Differentiating propofol-induced altered states of consciousness using features of EEG microstates

Abstract Objective In this study, we comprehensively studied alternations of EEG microstates in resting state, light, and deep level of propofol-induced unconsciousness. We further investigated the feasibility of using microstate features for differentiating different consciousness levels. Methods 60-channel EEG was recorded from 31 male subjects in resting, light, and deep anesthesia states. Microstate analysis was performed on each consciousness levels separately. We first identified the optimal number of microstate templates for each consciousness levels and aligned them based on spatial similarity. Then, we extracted features including duration, coverage, and occurrence. Machine learning models including SVM, LDA and Random Forest were employed to classify different consciousness levels using microstate features. Finally, the cortical source of each microstates was analyzed using standardized low-resolution electromagnetic tomography. Results We found that the optimal number of microstates differed in different consciousness levels. 7 common and 2 anesthesia-specific microstates were identified. M4, M5, M1 and M2 were similar to the canonical microstates A to D. Occurrence of M6 and duration of M1, M5 and M7 monotonically decreased with increasing level of consciousness suppression. All three features of the anesthesia-specific microstate M8 significantly decreased with increasing level of anesthesia. The classifiers using microstate features showed a mean accuracy of 85.6% to classify three consciousness levels. Conclusion EEG microstate features significantly altered during propofol-induced unconsciousness, and can be used to distinguish between consciousness levels. Significance Microstate analysis may be a useful tool in deciphering the neural mechanism of propofol-induced anesthesia and provide useful features for quantifying levels of consciousness.

[1]  G. Tononi,et al.  *Both authors contributed equally to this manuscript. , 2022 .

[2]  E R John,et al.  Quantitative EEG changes associated with loss and return of consciousness in healthy adult volunteers anaesthetized with propofol or sevoflurane. , 2001, British journal of anaesthesia.

[3]  George A. Mashour,et al.  Dynamic Cortical Connectivity during General Anesthesia in Healthy Volunteers , 2019, Anesthesiology.

[4]  E. Brown,et al.  General anesthesia and altered states of arousal: a systems neuroscience analysis. , 2011, Annual review of neuroscience.

[5]  S. Jbabdi,et al.  Slow-Wave Activity Saturation and Thalamocortical Isolation During Propofol Anesthesia in Humans , 2013, Science Translational Medicine.

[6]  Lars Kai Hansen,et al.  Microstate EEGlab toolbox: An introductory guide , 2018, bioRxiv.

[7]  N. Morton,et al.  Pharmacokinetic model driven infusion of propofol in children. , 1991, British journal of anaesthesia.

[8]  E. Brown,et al.  Clinical Electroencephalography for Anesthesiologists: Part I Background and Basic Signatures , 2015, Anesthesiology.

[9]  Emery N Brown,et al.  Dexmedetomidine Disrupts the Local and Global Efficiencies of Large-scale Brain Networks , 2017, Anesthesiology.

[10]  T. Koenig,et al.  Brain electric microstates and momentary conscious mind states as building blocks of spontaneous thinking: I. Visual imagery and abstract thoughts. , 1998, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[11]  Thomas Koenig,et al.  EEG microstates as a tool for studying the temporal dynamics of whole-brain neuronal networks: A review , 2017, NeuroImage.

[12]  Adam C. Searleman,et al.  Anesthesia awareness and the bispectral index. , 2008, The New England journal of medicine.

[13]  Srivas Chennu,et al.  Transient Topographical Dynamics of the Electroencephalogram Predict Brain Connectivity and Behavioural Responsiveness During Drowsiness , 2017, Brain Topography.

[14]  Emery N. Brown,et al.  Electroencephalogram signatures of loss and recovery of consciousness from propofol , 2013, Proceedings of the National Academy of Sciences.

[15]  Á. Pascual-Leone,et al.  Microstates in resting-state EEG: Current status and future directions , 2015, Neuroscience & Biobehavioral Reviews.

[16]  UnCheol Lee,et al.  Disruption of Frontal–Parietal Communication by Ketamine, Propofol, and Sevoflurane , 2013, Anesthesiology.

[17]  Thomas Koenig,et al.  A Method to Determine the Presence of Averaged Event-Related Fields Using Randomization Tests , 2010, Brain Topography.

[18]  UnCheol Lee,et al.  Reconfiguration of Network Hub Structure after Propofol-induced Unconsciousness , 2013, Anesthesiology.

[19]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[20]  George A. Mashour,et al.  Cortical dynamics during psychedelic and anesthetized states induced by ketamine , 2019, NeuroImage.

[21]  Denis Brunet,et al.  Topographic ERP Analyses: A Step-by-Step Tutorial Review , 2008, Brain Topography.

[22]  K. Leslie,et al.  For Personal Use. Only Reproduce with Permission from the Lancet , 2022 .

[23]  R. D. Pascual-Marqui,et al.  The EEG microstate topography is predominantly determined by intracortical sources in the alpha band , 2017, NeuroImage.

[24]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[25]  Amir Hussain,et al.  A novel multi-modal machine learning based approach for automatic classification of EEG recordings in dementia , 2019, Neural Networks.

[26]  Fei Yan,et al.  Investigating dynamic functional network patterns after propofol-induced loss of consciousness , 2019, Clinical Neurophysiology.

[27]  Andreas Bender,et al.  Consciousness Indexing and Outcome Prediction with Resting-State EEG in Severe Disorders of Consciousness , 2018, Brain Topography.

[28]  Yamin Li,et al.  Non-Canonical Microstate Becomes Salient in High Density EEG During Propofol-Induced Altered States of Consciousness , 2020, Int. J. Neural Syst..

[29]  Dimitri Van De Ville,et al.  BOLD correlates of EEG topography reveal rapid resting-state network dynamics , 2010, NeuroImage.

[30]  Enzo Tagliazucchi,et al.  Narcoleptic Patients Show Fragmented EEG-Microstructure During Early NREM Sleep , 2014, Brain Topography.

[31]  Gustavo Deco,et al.  Resting brains never rest: computational insights into potential cognitive architectures , 2013, Trends in Neurosciences.

[32]  Dietrich Lehmann,et al.  Millisecond by Millisecond, Year by Year: Normative EEG Microstates and Developmental Stages , 2002, NeuroImage.

[33]  Dietrich Lehmann,et al.  A deviant EEG brain microstate in acute, neuroleptic-naive schizophrenics at rest , 1999, European Archives of Psychiatry and Clinical Neuroscience.

[34]  Dietrich Lehmann,et al.  Classes of Multichannel EEG Microstates in Light and Deep Hypnotic Conditions , 2007, Brain Topography.

[35]  Emery N. Brown,et al.  Tracking brain states under general anesthesia by using global coherence analysis , 2011, Proceedings of the National Academy of Sciences.

[36]  J. Changeux,et al.  Experimental and Theoretical Approaches to Conscious Processing , 2011, Neuron.

[37]  Nai Ding,et al.  Assessing the depth of language processing in patients with disorders of consciousness , 2020, Nature Neuroscience.

[38]  Mercedes Atienza,et al.  Brain Spatial Microstates of Human Spontaneous Alpha Activity in Relaxed Wakefulness, Drowsiness Period, and REM Sleep , 2004, Brain Topography.

[39]  D. Lehmann,et al.  Adaptive segmentation of spontaneous EEG map series into spatially defined microstates. , 1993, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[40]  E Callaway,et al.  Scopolamine effects on visual information processing, attention, and event-related potential map latencies. , 1992, Psychophysiology.

[41]  Javad Haddadnia,et al.  Epileptic seizure detection using cross-bispectrum of electroencephalogram signal , 2019, Seizure.

[42]  Tracy Warbrick,et al.  Spontaneous brain activity and EEG microstates. A novel EEG/fMRI analysis approach to explore resting-state networks , 2010, NeuroImage.

[43]  D Lehmann,et al.  Segments of event-related potential map series reveal landscape changes with visual attention and subjective contours. , 1989, Electroencephalography and clinical neurophysiology.

[44]  D. Lehmann,et al.  Segmentation of brain electrical activity into microstates: model estimation and validation , 1995, IEEE Transactions on Biomedical Engineering.

[45]  Thomas Koenig,et al.  Association Between Resting-State Microstates and Ratings on the Amsterdam Resting-State Questionnaire , 2017, Brain Topography.

[46]  J Mazziotta,et al.  A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[47]  D. Lehmann Multichannel topography of human alpha EEG fields. , 1971, Electroencephalography and clinical neurophysiology.

[48]  D Lehmann,et al.  EEG alpha map series: brain micro-states by space-oriented adaptive segmentation. , 1987, Electroencephalography and clinical neurophysiology.

[49]  E. Brown,et al.  General anesthesia, sleep, and coma. , 2010, The New England journal of medicine.

[50]  E. Brown,et al.  Thalamocortical model for a propofol-induced α-rhythm associated with loss of consciousness , 2010, Proceedings of the National Academy of Sciences.

[51]  Ravi S. Menon,et al.  Resting‐state networks show dynamic functional connectivity in awake humans and anesthetized macaques , 2013, Human brain mapping.

[52]  Wolfgang Skrandies,et al.  The Effect of Stimulation Frequency and Retinal Stimulus Location on Visual Evoked Potential Topography , 2007, Brain Topography.

[53]  V. Feshchenko,et al.  Propofol-Induced Alpha Rhythm , 2004, Neuropsychobiology.

[54]  Christoph M. Michel,et al.  EEG microstates of wakefulness and NREM sleep , 2012, NeuroImage.

[55]  Dietrich Lehmann,et al.  EEG Microstates During Resting Represent Personality Differences , 2011, Brain Topography.