How hot is the hot zone? Computational modelling clarifies the role of parietal and frontoparietal connectivity during anaesthetic-induced loss of consciousness: Computational modelling of anaesthetic-induced LOC.
[en] In recent years, specific cortical networks have been proposed to be crucial for sustaining consciousness, including the posterior hot zone and frontoparietal resting state networks (RSN). Here, we computationally evaluate the relative contributions of three RSNs - the default mode network (DMN), the salience network (SAL), and the central executive network (CEN) - to consciousness and its loss during propofol anaesthesia. Specifically, we use dynamic causal modelling (DCM) of 10 minutes of high-density EEG recordings (N = 10, 4 males) obtained during behavioural responsiveness, unconsciousness and post-anaesthetic recovery to characterise differences in effective connectivity within frontal areas, the posterior 'hot zone', frontoparietal connections, and between-RSN connections. We estimate - for the first time - a large DCM model (LAR) of resting EEG, combining the three RSNs into a rich club of interconnectivity. Consistent with the hot zone theory, our findings demonstrate reductions in inter-RSN connectivity in the parietal cortex. Within the DMN itself, the strongest reductions are in feed-forward frontoparietal and parietal connections at the precuneus node. Within the SAL and CEN, loss of consciousness generates small increases in bidirectional connectivity. Using novel DCM leave-one-out cross-validation, we show that the most consistent out-of-sample predictions of the state of consciousness come from a key set of frontoparietal connections. This finding also generalises to unseen data collected during post-anaesthetic recovery. Our findings provide new, computational evidence for the importance of the posterior hot zone in explaining the loss of consciousness, highlighting also the distinct role of frontoparietal connectivity in underpinning conscious responsiveness, and consequently, suggest a dissociation between the mechanisms most prominently associated with explaining the contrast between conscious awareness and unconsciousness, and those maintaining consciousness.
Disciplines :
Anesthesia & intensive care
Author, co-author :
Ihalainen, Riku
Gosseries, Olivia ; Université de Liège - ULiège > GIGA Consciousness - Coma Science Group
de Steen, Frederik Van
Raimondo, Federico
Panda, Rajanikant ; Université de Liège - ULiège > GIGA Consciousness - Coma Science Group
Bonhomme, Vincent ; Université de Liège - ULiège > Département des sciences cliniques > Département des sciences cliniques
Marinazzo, Daniele
Bowman, Howard
Laureys, Steven ; Université de Liège - ULiège > GIGA Consciousness - Coma Science Group
Chennu, Srivas
Language :
English
Title :
How hot is the hot zone? Computational modelling clarifies the role of parietal and frontoparietal connectivity during anaesthetic-induced loss of consciousness: Computational modelling of anaesthetic-induced LOC.
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Bibliography
Baars, B.J., In the theatre of consciousness. Global workspace theory, a rigorous scientific theory of consciousness. J. Conscious. Stud. 4:4 (1997), 292–309, 10.1093/acprof:oso/9780195102659.001.1.
Baker, R., Gent, T.C., Yang, Q., Parker, S., Vyssotski, A.L., Wisden, W., …, Franks, N.P., Altered activity in the central medial thalamus precedes changes in the neocortex during transitions into both sleep and propofol anesthesia. J. Neurosci. 34:40 (2014), 13326–13335, 10.1523/JNEUROSCI.1519-14.2014.
Barrett, A.B., Murphy, M., Bruno, M.A., Noirhomme, Q., Boly, M., Laureys, S., Seth, A.K., Granger causality analysis of steady-state electroencephalographic signals during propofol-induced anaesthesia. PLoS ONE, 7(1), 2012, 10.1371/journal.pone.0029072.
Bojak, I., Liley, D.T.J., Modeling the effects of anesthesia on the electroencephalogram. Phys. Rev. E - Statistic., Nonlinear, Soft Matter Phys. 71:4 (2005), 1–22, 10.1103/PhysRevE.71.041902.
Boly, M., Moran, R., Murphy, M., Boveroux, P., Bruno, M.-.A., Noirhomme, Q., …, Friston, K., Connectivity changes underlying spectral EEG changes during propofol-induced loss of consciousness. J. Neurosci. 32:20 (2012), 7082–7090, 10.1523/JNEUROSCI.3769-11.2012.
Boly, M., Phillips, L., Tshibanda, A., Vanhaudenhuyse, M., Schabus, D., Dang-Vu, T.T., Moonen, G., Hustinx, R., …, Laureys, S., Intrinsic brain activity in altered states of consciousness: how conscious is the default mode of brain function?. Ann. N. Y. Acad. Sci. 1129 (2008), 119–129, 10.1196/annals.1417.015.Intrinsic.
Bonhomme, V., Staquet, C., Montupil, J., Defresne, A., Kirsch, M., Martial, C., …, Gosseries, O., General anesthesia: a probe to explore consciousness. Front. Syst. Neurosci., 13(August), 2019, 10.3389/fnsys.2019.00036.
Bor, D., Seth, A.K., Consciousness and the prefrontal parietal network: insights from attention, working memory, and chunking. Front. Psychol. 3:MAR (2012), 1–14, 10.3389/fpsyg.2012.00063.
Boveroux, P., Vanhaudenhuyse, A., Bruno, M.-.A., Noirhomme, Q., Lauwick, S., Luxen, A., …, Boly, M., Breakdown of within- and between-network resting state during propofol-induced loss of consciousness. Anesthesiology 113:5 (2010), 1038–1053.
Chennu, S., Finoia, P., Kamau, E., Allanson, J., Williams, G.B., Monti, M.M., …, Bekinschtein, T.A., Spectral signatures of reorganised brain networks in disorders of consciousness. PLoS Comput. Biol., 10(10), 2014, 10.1371/journal.pcbi.1003887.
Chennu, S., O'Connor, S., Adapa, R., Menon, D.K., Bekinschtein, T.A., Brain connectivity dissociates responsiveness from drug exposure during propofol-induced transitions of consciousness. PLoS Comput. Biol. 12:1 (2016), 1–17, 10.1371/journal.pcbi.1004669.
Cocchi, L., Zalesky, A., Fornito, A., Mattingley, J.B., Dynamic cooperation and competition between brain systems during cognitive control. Trends Cogn. Sci. 17:10 (2013), 493–501, 10.1016/j.tics.2013.08.006.
Crone, J.S., Ladurner, G., Höller, Y., Golaszewski, S., Trinka, E., Kronbichler, M., Deactivation of the default mode network as a marker of impaired consciousness: an fmri study. PLoS ONE, 6(10), 2011, 10.1371/journal.pone.0026373.
Crone, J.S., Lutkenhoff, E.S., Bio, B.J., Laureys, S., Monti, M.M., Testing proposed neuronal models of effective connectivity within the cortico-basal gangliathalamo-cortical loop during loss of consciousness. Cereb. Cortex 27:4 (2017), 2727–2738, 10.1093/cercor/bhw112.
David, O., Harrison, L., Friston, K.J., Modelling event-related responses in the brain. Neuroimage 25:3 (2005), 756–770, 10.1016/j.neuroimage.2004.12.030.
David, O., Kiebel, S.J., Harrison, L.M., Mattout, J., Kilner, J.M., Friston, K.J., Dynamic causal modeling of evoked responses in EEG and MEG. Neuroimage 30:4 (2006), 1255–1272, 10.1016/j.neuroimage.2005.10.045.
Dehaene, S., Changeux, J.-.P., Christen, Y., The global neuronal workspace model of conscious access: from neuronal architectures to clinical applications. Res. Perspect. Neurosci. 18 (2011), 55–84, 10.1007/978-3-642-18015-6.
Dehaene, S., Changeux, J.P., Experimental and theoretical approaches to conscious processing. Neuron 70:2 (2011), 200–227, 10.1016/j.neuron.2011.03.018.
Del Cul, A., Dehaene, S., Reyes, P., Bravo, E., Slachevsky, A., Causal role of prefrontal cortex in the threshold for access to consciousness. Brain 132:9 (2009), 2531–2540, 10.1093/brain/awp111.
Driesen, N.R., McCarthy, G., Bhagwagar, Z., Bloch, M., Calhoun, V., D'Souza, D.C., …, Krystal, J.H., Relationship of resting brain hyperconnectivity and schizophrenia-like symptoms produced by the NMDA receptor antagonist ketamine in humans. Mol. Psychiatry 18:11 (2013), 1199–1204, 10.1038/mp.2012.194.
Fastenrath, M., Friston, K.J., Kiebel, S.J., Dynamical causal modelling for M/EEG: spatial and temporal symmetry constraints. Neuroimage 44:1 (2009), 154–163, 10.1016/j.neuroimage.2008.07.041.
Fernández-Espejo, D., Soddu, A., Cruse, D., Palacios, E.M., Junque, C., Vanhaudenhuyse, A., …, Owen, A.M., A role for the default mode network in the bases of disorders of consciousness. Ann. Neurol. 72:3 (2012), 335–343, 10.1002/ana.23635.
Friston, K.J., Bastos, A., Litvak, V., Stephan, K.E., Fries, P., Moran, R.J., DCM for complex-valued data: cross-spectra, coherence and phase-delays. Neuroimage 59:1 (2012), 439–455, 10.1016/j.neuroimage.2011.07.048.
Friston, K., Mattout, J., Trujillo-Barreto, N., Ashburner, J., Penny, W., Variational free energy and the Laplace approximation. Neuroimage 34:1 (2007), 220–234, 10.1016/j.neuroimage.2006.08.035.
Friston, K., Penny, W., Post hoc Bayesian model selection. Neuroimage 56:4 (2011), 2089–2099, 10.1016/j.neuroimage.2011.03.062.
Friston, Karl J., Functional and effective connectivity: a review. Brain Connect. 1:1 (2011), 13–36, 10.1089/brain.2011.0008.
Friston, Karl J., Litvak, V., Oswal, A., Razi, A., Stephan, K.E., Van Wijk, B.C.M., … Zeidman, P., Bayesian model reduction and empirical Bayes for group (DCM) studies. Neuroimage 128 (2016), 413–431, 10.1016/j.neuroimage.2015.11.015.
Goldenholz, D.M., Ahlfors, S.P., Hämäläinen, M.S., Sharon, D., Ishitobi, M., Vaina, L.M., Stufflebeam, S.M., Mapping the signal-to-noise-ratios of cortical sources in magnetoencephalography and electroencephalography. Hum. Brain Mapp. 30:4 (2009), 1077–1086, 10.1002/hbm.20571.
Guldenmund, P., Gantner, I.S., Baquero, K., Das, T., Demertzi, A., Boveroux, P., …, Soddu, A., Propofol-induced frontal cortex disconnection: a study of resting-state networks, total brain connectivity, and mean BOLD signal oscillation frequencies. Brain Connect. 6:3 (2016), 225–237, 10.1089/brain.2015.0369.
Gurland, J., Tripathi, R.C., A simple approximation for unbiased estimation of the standard deviation. Am. Statistic. 25:4 (1971), 30–32, 10.1080/00031305.1971.10477279.
Heine, L., Soddu, A., Gómez, F., Vanhaudenhuyse, A., Tshibanda, L., Thonnard, M., …, Demertzi, A., Resting state networks and consciousness Alterations of multiple resting state network connectivity in physiological, pharmacological, and pathological consciousness states. Front. Psychol. 3:AUG (2012), 1–12, 10.3389/fpsyg.2012.00295.
Horovitz, S.G., Braun, A.R., Carr, W.S., Picchioni, D., Balkin, T.J., Fukunaga, M., Duyn, J.H., Decoupling of the brain's default mode network during deep sleep. Proc. Natl. Acad. Sci. 106:27 (2009), 11376–11381, 10.1073/pnas.0901435106.
Hutt, A., Longtin, A., Effects of the anesthetic agent propofol on neural populations. Cogn. Neurodyn. 4:1 (2010), 37–59, 10.1007/s11571-009-9092-2.
Jansen, B.H., Rit, V.G., Electroencephalogram and visual evoked potential generation in a mathematical model of coupled cortical columns. Biol. Cybern. 73:4 (1995), 357–366, 10.1007/BF00199471.
Kiebel, S.J., Garrido, M.I., Moran, R.J., Friston, K.J., Dynamic causal modelling for EEG and MEG. Cogn. Neurodyn. 2:2 (2008), 121–136, 10.1007/s11571-008-9038-0.
Koch, C., Massimini, M., Boly, M., Tononi, G., Neural correlates of consciousness: progress and problems. Nat. Rev. Neurosci. 17:5 (2016), 307–321, 10.1038/nrn.2016.22.
Koch, C., Massimini, M., Boly, M., Tononi, G., Posterior and anterior cortex — where is the difference that makes the difference?. Nat. Rev. Neurosci., 17(10), 2016, 10.1038/nrn.2016.105 666–666https://doi.org/.
Långsjö, J.W., Alkire, M.T., Kaskinoro, K., Hayama, H., Maksimow, A., Kaisti, K.K., …, Scheinin, H., Returning from oblivion: imaging the neural core of consciousness. J. Neurosci. 32:14 (2012), 4935–4943, 10.1523/JNEUROSCI.4962-11.2012.
Laureys, S., Goldman, S., Phillips, C., Van Bogaert, P., Aerts, J., Luxen, A., …, Maquet, P., Impaired effective cortical connectivity in vegetative state: preliminary investigation using PET. Neuroimage 9:4 (1999), 377–382, 10.1006/nimg.1998.0414.
Laureys, S., The neural correlate of (un)awareness: lessons from the vegetative state. Trends Cogn. Sci. 9:12 (2005), 556–559, 10.1016/j.tics.2005.10.010.
Laureys, S., Schiff, N.D., Coma and consciousness: paradigms (re)framed by neuroimaging. Neuroimage 61:2 (2012), 478–491, 10.1016/j.neuroimage.2011.12.041.
Lee, M., Baird, B., Gosseries, O., Nieminen, J.O., Boly, M., Postle, B.R., …, Lee, S.W., Connectivity differences between consciousness and unconsciousness in non-rapid eye movement sleep: a TMS–EEG study. Sci. Rep. 9:1 (2019), 1–9, 10.1038/s41598-019-41274-2.
Lee, UnCheol, Kim, S., Noh, G.J., Choi, B.M., Hwang, E., Mashour, G.A, The directionality and functional organization of frontoparietal connectivity during consciousness and anesthesia in humans. Conscious. Cogn. 18:4 (2009), 1069–1078, 10.1016/j.concog.2009.04.004.
Lee, Uncheol, Ku, S., Noh, G., Baek, S., Choi, B., Mashour, G.A, Disruption of frontal-parietal communication by ketamine, propofol, and sevoflurane. Anesthesiology 118:6 (2015), 1264–1275, 10.1097/ALN.0b013e31829103f5.Disruption.
Leech, R., Braga, R., Sharp, D.J., Echoes of the brain within the posterior cingulate cortex. J. Neurosci. 32:1 (2012), 215–222, 10.1523/JNEUROSCI.3689-11.2012.
Litvak, V., Jafarian, A., Zeidman, P., Tibon, R., Henson, R.N., Friston, K., There's no such thing as a “true” model: the challenge of assessing face validity. Conference Proceedings - IEEE International Conference on Systems, Man and Cybernetics, 2019-Octob, 2019, 4403–4408, 10.1109/SMC.2019.8914255.
Liu, X., Lauer, K., Ward, D., Li, S.-.J., Hudetz, A., Differential effects of deep sedation with propofol on the specific and nonspecific thalamocortical systems. Anesthesiology 118:1 (2013), 59–69, 10.1038/jid.2014.371.
Luppi, A.I., Craig, M.M., Finoia, P., Williams, G.B., Naci, L., Menon, D.K., Emmanuel, A., Consciousness-specific dynamic interactions of brain integration and functional diversity. Nat. Commun.(Box 65), 2019, 10.1038/s41467-019-12658-9.
Maksimow, A., Silfverhuth, M., Långsjö, J., Kaskinoro, K., Georgiadis, S., Jääskeläinen, S., Scheinin, H., Directional connectivity between frontal and posterior brain regions is altered with increasing concentrations of propofol. PLoS ONE 9:11 (2014), 1–16, 10.1371/journal.pone.0113616.
Mashour, G.A., Roelfsema, P., Changeux, J.P., Dehaene, S., Conscious processing and the global neuronal workspace hypothesis. Neuron 105:5 (2020), 776–798, 10.1016/j.neuron.2020.01.026.
Moran, R.J., Kiebel, S.J., Stephan, K.E., Reilly, R.B., Daunizeau, J., Friston, K.J., A neural mass model of spectral responses in electrophysiology. Neuroimage 37:3 (2007), 706–720, 10.1016/j.neuroimage.2007.05.032.
Moran, R., Pinotsis, D.A., Friston, K., Neural masses and fields in dynamic causal modelling. Front. Comput. Neurosci. 7:APR 2013 (2013), 1–12, 10.3389/fncom.2013.00057.
Murphy, M., Bruno, M.A., Riedner, B.A., Boveroux, P., Noirhomme, Q., Landsness, E.C., …, Boly, M., Propofol anesthesia and sleep: a high-density EEG study. Sleep(3), 2011, 34, 10.1093/sleep/34.3.283.
Nicolaou, N., Hourris, S., Alexandrou, P., Georgiou, J., EEG-based automatic classification of “awake” versus “anesthetized” state in general anesthesia using granger causality. PLoS ONE, 7(3), 2012, 10.1371/journal.pone.0033869.
Raichle, M.E., Snyder, A.Z., A default mode of brain function: a brief history of an evolving idea. Neuroimage 37:4 (2007), 1083–1090, 10.1016/j.neuroimage.2007.02.041.
Ramsay, M.A.E., Savege, T.M., Simpson, B.R.J., Goodwin, R, Hospital topics controlled sedation with Alphaxalone–Alphadolone. Br. Med. J. 22 (1974), 656–659.
Razi, A., Friston, K.J., The Connected Brain: causality, models, and intrinsic dynamics. IEEE Signal Process. Mag. 33:3 (2016), 14–55, 10.1109/MSP.2015.2482121.
Razi, A., Seghier, M.L., Zhou, Y., McColgan, P., Zeidman, P., Park, H.-.J., …, Friston, K.J., Large-scale DCMs for resting-state fMRI. Network Neurosci., 2017, 10.1162/NETN_a_00015.
Rosa, M.J., Friston, K., Penny, W., Post-hoc selection of dynamic causal models. J. Neurosci. Methods 208:1 (2012), 66–78, 10.1016/j.jneumeth.2012.04.013.
Salin, P.A., Bullier, J., Corticocortical connections in the visual system: structure and function. Physiol. Rev. 75:1 (1995), 107–154, 10.1152/physrev.1995.75.1.107.
Sanders, R.D., Banks, M.I., Darracq, M., Moran, R., Sleigh, J., Gosseries, O., …, Boly, M., Propofol-induced unresponsiveness is associated with impaired feedforward connectivity in cortical hierarchy. Br. J. Anaesth. 121:5 (2018), 1084–1096, 10.1016/j.bja.2018.07.006.
Sarasso, S., Boly, M., Napolitani, M., Gosseries, O., Charland-Verville, V., Casarotto, S., …, Massimini, M., Consciousness and complexity during unresponsiveness induced by propofol, xenon, and ketamine. Curr. Biol. 25:23 (2015), 3099–3105, 10.1016/j.cub.2015.10.014.
Schrouff, J., Perlbarg, V., Boly, M., Marrelec, G., Boveroux, P., Vanhaudenhuyse, A., …, Benali, H., Brain functional integration decreases during propofol-induced loss of consciousness. Neuroimage 57:1 (2011), 198–205, 10.1016/j.neuroimage.2011.04.020.
Sherman, S.M., Guillery, R.W., On the actions that one nerve cell can have on another: distinguishing “drivers” from “modulators. PNAS 95:12 (1998), 7121–7126, 10.1073/pnas.95.12.7121.
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