Brain Connectivity in Disorders of Consciousness

The last 10 years witnessed a considerable increase in our knowledge of brain function in survivors to severe brain injuries with disorders of consciousness (DOC). At the same time, a growing interest developed for the use of functional neuroimaging as a new diagnostic tool in these patients. In this context, particular attention has been devoted to connectivity studies-as these, more than measures of brain metabolism, may be more appropriate to capture the dynamics of large populations of neurons. Here, we will review the pros and cons of various connectivity methods as potential diagnostic tools in brain-damaged patients with DOC. We will also discuss the relevance of the study of the level versus the contents of consciousness in this context.

[1]  T. Gunter,et al.  Sequential Effects of Increasing Propofol Sedation on Frontal and Temporal Cortices as Indexed by Auditory Event-related Potentials , 2004, Anesthesiology.

[2]  Anthony G Hudetz,et al.  General Anesthesia and Human Brain Connectivity , 2012, Brain Connect..

[3]  J. Changeux,et al.  Opinion TRENDS in Cognitive Sciences Vol.10 No.5 May 2006 Conscious, preconscious, and subliminal processing: a testable taxonomy , 2022 .

[4]  A. Engel,et al.  Cortical Hypersynchrony Predicts Breakdown of Sensory Processing during Loss of Consciousness , 2011, Current Biology.

[5]  G. Tononi,et al.  Consciousness and Anesthesia , 2008, Science.

[6]  Steven Laureys,et al.  Brain function in coma, vegetative state, and related disorders , 2004, The Lancet Neurology.

[7]  G. Tononi,et al.  Breakdown of Cortical Effective Connectivity During Sleep , 2005, Science.

[8]  Matthew H. Davis,et al.  Towards the routine use of brain imaging to aid the clinical diagnosis of disorders of consciousness. , 2009, Brain : a journal of neurology.

[9]  Karl J. Friston,et al.  Preserved Feedforward But Impaired Top-Down Processes in the Vegetative State , 2011, Science.

[10]  Habib Benali,et al.  CORSICA: correction of structured noise in fMRI by automatic identification of ICA components. , 2007, Magnetic resonance imaging.

[11]  J. Giacino,et al.  The minimally conscious state: Definition and diagnostic criteria , 2002, Neurology.

[12]  Srivas Chennu,et al.  Bedside detection of awareness in the vegetative state: a cohort study , 2011, The Lancet.

[13]  R. Newcombe Consciousness , 1996, Journal of Clinical Neuroscience.

[14]  R. Todd Constable,et al.  Functional connectivity and alterations in baseline brain state in humans , 2010, NeuroImage.

[15]  Steven Laureys,et al.  Perception of pain in the minimally conscious state with PET activation: an observational study , 2008, The Lancet Neurology.

[16]  Á. Pascual-Leone,et al.  Noninvasive human brain stimulation. , 2007, Annual review of biomedical engineering.

[17]  M. Czisch,et al.  Development of the brain's default mode network from wakefulness to slow wave sleep. , 2011, Cerebral cortex.

[18]  M. Boly,et al.  Willful modulation of brain activity in disorders of consciousness. , 2010, The New England journal of medicine.

[19]  Karl J. Friston,et al.  Evoked brain responses are generated by feedback loops , 2007, Proceedings of the National Academy of Sciences.

[20]  Adrian M. Owen,et al.  Diffusion weighted imaging distinguishes the vegetative state from the minimally conscious state , 2011, NeuroImage.

[21]  M. Boly,et al.  Diagnostic accuracy of the vegetative and minimally conscious state: Clinical consensus versus standardized neurobehavioral assessment , 2009, BMC neurology.

[22]  Satoru Miyauchi,et al.  Connectivity pattern changes in default-mode network with deep non-REM and REM sleep , 2011, Neuroscience Research.

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

[24]  M. Mataró,et al.  Long-term effects of bilateral frontal brain lesion: 60 years after injury with an iron bar. , 2001, Archives of neurology.

[25]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[26]  V. Lamme Towards a true neural stance on consciousness , 2006, Trends in Cognitive Sciences.

[27]  M. Boly,et al.  Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient , 2009, Human brain mapping.

[28]  M. Boly,et al.  Consciousness and cerebral baseline activity fluctuations , 2008, Human brain mapping.

[29]  N. Schiff,et al.  Dissociations between behavioural and functional magnetic resonance imaging-based evaluations of cognitive function after brain injury. , 2011, Brain : a journal of neurology.

[30]  I. Fried,et al.  Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex , 2008, Nature Neuroscience.

[31]  Vladimir Litvak,et al.  Artifact correction and source analysis of early electroencephalographic responses evoked by transcranial magnetic stimulation over primary motor cortex , 2007, NeuroImage.

[32]  Karl J. Friston,et al.  The relation of ongoing brain activity , evoked neural responses , and cognition , 2010 .

[33]  G. Tononi,et al.  Triggering sleep slow waves by transcranial magnetic stimulation , 2007, Proceedings of the National Academy of Sciences.

[34]  Schreiber,et al.  Measuring information transfer , 2000, Physical review letters.

[35]  R. Malach,et al.  Reaching across the abyss: recent advances in functional magnetic resonance imaging and their potential relevance to disorders of consciousness. , 2009, Progress in brain research.

[36]  N. Schiff Recovery of consciousness after brain injury: a mesocircuit hypothesis , 2010, Trends in Neurosciences.

[37]  George Zouridakis,et al.  Information Communication Networks in Severe Traumatic Brain Injury , 2010, Brain Topography.

[38]  S H Curry,et al.  Quantitative electroencephalographic evaluation of non-fatal and fatal traumatic coma. , 1998, Electroencephalography and clinical neurophysiology.

[39]  P. Bandettini,et al.  The effect of respiration variations on independent component analysis results of resting state functional connectivity , 2008, Human brain mapping.

[40]  UnCheol Lee,et al.  Preferential Inhibition of Frontal-to-Parietal Feedback Connectivity Is a Neurophysiologic Correlate of General Anesthesia in Surgical Patients , 2011, PloS one.

[41]  J. Kessler,et al.  Massive impairment in executive functions with partial preservation of other cognitive functions: the case of a young patient with severe degeneration of the prefrontal cortex , 2000, Experimental Brain Research.

[42]  M. Boly,et al.  Breakdown of within- and between-network Resting State Functional Magnetic Resonance Imaging Connectivity during Propofol-induced Loss of Consciousness , 2010, Anesthesiology.

[43]  Perrine Ruby,et al.  Odd Sound Processing in the Sleeping Brain , 2008, Journal of Cognitive Neuroscience.

[44]  M. Boly,et al.  Modes and models in disorders of consciousness science. , 2012, Archives italiennes de biologie.

[45]  Peter A. Bandettini,et al.  Integration of motion correction and physiological noise regression in fMRI , 2008, NeuroImage.

[46]  Florin Amzica,et al.  Hypersensitivity of the Anesthesia-Induced Comatose Brain , 2007, The Journal of Neuroscience.

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

[48]  I F Russell Isolated forearm technique. , 1990, Anaesthesia.

[49]  Steven Laureys,et al.  When thoughts become action: An fMRI paradigm to study volitional brain activity in non-communicative brain injured patients , 2007, NeuroImage.

[50]  Katsuyuki Sakai,et al.  Task-specific signal transmission from prefrontal cortex in visual selective attention , 2009, Nature Neuroscience.

[51]  W Vycudilik,et al.  Direct Current Auditory Evoked Potentials During Wakefulness, Anesthesia, and Emergence from Anesthesia , 2001, Anesthesia and analgesia.

[52]  Matthew H. Davis,et al.  Detecting awareness in the vegetative state. , 2006, Science.

[53]  Karl J. Friston,et al.  Forward and backward connections in the brain: A DCM study of functional asymmetries , 2009, NeuroImage.

[54]  M. Boly,et al.  Auditory processing in severely brain injured patients: differences between the minimally conscious state and the persistent vegetative state. , 2004, Archives of neurology.

[55]  G. Tononi An information integration theory of consciousness , 2004, BMC Neuroscience.

[56]  Steven Laureys The neural correlate of (un)awareness: lessons from the vegetative state , 2005, Trends in Cognitive Sciences.

[57]  A. Seth,et al.  Causal density and integrated information as measures of conscious level , 2011, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[58]  J. Changeux,et al.  Ongoing Spontaneous Activity Controls Access to Consciousness: A Neuronal Model for Inattentional Blindness , 2005, PLoS biology.

[59]  Marcello Massimini,et al.  Recovery of cortical effective connectivity and recovery of consciousness in vegetative patients , 2012, Brain : a journal of neurology.

[60]  Steven Laureys,et al.  Resting state activity in patients with disorders of consciousness. , 2011, Functional neurology.

[61]  UnCheol Lee,et al.  The directionality and functional organization of frontoparietal connectivity during consciousness and anesthesia in humans , 2009, Consciousness and Cognition.

[62]  C. Degueldre,et al.  Auditory processing in the vegetative state. , 2000, Brain : a journal of neurology.

[63]  M. Boly,et al.  Granger Causality Analysis of Steady-State Electroencephalographic Signals during Propofol-Induced Anaesthesia , 2012, PloS one.

[64]  G Tononi,et al.  Cortical mechanisms of loss of consciousness: insight from TMS/EEG studies. , 2012, Archives italiennes de biologie.

[65]  Marcello Massimini,et al.  General indices to characterize the electrical response of the cerebral cortex to TMS , 2010, NeuroImage.

[66]  M. Boly,et al.  Brain Connectivity in Pathological and Pharmacological Coma , 2010, Front. Syst. Neurosci..

[67]  Morten Overgaard,et al.  Neural Correlates of Contents and Levels of Consciousness , 2010, Front. Psychology.

[68]  Athena Demertzi,et al.  Identifying the default‐mode component in spatial IC analyses of patients with disorders of consciousness , 2012, Human brain mapping.

[69]  J. Victor,et al.  Power spectra and coherence in the EEG of a vegetative patient with severe asymmetric brain damage , 2000, Clinical Neurophysiology.

[70]  J. Born,et al.  EEG-Guided Transcranial Magnetic Stimulation Reveals Rapid Shifts in Motor Cortical Excitability during the Human Sleep Slow Oscillation , 2012, The Journal of Neuroscience.

[71]  R. Ilmoniemi,et al.  Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity , 1997, Neuroreport.

[72]  Jaan Aru,et al.  Right-frontal slow negative potentials evoked by occipital TMS are reduced in NREM sleep , 2011, Neuroscience Letters.

[73]  Mélanie Boly,et al.  Measuring the fading consciousness in the human brain. , 2011, Current opinion in neurology.

[74]  Olaf Sporns,et al.  Network structure of cerebral cortex shapes functional connectivity on multiple time scales , 2007, Proceedings of the National Academy of Sciences.

[75]  S Laureys,et al.  Cerebral metabolism during vegetative state and after recovery to consciousness , 1999, Journal of neurology, neurosurgery, and psychiatry.

[76]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[77]  C. Koch,et al.  The Neural Correlates of Consciousness , 2008, Annals of the New York Academy of Sciences.

[78]  Axel Cleeremans,et al.  Measuring consciousness: relating behavioural and neurophysiological approaches , 2008, Trends in Cognitive Sciences.

[79]  S. Dehaene,et al.  Brain Dynamics Underlying the Nonlinear Threshold for Access to Consciousness , 2007, PLoS biology.

[80]  S Laureys,et al.  Multimodal neuroimaging in patients with disorders of consciousness showing "functional hemispherectomy". , 2011, Progress in brain research.

[81]  C. Koch,et al.  Are we aware of neural activity in primary visual cortex? , 1995, Nature.

[82]  Steven L. Bressler,et al.  Wiener–Granger Causality: A well established methodology , 2011, NeuroImage.

[83]  G. Tononi,et al.  Source modeling sleep slow waves , 2009, Proceedings of the National Academy of Sciences.

[84]  B. Baars A cognitive theory of consciousness , 1988 .

[85]  Christophe Phillips,et al.  Brain functional integration decreases during propofol-induced loss of consciousness , 2011, NeuroImage.

[86]  A. Braun,et al.  Decoupling of the brain's default mode network during deep sleep , 2009, Proceedings of the National Academy of Sciences.

[87]  Marcello Massimini,et al.  A perturbational approach for evaluating the brain's capacity for consciousness. , 2009, Progress in brain research.

[88]  C. Frith,et al.  The neural correlates of conscious experience: an experimental framework , 1999, Trends in Cognitive Sciences.

[89]  Maxime Bonjean,et al.  “Relevance vector machine” consciousness classifier applied to cerebral metabolism of vegetative and locked-in patients , 2011, NeuroImage.

[90]  Chris D. Frith What Brain Plasticity Reveals About the Nature of Consciousness: Commentary , 2011, Front. Psychology.

[91]  Audny Anke,et al.  Reliability and Diagnostic Characteristics of the JFK Coma Recovery Scale–Revised: Exploring the Influence of Rater's Level of Experience , 2010, The Journal of head trauma rehabilitation.

[92]  Marcello Massimini,et al.  Theoretical approaches to the diagnosis of altered states of consciousness. , 2009, Progress in brain research.

[93]  G. Tononi Consciousness as Integrated Information: a Provisional Manifesto , 2008, The Biological Bulletin.

[94]  S Laureys,et al.  vegetative state , 2008 .

[95]  Gustave Moonen,et al.  Cortical Processing of Noxious Somatosensory Stimuli in the Persistent Vegetative State , 2002, NeuroImage.

[96]  Ross Zafonte,et al.  Assessment scales for disorders of consciousness: evidence-based recommendations for clinical practice and research. , 2010, Archives of physical medicine and rehabilitation.

[97]  Athena Demertzi,et al.  Two Distinct Neuronal Networks Mediate the Awareness of Environment and of Self , 2011, Journal of Cognitive Neuroscience.

[98]  Montserrat Bernabeu,et al.  Combination of diffusion tensor and functional magnetic resonance imaging during recovery from the vegetative state , 2010, BMC neurology.

[99]  M. Brass,et al.  Unconscious determinants of free decisions in the human brain , 2008, Nature Neuroscience.

[100]  G. Tononi,et al.  Breakdown in cortical effective connectivity during midazolam-induced loss of consciousness , 2010, Proceedings of the National Academy of Sciences.

[101]  G Tononi,et al.  Cortical reactivity and effective connectivity during REM sleep in humans , 2010, Cognitive neuroscience.

[102]  Steven Laureys,et al.  Cerebral response to patient's own name in the vegetative and minimally conscious states , 2007, Neurology.

[103]  M. Boly,et al.  Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. , 2010, Brain : a journal of neurology.

[104]  M. Sahani,et al.  Nonlinearities and Contextual Influences in Auditory Cortical Responses Modeled with Multilinear Spectrotemporal Methods , 2008, The Journal of Neuroscience.

[105]  Stanislas Dehaene,et al.  Comment on “Preserved Feedforward But Impaired Top-Down Processes in the Vegetative State” , 2011, Science.

[106]  N. Schiff,et al.  Neurophysiological correlates of persistent vegetative and minimally conscious states , 2005, Neuropsychological rehabilitation.

[107]  I. Fried,et al.  Coupling between Neuronal Firing Rate, Gamma LFP, and BOLD fMRI Is Related to Interneuronal Correlations , 2007, Current Biology.

[108]  G. Tononi,et al.  Dreaming and the brain: from phenomenology to neurophysiology , 2010, Trends in Cognitive Sciences.