Changes in Whole Brain Dynamics and Connectivity Patterns during Sevoflurane- and Propofol-induced Unconsciousness Identified by Functional Magnetic Resonance Imaging
Golkowski, Daniel; Larroque, Stephen Karl; VANHAUDENHUYSE, Audreyet al.
[en] Background: A key feature of the human brain is its capability to adapt flexibly to changing external stimuli. This capability can be eliminated by general anesthesia, a state characterized by unresponsiveness, amnesia, and (most likely) unconsciousness. Previous studies demonstrated decreased connectivity within the thalamus, frontoparietal, and default mode networks during general anesthesia. We hypothesized that these alterations within specific brain networks lead to a change of communication between networks and their temporal dynamics.
Methods: We conducted a pooled spatial independent component analysis of resting-state functional magnetic resonance imaging data obtained from 16 volunteers during propofol and 14 volunteers during sevoflurane general anesthesia that have been previously published. Similar to previous studies, mean z-scores of the resulting spatial maps served as a measure of the activity within a network. Additionally, correlations of associated time courses served as a measure of the connectivity between networks. To analyze the temporal dynamics of between-network connectivity, we computed the correlation matrices during sliding windows of 1 min and applied k-means clustering to the matrices during both general anesthesia and wakefulness.
Results: Within-network activity was decreased in the default mode, attentional, and salience networks during general anesthesia (P < 0.001, range of median changes: –0.34, –0.13). Average between-network connectivity was reduced during general anesthesia (P < 0.001, median change: –0.031). Distinct between-network connectivity patterns for both wakefulness and general anesthesia were observed irrespective of the anesthetic agent (P < 0.001), and there were fewer transitions in between-network connectivity patterns during general anesthesia (P < 0.001, median number of transitions during wakefulness: 4 and during general anesthesia: 0).
Conclusions: These results suggest that (1) higher-order brain regions play a crucial role in the generation of specific between-network connectivity patterns and their dynamics, and (2) the capability to interact with external stimuli is represented by complex between-network connectivity patterns.
Research Center/Unit :
GIGA CRC (Cyclotron Research Center) In vivo Imaging-Aging & Memory - ULiège
Changes in Whole Brain Dynamics and Connectivity Patterns during Sevoflurane- and Propofol-induced Unconsciousness Identified by Functional Magnetic Resonance Imaging
Publication date :
June 2019
Journal title :
Anesthesiology
ISSN :
0003-3022
eISSN :
1528-1175
Publisher :
Lippincott Williams & Wilkins, Philadelphia, United States - Pennsylvania
Lee U, Kim S, Noh GJ, Choi BM, Hwang E, Mashour GA: The directionality and functional organization of frontoparietal connectivity during consciousness and anesthesia in humans. Conscious Cogn 2009; 18:1069-78
Ku SW, Lee U, Noh GJ, Jun IG, Mashour GA: Preferential inhibition of frontal-to-parietal feedback connectivity is a neurophysiologic correlate of general anesthesia in surgical patients. PLoS One 2011; 6:e25155
Jordan D, Ilg R, Riedl V, Schorer A, Grimberg S, Neufang S, Omerovic A, Berger S, Untergehrer G, Preibisch C, Schulz E, Schuster T, Schroter M, Spoormaker V, Zimmer C, Hemmer B, Wohlschlager A, Kochs EF, Schneider G: Simultaneous electroencephalographic and functional magnetic resonance imaging indicate impaired cortical top-down processing in association with anesthetic-induced unconsciousness. Anesthesiology 2013; 119:1031-42
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- A nd between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness. Anesthesiology 2010; 113:1038-53
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. J Neurosci 2010; 30:9095-102
Palanca BJ, Mitra A, Larson-Prior L, Snyder AZ, Avidan MS, Raichle ME: Resting-state functional magnetic resonance imaging correlates of sevoflurane-induced unconsciousness. Anesthesiology 2015; 123:346-56
Ranft A, Golkowski D, Kiel T, Riedl V, Kohl P, Rohrer G, Pientka J, Berger S, Thul A, Maurer M, Preibisch C, Zimmer C, Mashour GA, Kochs EF, Jordan D, Ilg R: Neural correlates of sevoflurane-induced unconsciousness identified by simultaneous functional magnetic resonance imaging and electroencephalography. Anesthesiology 2016; 125:861-72
Bonhomme V, Vanhaudenhuyse A, Demertzi A, Bruno MA, Jaquet O, Bahri MA, Plenevaux A, Boly M, Boveroux P, Soddu A, Brichant JF, Maquet P, Laureys S: Resting-state network-specific breakdown of functional connectivity during ketamine alteration of consciousness in volunteers. Anesthesiology 2016; 125:873-88
Lee U, Ku S, Noh G, Baek S, Choi B, Mashour GA: Disruption of frontal-parietal communication by ketamine, propofol, and sevoflurane. Anesthesiology 2013; 118:1264-75
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 2014; 3:e04499
van den Heuvel MP, Sporns O: Rich-club organization of the human connectome. J Neurosci 2011; 31:15775-86
Vaša F, Shanahan M, Hellyer PJ, Scott G, Cabral J, Leech R: Effects of lesions on synchrony and metastability in cortical networks. Neuroimage 2015; 118:456-67
Alstott J, Breakspear M, Hagmann P, Cammoun L, Sporns O: Modeling the impact of lesions in the human brain. PLoS Comput Biol 2009; 5:e1000408
Gratton C, Nomura EM, Perez F, D'Esposito M: Focal brain lesions to critical locations cause widespread disruption of the modular organization of the brain. J Cogn Neurosci 2012; 24:1275-85
Moon JY, Lee U, Blain-Moraes S, Mashour GA: General relationship of global topology, local dynamics, and directionality in large-scale brain networks. PLoS Comput Biol 2015; 11:e1004225
Schroter MS, Spoormaker VI, Schorer A, Wohlschlager A, Czisch M, Kochs EF, Zimmer C, Hemmer B, Schneider G, Jordan D, Ilg R: Spatiotemporal reconfiguration of large-scale brain functional networks during propofol-induced loss of consciousness. J Neurosci 2012; 32:12832-40
Hudetz AG, Liu X, Pillay S: Dynamic repertoire of intrinsic brain states is reduced in propofol-induced unconsciousness. Brain Connect 2015; 5:10-22
Hutchison RM, Hutchison M, Manning KY, Menon RS, Everling S: Isoflurane induces dose-dependent alterations in the cortical connectivity profiles and dynamic properties of the brain's functional architecture. Hum Brain Mapp 2014; 35:5754-75
Barttfeld P, Uhrig L, Sitt JD, Sigman M, Jarraya B, Dehaene S: Signature of consciousness in the dynamics of resting-state brain activity. Proc Natl Acad Sci USA 2015; 112:887-92
Allen EA, Damaraju E, Plis SM, Erhardt EB, Eichele T, Calhoun VD: Tracking whole-brain connectivity dynamics in the resting state. Cereb Cortex 2014; 24:663-76
Calhoun V: GroupICATv4.0b, 2017. Available at: Http://mialab.mrn.org/software/gift/#. Accessed April 14, 2019
Correa N, Adali T, Calhoun VD: Performance of blind source separation algorithms for fMRI analysis using a group ICA method. Magn Reson Imaging 2007; 25:684-94
Allen EA, Erhardt EB, Damaraju E, Gruner W, Segall JM, Silva RF, Havlicek M, Rachakonda S, Fries J, Kalyanam R, Michael AM, Caprihan A, Turner JA, Eichele T, Adelsheim S, Bryan AD, Bustillo J, Clark VP, Feldstein Ewing SW, Filbey F, Ford CC, Hutchison K, Jung RE, Kiehl KA, Kodituwakku P, Komesu YM, Mayer AR, Pearlson GD, Phillips JP, Sadek JR, Stevens M, Teuscher U, Thoma RJ, Calhoun VD: A baseline for the multivariate comparison of resting-state networks. Front Syst Neurosci 2011; 5:2
Gu Q, Li Z, Han J: Generalized Fisher score for feature selection. arXiv preprint arXiv:1202.3725, 2012.Available at: Https://arxiv.org/ftp/arxiv/papers/1202/1202.3725. pdf. Accessed April 14, 2019
Frohlich H, Chapelle O, Scholkopf B: Feature selection for support vector machines by means of genetic algorithm, tools with artificial intelligence, 2003. Proceedings. 15th ieee international conference on, IEEE, 2003, pp 142-148. Available at: Https://www.researchgate.net/profile/Holger-Froehlich2/publication/221417489-Feature-Selection-for-Support-Vector-Machines-by-Means-of-Genetic-Algorithms/links/0deec53c66ef1ad803000000. pdf. Accessed April 14, 2019
Roffo G, Melzi S, Castellani U, Vinciarelli A: Infinite latent feature selection: A probabilistic latent graph-based ranking approach. arXiv preprint arXiv:1707.07538, 2017. Available at: Http://openaccess. thecvf.com/content-ICCV-2017/papers/Roffo-Infinite-Latent-Feature-ICCV-2017-paper. pdf. Accessed April 14, 2019
Demertzi A, Antonopoulos G, Heine L, Voss HU, Crone JS, de Los Angeles C, Bahri MA, Di Perri C, Vanhaudenhuyse A, Charland-Verville V, Kronbichler M, Trinka E, Phillips C, Gomez F, Tshibanda L, Soddu A, Schiff ND, Whitfield-Gabrieli S, Laureys S: Intrinsic functional connectivity differentiates minimally conscious from unresponsive patients. Brain 2015; 138(pt 9):2619-31
Alkire MT, McReynolds JR, Hahn EL, Trivedi AN: Thalamic microinjection of nicotine reverses sevoflurane-induced loss of righting reflex in the rat. Anesthesiology 2007; 107:264-72
Liang Z, Liu X, Zhang N: Dynamic resting state functional connectivity in awake and anesthetized rodents. Neuroimage 2015; 104:89-99
Franks NP: General anaesthesia: From molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci 2008; 9:370-86
Persson A, d'Argy R, Gillberg PG, Halldin C, Litton JE, Swahn CG, Sedvall G: Autoradiography with saturation experiments of 11C-Ro 15-1788 binding to human brain sections. J Neurosci Methods 1991; 36:53-61
Antkowiak B: How do general anaesthetics work Naturwissenschaften 2001; 88:201-13
Dehaene S, Changeux JP: Experimental and theoretical approaches to conscious processing. Neuron 2011; 70:200-27
van Vugt B, Dagnino B, Vartak D, Safaai H, Panzeri S, Dehaene S, Roelfsema PR: The threshold for conscious report: Signal loss and response bias in visual and frontal cortex. Science 2018; 360:537-42
Dehaene S, Sergent C, Changeux JP: A neuronal network model linking subjective reports and objective physiological data during conscious perception. Proc Natl Acad Sci USA 2003; 100:8520-5
Pal D, Dean JG, Liu T, Li D, Watson CJ, Hudetz AG, Mashour GA: Differential role of prefrontal and parietal cortices in controlling level of consciousness. Curr Biol 2018; 28:2145-2152.e5
Kaisti KK, Langsjo JW, Aalto S, Oikonen V, Sipila H, Teras M, Hinkka S, Metsahonkala L, Scheinin H: Effects of sevoflurane, propofol, and adjunct nitrous oxide on regional cerebral blood flow, oxygen consumption, and blood volume in humans. Anesthesiology 2003; 99:603-13
Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, Boulby PA, Barker GJ, Sillery EL, Sheehan K, Ciccarelli O, Thompson AJ, Brady JM, Matthews PM: Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 2003; 6:750-7
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
Deco G, Kringelbach ML: Metastability and coherence: Extending the communication through coherence hypothesis using a whole-brain computational perspective. Trends Neurosci 2016; 39:125-35
Deco G, Van Hartevelt TJ, Fernandes HM, Stevner A, Kringelbach ML: The most relevant human brain regions for functional connectivity: Evidence for a dynamical workspace of binding nodes from wholebrain computational modelling. Neuroimage 2017; 146:197-210
Di Perri C, Amico E, Heine L, Annen J, Martial C, Larroque SK, Soddu A, Marinazzo D, Laureys S: Multifaceted brain networks reconfiguration in disorders of consciousness uncovered by co-activation patterns. Hum Brain Mapp 2018; 39:89-103
Lemon RN, Edgley SA: Life without a cerebellum. Brain 2010; 133(pt 3):652-4