring brain state during general anesthesia and sedation; p. 50.
- Casali AG, Gosseries O, Rosanova M, Boly M, Sarasso S, Casali KR, Casarotto S, Bruno MA, Laureys S, Tononi G, Massimini M. A theoretically based index of consciousness independent of sensory processing and behavior. Science Translational Medicine. 2013;5:198ra105. doi: 10.1126/scitranslmed.3006294.
- Catts VS, Fung SJ, Long LE, Joshi D, Vercammen A, Allen KM, Fillman SG, Rothmond DA, Sinclair D, Tiwari Y, Tsai SY, Weickert TW, Shannon Weickert C. Rethinking schizophrenia in the context of normal neurodevelopment. Frontiers in Cellular Neuroscience. 2013;7:60. doi: 10.3389/fncel.2013.00060.
- Ching S, Brown EN. Modeling the dynamical effects of anesthesia on brain circuits. Current Opinion in Neurobiology. 2014;25:116–122. doi: 10.1016/j.conb.2013.12.011.
- Ching S, Cimenser A, Purdon PL, Brown EN, Kopell NJ. Thalamocortical model for a propofol-induced alpha-rhythm associated with loss of consciousness. Proceedings of the National Academy of Sciences of USA. 2010;107:22665–22670. doi: 10.1073/pnas.1017069108.
- Chugani HT, Phelps ME. Maturational changes in cerebral function in infants determined by 18FDG positron emission tomography. Science. 1986;231:840–843. doi: 10.1126/science.3945811.
- Chugani HT, Phelps ME, Mazziotta JC. Positron emission tomography study of human brain functional development. Annals of Neurology. 1987;22:487–497. doi: 10.1002/ana.410220408.
- Cimenser A, Purdon PL, Pierce ET, Walsh JL, Salazar-Gomez AF, Harrell PG, Tavares-Stoeckel C, Habeeb K, Brown EN. Tracking brain states under general anesthesia by using global coherence analysis. Proceedings of the National Academy of Sciences of USA. 2011;108:8832–8837. doi: 10.1073/pnas.1017041108.
- Constant I, Sabourdin N. The EEG signal: a window on the cortical brain activity. Paediatric Anaesthesia. 2012;22:539–552. doi: 10.1111/j.1460-9592.2012.03883.x.
- Davidson AJ. Monitoring the anaesthetic depth in children—an update. Current Opinion in Anaesthesiology. 2007;20:236–243. doi: 10.1097/ACO.0b013e3280c60c66.
- Davidson AJ, Sale SM, Wong C, McKeever S, Sheppard S, Chan Z, Williams C. The electroencephalograph during anesthesia and emergence in infants and children. Paediatric Anaesthesia. 2008;18:60–70. doi: 10.1111/j.1460-9592.2007.02359.x.
- Dehorter N, Vinay L, Hammond C, Ben-Ari Y. Timing of developmental sequences in different brain structures: physiological and pathological implications. The European Journal of Neuroscience. 2012;35:1846–1856. doi: 10.1111/j.1460-9568.2012.08152.x.
- Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods. 2004;134:9–21. doi: 10.1016/j.jneumeth.2003.10.009.
- Feshchenko VA, Veselis RA, Reinsel RA. Propofol-induced alpha rhythm. Neuropsychobiology. 2004;50:257–266. doi: 10.1159/000079981.
- Hayashi K, Shigemi K, Sawa T. Neonatal electroencephalography shows low sensitivity to anesthesia. Neuroscience Letters. 2012;517:87–91. doi: 10.1016/j.neulet.2012.04.028.
- Hensch T. Critical period regulation. Annual Review of Neuroscience. 2004;27:549–579. doi: 10.1146/annurev.neuro.27.070203.144327.
- Huttenlocher PR, de Courten C, Garey LJ, Van der Loos H. Synaptogenesis in human visual cortex—evidence for synapse elimination during normal development. Neuroscience Letters. 1982;33:247–252. doi: 10.1016/0304-394090379-2.
- Huttenlocher PR, Dabholkar AS. Regional differences in synaptogenesis in human cerebral cortex. The Journal of Comparative Neurology. 1997;387:167–178. doi: 10.1002/(SICI)1096-9861(19971020)387:2<167::AID-CNE1>;2-Z.
- Jevtovic-Todorovic V, Absalom AR, Blomgren K, Brambrink A, Crosby G, Culley DJ, Fiskum G, Giffard RG, Herold KF, Loepke AW, Ma D, Orser BA, Planel E, Slikker W, Jr, Soriano SG, Stratmann G, Vutskits L, Xie Z, Hemmings HC., Jr Anaesthetic neurotoxicity and neuroplasticity: an expert group report and statement based on the BJA Salzburg Seminar. British Journal of Anaesthesia. 2013;111:143–151. doi: 10.1093/bja/aet177.
- Johnson MH. Functional brain development in humans. Nature Reviews Neuroscience. 2001;2:475–483. doi: 10.1038/35081509.
- Kanold PO, Luhmann HJ. The subplate and early cortical circuits. Annual Review of Neuroscience. 2010;33:23–48. doi: 10.1146/annurev-neuro-060909-153244.
- Kinnala A, Suhonen-Polvi H, Aärimaa T, Kero P, Korvenranta H, Ruotsalainen U, Bergman J, Haaparanta M, Solin O, Nuutila P, Wegelius U. Cerebral metabolic rate for glucose during the first six months of life: An FDG positron emission tomography study. Archives of Disease in Childhood. Fetal and Neonatal Edition. 1996;74:F153–F157. doi: 10.1136/fn.74.3.F153.
- Kinney HC, Brody BA, Kloman AS, Gilles FH. Sequence of central nervous system myelination in human infancy. II. patterns of myelination in autopsied infants. Journal of Neuropathology and Experimental Neurology. 1988;47:217–234. doi: 10.1097/00005072-198805000-00003.
- Kirch C, Politis DN. Tft-bootstrap: resampling time series in the frequency domain to obtain replicates in the time domain. The Annals of Statistics. 2011;39:1427–1470. doi: 10.1214/10-AOS868.
- Kostović I, Judas M. The development of the subplate and thalamocortical connections in the human foetal brain. Acta Paediatrica. 2010;99:1119–1127. doi: 10.1111/j.1651-2227.2010.01811.x.
- Lee U, Ku S, Noh G, Baek S, Choi B, Mashour GA. Disruption of frontal-parietal communication by ketamine, propofol, and sevoflurane. Anesthesiology. 2013;118:1264–1275. doi: 10.1097/ALN.0b013e31829103f5.
- Lewis LD, Weiner VS, Mukamel EA, Donoghue JA, Eskandar EN, Madsen JR, Anderson WS, Hochberg LR, Cash SS, Brown EN, Purdon PL. Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness. Proceedings of the National Academy of Sciences of USA. 2012;109:E3377–E3386. doi: 10.1073/pnas.1210907109.
- Lin EP, Soriano SG, Loepke AW. Anesthetic neurotoxicity. Anesthesiology Clinics. 2014;32:133–155. doi: 10.1016/j.anclin.2013.10.003.
- Liu X, Lauer KK, Ward BD, Li SJ, Hudetz AG. Differential effects of deep sedation with propofol on the specific and nonspecific thalamocortical systems: a functional magnetic resonance imaging study. Anesthesiology. 2013;118:59–69. doi: 10.1097/ALN.0b013e318277a801.
- Lo SS, Sobol JB, Mallavaram N, Carson M, Chang C, Grieve PG, Emerson RG, Stark RI, Sun LS. Anesthetic-specific electroencephalographic patterns during emergence from sevoflurane and isoflurane in infants and children. Paediatric Anaesthesia. 2009;19:1157–1165. doi: 10.1111/j.1460-9592.2009.03128.x.
- Martuzzi R, Ramani R, Qiu M, Shen X, Papademetris X, Constable RT. A whole-brain voxel based measure of Intrinsic connectivity contrast reveals local changes in tissue connectivity with anesthetic without a priori assumptions on thresholds or regions of interest. Neuroimage. 2011;58:1044–1050. doi: 10.1016/j.neuroimage.2011.06.075.
- McCann ME, Soriano SG. General anesthetics in pediatric anesthesia: influences on the developing brain. Current Drug Targets. 2012;13:944–951. doi: 10.2174/138945012800675768.
- McKeever S, Johnston L, Davidson AJ. An observational study exploring amplitude-integrated electroencephalogram and spectral edge frequency during paediatric anaesthesia. Anaesthesia and Intensive Care. 2012;40:275–284.
- Mhuircheartaigh RN, Rosenorn-Lanng D, Wise R, Jbabdi S, Rogers R, Tracey I. Cortical and subcortical connectivity changes during decreasing levels of consciousness in humans: a functional magnetic resonance imaging study using propofol. The Journal of Neuroscience. 2010;30:9095–9102. doi: 10.1523/JNEUROSCI.5516-09.2010.
- Murphy M, Bruno MA, Riedner BA, Boveroux P, Noirhomme Q, Landsness EC, Brichant JF, Phillips C, Massimini M, Laureys S, Tononi G, Boly M. Propofol anesthesia and sleep: a high-density EEG study. Sleep. 2011;34:283–291A.
- Ní Mhuircheartaigh R, Warnaby C, Rogers R, Jbabdi S, Tracey I. Slow-wave activity saturation and thalamocortical isolation during propofol anesthesia in humans. Science Translational Medicine. 2013;5:208ra148. doi: 10.1126/scitranslmed.3006007.
- Purdon PL, Pierce ET, Mukamel EA, Prerau MJ, Walsh JL, Wong KF, Salazar-Gomez AF, Harrell PG, Sampson AL, Cimenser A, Ching S, Kopell NJ, Tavares-Stoeckel C, Habeeb K, Merhar R, Brown EN. Electroencephalogram signatures of loss and recovery of consciousness from propofol. Proceedings of the National Academy of Sciences of USA. 2013;110:E1142–E1151. doi: 10.1073/pnas.1221180110.
- Rabbitts JA, Groenewald CB, Moriarty JP, Flick R. Epidemiology of ambulatory anesthesia for children in the United States: 2006 and 1996. Anesthesia and Analgesia. 2010;111:1011–1015. doi: 10.1213/ANE.0b013e3181ee8479.
- Semple BD, Blomgren K, Gimlin K, Ferriero DM, Noble-Haeusslein LJ. Brain development in rodents and humans: identifying benchmarks of maturation and vulnerability to injury across species. Progress in Neurobiology. 2013;106–107:1–16. doi: 10.1016/j.pneurobio.2013.04.001.
- Sury MR, Worley A, Boyd SG. Age-related changes in EEG power spectra in infants during sevoflurane wash-out. British Journal of Anaesthesia. 2014;112:686–694. doi: 10.1093/bja/aet409.
- Tau GZ, Peterson BS. Normal development of brain circuits. Neuropsychopharmacology. 2010;35:147–168. doi: 10.1038/npp.2009.115.
- Vijayan S, Ching S, Purdon PL, Brown EN, Kopell NJ. Thalamocortical mechanisms for the anteriorization of Α rhythms during propofol-induced unconsciousness. The Journal of Neuroscience. 2013;33:11070–11075. doi: 10.1523/JNEUROSCI.5670-12.2013.
- Vizuete JA, Pillay S, Ropella KM, Hudetz AG. Graded defragmentation of cortical neuronal firing during recovery of consciousness in rats. Neuroscience. 2014;275:340–351. doi: 10.1016/j.neuroscience.2014.06.018.
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