Breakdown of within- and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness.
Adolescent; Adult; Conscious Sedation/methods; Consciousness/drug effects/physiology; Deep Sedation/methods; Female; Humans; Magnetic Resonance Imaging/methods; Male; Nerve Net/drug effects/physiology; Propofol/pharmacology; Rest/physiology; Unconsciousness/chemically induced/physiopathology; Young Adult
Abstract :
[en] BACKGROUND: Mechanisms of anesthesia-induced loss of consciousness remain poorly understood. Resting-state functional magnetic resonance imaging allows investigating whole-brain connectivity changes during pharmacological modulation of the level of consciousness. METHODS: Low-frequency spontaneous blood oxygen level-dependent fluctuations were measured in 19 healthy volunteers during wakefulness, mild sedation, deep sedation with clinical unconsciousness, and subsequent recovery of consciousness. RESULTS: Propofol-induced decrease in consciousness linearly correlates with decreased corticocortical and thalamocortical connectivity in frontoparietal networks (i.e., default- and executive-control networks). Furthermore, during propofol-induced unconsciousness, a negative correlation was identified between thalamic and cortical activity in these networks. Finally, negative correlations between default network and lateral frontoparietal cortices activity, present during wakefulness, decreased proportionally to propofol-induced loss of consciousness. In contrast, connectivity was globally preserved in low-level sensory cortices, (i.e., in auditory and visual networks across sedation stages). This was paired with preserved thalamocortical connectivity in these networks. Rather, waning of consciousness was associated with a loss of cross-modal interactions between visual and auditory networks. CONCLUSIONS: Our results shed light on the functional significance of spontaneous brain activity fluctuations observed in functional magnetic resonance imaging. They suggest that propofol-induced unconsciousness could be linked to a breakdown of cerebral temporal architecture that modifies both within- and between-network connectivity and thus prevents communication between low-level sensory and higher-order frontoparietal cortices, thought to be necessary for perception of external stimuli. They emphasize the importance of thalamocortical connectivity in higher-order cognitive brain networks in the genesis of conscious perception.
Research Center/Unit :
GIGA CRC (Cyclotron Research Center) In vivo Imaging-Aging & Memory - ULiège
Disciplines :
Neurology
Author, co-author :
Boveroux, Pierre ; Centre Hospitalier Universitaire de Liège - CHU > Anesthésie et réanimation
Vanhaudenhuyse, Audrey ; Université de Liège - ULiège > Centre de recherches du cyclotron > Coma Science Group
Bruno, Marie-Aurélie ; Université de Liège - ULiège > Centre de recherches du cyclotron > Coma Science Group
Noirhomme, Quentin ; Université de Liège - ULiège > Centre de recherches du cyclotron
Lauwick, Séverine ; Centre Hospitalier Universitaire de Liège - CHU > Anesthésie et réanimation
Luxen, André ; Université de Liège - ULiège > Centre de recherches du cyclotron Département de chimie (sciences) > Chimie organique de synthèse - Centre de recherches du cyclotron
Degueldre, Christian ; Université de Liège - ULiège > Centre de recherches du cyclotron
Plenevaux, Alain ; Université de Liège - ULiège > Centre de recherches du cyclotron
Schnakers, Caroline ; Université de Liège - ULiège > Centre de recherches du cyclotron
Phillips, Christophe ; Université de Liège - ULiège > Centre de recherches du cyclotron
Brichant, Jean-François ; Université de Liège - ULiège > Département des sciences cliniques > Anesthésie et réanimation
Bonhomme, Vincent ; Centre Hospitalier Universitaire de Liège - CHU > Anesthésie et réanimation
Maquet, Pierre ; Université de Liège - ULiège > Centre de reherches du cyclotron > Neurologie Sart Tilman
Greicius, Michael D
Laureys, Steven ; Université de Liège - ULiège > Centre de recherches du cyclotron - Département des sciences cliniques
Boly, Mélanie ; Université de Liège - ULiège > Centre de recherches du cyclotron - Coma group Département des sciences cliniques > Neurologie
Breakdown of within- and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness.
Publication date :
2010
Journal title :
Anesthesiology
ISSN :
0003-3022
eISSN :
1528-1175
Publisher :
Lippincott Williams & Wilkins, Philadelphia, United States - Pennsylvania
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
Campagna JA, Miller KW, Forman SA: Mechanisms of actions of inhaled anesthetics. N Engl J Med 2003; 348: 2110-24
Collins JG, Kendig JJ, Mason P: Anesthetic actions within the spinal cord: Contributions to the state of general anesthesia. Trends Neurosci 1995; 18:549-53
Angel A: Central neuronal pathways and the process of anaesthesia. Br J Anaesth 1993; 71:148-63
Antognini JF, Wang XW, Carstens E: Isoflurane action in the spinal cord blunts electroencephalographic and tha-lamic-reticular formation responses to noxious stimulation in goats. ANESTHESIOLOGY 2000; 92:559-66
Heinke W, Schwarzbauer C: Subanesthetic isoflurane affects task-induced brain activation in a highly specific manner: A functional magnetic resonance imaging study. ANESTHESIOLOGY 2001; 94:973-81
Alkire MT, Haier RJ, Fallon JH: Toward a unified theory of narcosis: Brain imaging evidence for a thalamocortical switch as the neurophysiologic basis of anesthetic-induced unconsciousness. Conscious Cogn 2000; 9:370-86
Franks NP: General anaesthesia: From molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci 2008; 9:370-86
Velly LJ, Rey MF, Bruder NJ, Gouvitsos FA, Witjas T, Regis JM, Peragut JC, Gouin FM: Differential dynamic of action on cortical and subcortical structures of anesthetic agents during induction of anesthesia. ANESTHESIOLOGY 2007; 107: 202-12
Alkire MT, Miller J: General anesthesia and the neural correlates of consciousness. Prog Brain Res 2005; 150: 229-44
White NS, Alkire MT: Impaired thalamocortical connectivity in humans during general-anesthetic-induced unconsciousness. Neuroimage 2003; 19:402-11
John ER, Prichep LS, Kox W, Valdés-Sosa P, Bosch-Bayard J, Aubert E, Tom M, di Michele F, Gugino LD: Invariant reversible QEEG effects of anesthetics. Conscious Cogn 2001; 10:165-83
Martuzzi R, Ramani R, Qiu M, Rajeevan N, Constable RT: Functional connectivity and alterations in baseline brain state in humans. Neuroimage 2010; 49:823-34
Deshpande G, Kerssens C, Sebel PS, Hu X: Altered local coherence in the default mode network due to sevoflurane anesthesia. Brain Res 2010; 1318:110-21
Goodman SJ, Mann PE: Reticular and thalamic multiple unit activity during wakefulness, sleep and anesthesia. Exp Neurol 1967; 19:11-24
Keifer JC, Baghdoyan HA, Lydic R: Pontine cholinergic mechanisms modulate the cortical electroencephalo-graphic spindles of halothane anesthesia. ANESTHESIOLOGY 1996; 84:945-54
Eikermann M, Fassbender P, Zaremba S, Jordan AS, Rosow C, Malhotra A, Chamberlin NL: Pentobarbital dose-depen-dently increases respiratory genioglossus muscle activity while impairing diaphragmatic function in anesthetized rats. ANESTHESIOLOGY 2009; 110:1327-34
Mashour GA: Cognitive unbinding in sleep and anesthesia. Science 2005; 310:1768-9
Baars BJ, Ramsøy TZ, Laureys S: Brain, conscious experience and the observing self. Trends Neurosci 2003; 26: 671-5
Fiset P, Paus T, Daloze T, Plourde G, Meuret P, Bonhomme V, Hajj-Ali N, Backman SB, Evans AC: Brain mechanisms of propofol-induced loss of consciousness in humans: A positron emission tomographic study. J Neurosci 1999; 19:5506-13
Boly M, Phillips C, Balteau E, Schnakers C, Degueldre C, Moonen G, Luxen A, Peigneux P, Faymonville ME, Maquet P, Laureys S: Consciousness and cerebral baseline activity fluctuations. Hum Brain Mapp 2008; 29:868-74
Boly M, Phillips C, Tshibanda L, Vanhaudenhuyse A, Scha-bus M, Dang-Vu TT, Moonen G, Hustinx R, Maquet P, Laureys S: Intrinsic brain activity in altered states of consciousness: How conscious is the default mode of brain function? Ann N Y Acad Sci 2008; 1129:119-29
Gusnard DA, Raichle ME, Raichle ME: Searching for a baseline: Functional imaging and the resting human brain. Nat Rev Neurosci 2001; 2:685-94
Mason MF, Norton MI, Van Horn JD, Wegner DM, Grafton ST, Macrae CN: Wandering minds: The default network and stimulus-independent thought. Science 2007; 315:393-5
Lamme VA: Towards a true neural stance on consciousness. Trends Cogn Sci 2006; 10:494-501
Fox MD, Raichle ME: Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 2007; 8:700-11
Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF: Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci \USA 2006; 103:13848-53
Morcom AM, Fletcher PC: Does the brain have a baseline? Why we should be resisting a rest. Neuroimage 2007; 37:1073-82
Vincent JL, Patel GH, Fox MD, Snyder AZ, Baker JT, Van Essen DC, Zempel JM, Snyder LH, Corbetta M, Raichle ME: Intrinsic functional architecture in the anaesthetized monkey brain. Nature 2007; 447:83-6
Horovitz SG, Fukunaga M, de Zwart JA, van Gelderen P, Fulton SC, Balkin TJ, Duyn JH: Low frequency BOLD fluctuations during resting wakefulness and light sleep: A simultaneous EEG-fMRI study. Hum Brain Mapp 2008; 29: 671-82
Tononi G: Sleep and dreaming, The Neurology of Consciousness: Cognitive Neuroscience and Neuropathology. Edited by Laureys S, Tononi G. London, Academic Press-Elsevier, 2009, pp 89-107
Soddu A, Boly M, Nir Y, Noirhomme Q, Vanhaudenhuyse A, Demertzi A, Arzi A, Ovadia S, Stanziano M, Papa M, Laureys S, Malach R: Reaching across the abyss: Recent advances in functional magnetic resonance imaging and their potential relevance to disorders of consciousness. Prog Brain Res 2009; 177:261-74
Marsh B, White M, Morton N, Kenny GN: Pharmacokinetic model driven infusion of propofol in children. Br J Anaesth 1991; 67:41-8
Ramsay MA, Savege TM, Simpson BR, Goodwin R: Controlled sedation with alphaxalone-alphadolone. Br Med J 1974; 2:656-9
Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME: The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 2005; 102:9673-8
Greicius MD, Srivastava G, Reiss AL, Menon V: Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI. Proc Natl Acad Sci USA 2004; 101:4637-42
Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD: Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 2007; 27:2349-56
Eckert MA, Kamdar NV, Chang CE, Beckmann CF, Greicius MD, Menon V: A cross-modal system linking primary auditory and visual cortices: Evidence from intrinsic fMRI connectivity analysis. Hum Brain Mapp 2008; 29:848-57
Fransson P: Spontaneous low-frequency BOLD signal fluctuations: An fMRI investigation of the resting-state default mode of brain function hypothesis. Hum Brain Mapp 2005; 26:15-29
N'Kaoua B, Veron AL, Lespinet VC, Claverie B, Sztark F: Time course of cognitive recovery after propofol anaesthesia: A level of processing approach. J Clin Exp Neuro-psychol 2002; 24:713-9
Vanhaudenhuyse A, Noirhomme Q, Tshibanda LJ, Bruno MA, Boveroux P, Schnakers C, Soddu A, Perlbarg V, Le-doux D, Brichant JF, Moonen G, Maquet P, Greicius MD, Laureys S, Boly M: Default network connectivity reflects the level of consciousness in non-communicative braindamaged patients. Brain 2010; 133:161-71
Boly M, Balteau E, Schnakers C, Degueldre C, Moonen G, Luxen A, Phillips C, Peigneux P, Maquet P, Laureys S: Baseline brain activity fluctuations predict somatosensory perception in humans. Proc Natl Acad Sci USA 2007; 104:12187-92
Peigneux P, Orban P, Balteau E, Degueldre C, Luxen A, Laureys S, Maquet P: Offline persistence of memory-related cerebral activity during active wakefulness. PLoS Biol 2006; 4:e100
Boly M, Tshibanda L, Vanhaudenhuyse A, Noirhomme Q, Schnakers C, Ledoux D, Boveroux P, Garweg C, Lamber-mont B, Phillips C, Luxen A, Moonen G, Bassetti C, Maquet P, Laureys S: Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient. Hum Brain Mapp 2009; 30: 2393-400
Mashour GA: Integrating the science of consciousness and anesthesia. Anesth Analg 2006; 103:975-82
Mashour GA: Consciousness unbound: Toward a paradigm of general anesthesia. ANESTHESIOLOGY 2004; 100:428-33
Vahle-Hinz C, Detsch O, Siemers M, Kochs E: Contributions of GABAergic and glutamatergic mechanisms to isoflurane-induced suppression of thalamic somatosensory information transfer. Exp Brain Res 2007; 176:159-72
Kaisti KK, Metsahonkala L, Teras M, Oikonen V, Aalto S, Jaaskelainen S, Hinkka S, Scheinin H: Effects of surgical levels of propofol and sevoflurane anesthesia on cerebral blood flow in healthy subjects studied with positron emission tomography. ANESTHESIOLOGY 2002; 96:1358-70
Veselis RA, Feshchenko VA, Reinsel RA, Dnistrian AM, Beattie B, Akhurst TJ: Thiopental and propofol affect different regions of the brain at similar pharmacologic effects. Anesth Analg 2004; 99:399-408
Massimini M, Ferrarelli F, Huber R, Esser SK, Singh H, Tononi G: Breakdown of cortical effective connectivity during sleep. Science 2005; 309:2228-32
John ER, Prichep LS: The anesthetic cascade: A theory of how anesthesia suppresses consciousness. ANESTHESIOLOGY 2005; 102:447-71
Guillery RW, Sherman SM: Thalamic relay functions and their role in corticocortical communication: Generalizations from the visual system. Neuron 2002; 33:163-75
Lu J, Nelson LE, Franks N, Maze M, Chamberlin NL, Saper CB: Role of endogenous sleep-wake and analgesic systems in anesthesia. J Comp Neurol 2008; 508:648-62
Långsjö JW, Maksimow A, Salmi E, Kaisti K, Aalto S, Oikonen V, Hinkka S, Aantaa R, Sipilä H, Viljanen T, Parkkola R, Scheinin H: S-ketamine anesthesia increases cerebral blood flow in excess of the metabolic needs in humans. ANESTHESIOLOGY 2005; 103:258-68
Laureys S: The neural correlate of (un)awareness: Lessons from the vegetative state. Trends Cogn Sci 2005; 9:556-9
Plourde G, Belin P, Chartrand D, Fiset P, Backman SB, Xie G, Zatorre RJ: Cortical processing of complex auditory stimuli during alterations of consciousness with the general anesthetic propofol. ANESTHESIOLOGY 2006; 104:448-57
Baars BJ. A Cognitive Theory of Consciousness. New York, Cambridge University Press, 1988, pp 1-70
Greicius MD, Krasnow B, Reiss AL, Menon V: Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proc Natl Acad Sci \USA 2003; 100:253-8
Alkire MT: General anesthesia and consciousness, The Neurology of Consciousness: Cognitive Neuroscience and Neuropathology. Edited by Laureys S, Tononi G. London, Academic Press-Elsevier, 2009, pp 118-34
Murphy K, Birn RM, Handwerker DA, Jones TB, Bandettini PA: The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? Neuroimage 2009; 44:893-905
Fox MD, Zhang D, Snyder AZ, Raichle ME: The global signal and observed anticorrelated resting state brain networks. J Neurophysiol 2009; 101:3270-83
Ying SW, Goldstein PA: Propofol-block of SK channels in reticular thalamic neurons enhances GABAergic inhibition in relay neurons. J Neurophysiol 2005; 93:1935-48
Zecharia AY, Nelson LE, Gent TC, Schumacher M, Jurd R, Rudolph U, Brickley SG, Maze M, Franks NP: The involvement of hypothalamic sleep pathways in general anesthesia: Testing the hypothesis using the GABAA receptor beta3N265M knock-in mouse. J Neurosci 2009; 29:2177-87
Nelson LE, Guo TZ, Lu J, Saper CB, Franks NP, Maze M: The sedative component of anesthesia is mediated by GABA(A) receptors in an endogenous sleep pathway. Nat Neurosci 2002; 5:979-84
Englot DJ, Modi B, Mishra AM, DeSalvo M, Hyder F, Blu-menfeld H: Cortical deactivation induced by subcortical network dysfunction in limbic seizures. J Neurosci 2009; 29:13006-18
Czisch M, Wehrle R, Kaufmann C, Wetter TC, Holsboer F, Pollmächer T, Auer DP: Functional MRI during sleep BOLD signal decreases and their electrophysiological correlates. Eur J Neurosci 2004; 20:566-74
Czisch M, Wetter TC, Kaufmann C, Pollm̈acher T, Hols-boer F, Auer DP: Altered processing of acoustic stimuli during sleep: Reduced auditory activation and visual deac-tivation detected by a combined fMRI/EEG study. Neuro-image 2002; 16:251-8
Bokor H, Frère SG, Eyre MD, Slézia A, Ulbert I, Lüthi A, Acśady L: Selective GABAergic control of higher-order thalamic relays. Neuron 2005; 45:929-40
Alkire MT, Asher CD, Franciscus AM, Hahn EL: Thalamic micro-infusion of antibody to a voltage-gated potassium channel restores consciousness during anesthesia. ANESTHESIOLOGY 2009; 110:766-73
Kochs E, Bischoff P, Pichlmeier U, Schulte am Esch J: Surgical stimulation induces changes in brain electrical activity during isoflurane/nitrous oxide anesthesia. A topographic electroen-cephalographic analysis. ANESTHESIOLOGY 1994; 80:1026-34
Jones EG: The thalamic matrix and thalamocortical synchrony. Trends Neurosci 2001; 24:595-601
Beckmann CF, DeLuca M, Devlin JT, Smith SM: Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 2005; 360:1001-13
Thirion B, Pinel P, Mériaux S, Roche A, Dehaene S, Poline JB: Analysis of a large fMRI cohort: Statistical and methodological issues for group analyses. Neuroimage 2007; 35: 105-20
Dueck MH, Petzke F, Gerbershagen HJ, Paul M, Hessel-mann V, Girnus R, Krug B, Sorger B, Goebel R, Lehrke R, Sturm V, Boerner U: Propofol attenuates responses of the auditory cortex to acoustic stimulation in a dose-dependent manner: A FMRI study. Acta Anaesthesiol Scand 2005; 49:784-91
Penny WD, Holmes AJ: Random effects analysis, Statistical Parametric Mapping: The Analysis of Functional Brain Images. Edited by Friston K, Ashburner J, Kiebel S, Nichols T, Penny W. London, Academic Press 2006, pp 156-65
Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A: Neurophysiological investigation of the basis of the fMRI signal. Nature 2001; 412:150-7
Logothetis NK: The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. Philos Trans R Soc Lond B Biol Sci 2002; 357:1003-37
Shmuel A, Augath M, Oeltermann A, Logothetis NK: Neg-ative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat Neurosci 2006; 9:569-77
Goense JB, Logothetis NK: Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr Biol 2008; 18:631-40
Nir Y, Fisch L, Mukamel R, Gelbard-Sagiv H, Arieli A, Fried I, Malach R: Coupling between neuronal firing rate, gamma LFP, and BOLD fMRI is related to interneuronal correlations. Curr Biol 2007; 17:1275-85
Veselis RA, Feshchenko VA, Reinsel RA, Beattie B, Akhurst TJ: Propofol and thiopental do not interfere with regional cerebral blood flow response at sedative concentrations. ANESTHESIOLOGY 2005; 102:26-34
Johnston AJ, Steiner LA, Chatfield DA, Coleman MR, Coles JP, Al-Rawi PG, Menon DK, Gupta AK: Effects of propofol on cerebral oxygenation and metabolism after head injury. Br J Anaesth 2003; 91:781-6
Birn RM, Diamond JB, Smith MA, Bandettini PA: Separating respiratory-variation-related fluctuations from neuronal-ac-tivity-related fluctuations in fMRI. Neuroimage 2006; 31: 1536-48
Wise RG, Ide K, Poulin MJ, Tracey I: Resting fluctuations in arterial carbon dioxide induce significant low frequency variations in BOLD signal. Neuroimage 2004; 21:1652-64
Corfield DR, Murphy K, Josephs O, Adams L, Turner R: Does hypercapnia-induced cerebral vasodilation modulate the hemodynamic response to neural activation? Neuroim-age 2001; 13:1207-11
Chang C, Glover GH: Effects of model-based physiological noise correction on default mode network anti-correlations and correlations. Neuroimage 2009; 47:1448-59
Rodriguez RA, Hall LE, Duggan S, Splinter WM: The bispec-tral index does not correlate with clinical signs of inhala-tional anesthesia during sevoflurane induction and arousal in children. Can J Anaesth 2004; 51:472-80
Allada R: An emerging link between general anesthesia and sleep. Proc Natl Acad Sci \USA 2008; 105:2257-8
Kelz MB, Sun Y, Chen J, Cheng Meng Q, Moore JT, Veasey SC, Dixon S, Thornton M, Funato H, Yanagisawa M: An essential role for orexins in emergence from general anesthesia. Proc Natl Acad Sci \USA 2008; 105:1309-14
Honey CJ, Sporns O: Dynamical consequences of lesions in cortical networks. Hum Brain Mapp 2008; 29:802-9
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.
Boly M, Massimini M, Tononi G: Theoretical approaches to the diagnosis of altered states of consciousness. Prog Brain Res 2009; 177:383-98
Similar publications
Sorry the service is unavailable at the moment. Please try again later.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.
