Modulation of the spontaneous hemodynamic response function across levels of consciousness

Functional imaging research has already contributed with several results to the study of neural correlates of consciousness. Apart from task-related activation derived in fMRI, PET based glucose metabolism rate or cerebral blood flow account for a considerable proportion of the study of brain activity under different levels of consciousness. Resting state functional connectivity MRI is playing a crucial role to explore the consciousness related functional integration, successfully complementing PET, another widely used neuroimaging technique. Here, spontaneous hemodynamic response is introduced to characterize resting state brain activity giving information on the local metabolism (neurovascular coupling), and useful to improve the time-resolved activity and connectivity measures based on BOLD fMRI. This voxel-wise measure is then used to investigate the loss of consciousness under Propofol anesthesia and unresponsive wakefulness syndrome. The dysfunction of hemodynamic response in precuneus and posterior cingulate is found to be a common principle underlying loss of consciousness in both conditions. The thalamus appears to be less obviously modulated by Propofol, compared with frontoparietal regions. However, a significant increase in spontaneous thalamic hemodynamic response was found in patients in unresponsive wakefulness syndrome compared with healthy control. Our results ultimately show that anesthesia- or pathology-induced neurovascular coupling could be tracked by modulated spontaneous hemodynamic response derived from resting state fMRI.

[1]  S Laureys,et al.  Restoration of thalamocortical connectivity after recovery from persistent vegetative state , 2000, The Lancet.

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

[3]  Mary Beth Nebel,et al.  Reduction of motion-related artifacts in resting state fMRI using aCompCor , 2014, NeuroImage.

[4]  C. Phillips,et al.  Impaired Effective Cortical Connectivity in Vegetative State: Preliminary Investigation Using PET , 1999, NeuroImage.

[5]  Rodrigo M. Braga,et al.  Echoes of the Brain within the Posterior Cingulate Cortex , 2012, The Journal of Neuroscience.

[6]  Nicholas D. Schiff,et al.  Cortical function in the persistent vegetative state , 1999, Trends in Cognitive Sciences.

[7]  Karl J. Friston,et al.  Topological FDR for neuroimaging , 2010, NeuroImage.

[8]  Daniele Marinazzo,et al.  Hemodynamic response function (HRF) variability confounds resting‐state fMRI functional connectivity , 2018, Magnetic resonance in medicine.

[9]  Nikos K Logothetis,et al.  Interpreting the BOLD signal. , 2004, Annual review of physiology.

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

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

[12]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[13]  Matthew H. Davis,et al.  Using a hierarchical approach to investigate residual auditory cognition in persistent vegetative state. , 2005, Progress in brain research.

[14]  Steven Laureys,et al.  Retrieving the Hemodynamic Response Function in resting state fMRI: Methodology and application , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[15]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

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

[17]  R. Buckner,et al.  Human Brain Mapping 6:373–377(1998) � Event-Related fMRI and the Hemodynamic Response , 2022 .

[18]  A. Dale,et al.  Selective averaging of rapidly presented individual trials using fMRI , 1997, Human brain mapping.

[19]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[20]  N. Nakayama,et al.  Relationship between regional cerebral metabolism and consciousness disturbance in traumatic diffuse brain injury without large focal lesions: an FDG-PET study with statistical parametric mapping analysis , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[21]  X Quan,et al.  Propofol and memory: a study using a process dissociation procedure and functional magnetic resonance imaging , 2013, Anaesthesia.

[22]  N. Volkow,et al.  Association Between Brain Activation and Functional Connectivity. , 2019, Cerebral cortex.

[23]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

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

[25]  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.

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

[27]  Steven Laureys,et al.  Limbic hyperconnectivity in the vegetative state , 2013, Neurology.

[28]  Steven Laureys,et al.  Coma and consciousness: Paradigms (re)framed by neuroimaging , 2012, NeuroImage.

[29]  Steven Laureys,et al.  Prevalence of coma-recovery scale-revised signs of consciousness in patients in minimally conscious state , 2017, Neuropsychological rehabilitation.

[30]  Daniele Marinazzo,et al.  Sensitivity of the resting-state haemodynamic response function estimation to autonomic nervous system fluctuations , 2016, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[31]  Steven Laureys,et al.  Diagnostic precision of PET imaging and functional MRI in disorders of consciousness: a clinical validation study , 2014, The Lancet.

[32]  M. Raichle The brain's default mode network. , 2015, Annual review of neuroscience.

[33]  W. Chai,et al.  Imaging the Effects of Propofol on Human Cerebral Glucose Metabolism Using Positron Emission Tomography , 2008, The Journal of international medical research.

[34]  Sungho Tak,et al.  Dynamic and static contributions of the cerebrovasculature to the resting-state BOLD signal , 2014, NeuroImage.

[35]  M. Lindquist,et al.  Validity and power in hemodynamic response modeling: A comparison study and a new approach , 2007, Human Brain Mapping.

[36]  Guorong Wu,et al.  A blind deconvolution approach to recover effective connectivity brain networks from resting state fMRI data , 2012, Medical Image Anal..

[37]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[38]  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.

[39]  Thomas S. Denney,et al.  Hemodynamic variability in soldiers with trauma: Implications for functional MRI connectivity studies , 2017, NeuroImage: Clinical.

[40]  L. M. Ward,et al.  The thalamic dynamic core theory of conscious experience , 2011, Consciousness and Cognition.

[41]  Steven Laureys,et al.  Neuroimaging activation studies in the vegetative state: predictors of recovery? , 2008, Clinical medicine.

[42]  P. Karunanayaka,et al.  BOLD fMRI in infants under sedation: Comparing the impact of pentobarbital and propofol on auditory and language activation , 2013, Journal of magnetic resonance imaging : JMRI.

[43]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[44]  J. Giacino,et al.  The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. , 2004, Archives of physical medicine and rehabilitation.

[45]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[46]  Martin A. Lindquist,et al.  Modeling the hemodynamic response function in fMRI: Efficiency, bias and mis-modeling , 2009, NeuroImage.

[47]  A. M. Owen,et al.  Response from Menon, Owen and Pickard , 1999, Trends in Cognitive Sciences.

[48]  Athena Demertzi,et al.  Thalamus, Brainstem and Salience Network Connectivity Changes During Propofol-Induced Sedation and Unconsciousness , 2013, Brain Connect..

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

[50]  E. Brown,et al.  Thalamocortical Mechanisms for the Anteriorization of Alpha Rhythms during Propofol-Induced Unconsciousness , 2013, The Journal of Neuroscience.

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

[52]  D. Rangaprakash,et al.  Aberrant hemodynamic responses in autism: Implications for resting state fMRI functional connectivity studies , 2018, NeuroImage: Clinical.

[53]  Gilles Plourde,et al.  Brain imaging in research on anesthetic mechanisms: studies with propofol. , 2005, Progress in brain research.

[54]  Pablo Balenzuela,et al.  Criticality in Large-Scale Brain fMRI Dynamics Unveiled by a Novel Point Process Analysis , 2012, Front. Physio..

[55]  Michael T Alkire,et al.  General anesthesia and the neural correlates of consciousness. , 2005, Progress in brain research.

[56]  Peter Kirsch,et al.  Test–retest reliability of evoked BOLD signals from a cognitive–emotive fMRI test battery , 2012, NeuroImage.

[57]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[58]  Steven Laureys,et al.  Posterior Cingulate Cortex-Related Co-Activation Patterns: A Resting State fMRI Study in Propofol-Induced Loss of Consciousness , 2014, PloS one.

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

[60]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[61]  N. Schiff Central Thalamic Contributions to Arousal Regulation and Neurological Disorders of Consciousness , 2008, Annals of the New York Academy of Sciences.