Preferential Inhibition of Frontal-to-Parietal Feedback Connectivity Is a Neurophysiologic Correlate of General Anesthesia in Surgical Patients

Background The precise mechanism and optimal measure of anesthetic-induced unconsciousness has yet to be elucidated. Preferential inhibition of feedback connectivity from frontal to parietal brain networks is one potential neurophysiologic correlate, but has only been demonstrated in animals or under limited conditions in healthy volunteers. Methods and Findings We recruited eighteen patients presenting for surgery under general anesthesia; electroencephalography of the frontal and parietal regions was acquired during (i) baseline consciousness, (ii) anesthetic induction with propofol or sevoflurane, (iii) general anesthesia, (iv) recovery of consciousness, and (v) post-recovery states. We used two measures of effective connectivity, evolutional map approach and symbolic transfer entropy, to analyze causal interactions of the frontal and parietal regions. The dominant feedback connectivity of the baseline conscious state was inhibited after anesthetic induction and during general anesthesia, resulting in reduced asymmetry of feedback and feedforward connections in the frontoparietal network. Dominant feedback connectivity returned when patients recovered from anesthesia. Both analytic techniques and both classes of anesthetics demonstrated similar results in this heterogeneous population of surgical patients. Conclusions The disruption of dominant feedback connectivity in the frontoparietal network is a common neurophysiologic correlate of general anesthesia across two anesthetic classes and two analytic measures. This study represents a key translational step from the underlying cognitive neuroscience of consciousness to more sophisticated monitoring of anesthetic effects in human surgical patients.

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

[2]  Tao Zhang,et al.  Impairments of behavior, information flow between thalamus and cortex, and prefrontal cortical synaptic plasticity in an animal model of depression , 2011, Brain Research Bulletin.

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

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

[5]  UnCheol Lee,et al.  Dissociable Network Properties of Anesthetic State Transitions , 2011, Anesthesiology.

[6]  Tao Zhang,et al.  Directionality index of neural information flow as a measure of synaptic plasticity in chronic unpredictable stress rats , 2011, Neuroscience Letters.

[7]  D. Menon,et al.  Changes in Resting Neural Connectivity during Propofol Sedation , 2010, PLoS ONE.

[8]  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.

[9]  Gordon Pipa,et al.  Transfer entropy—a model-free measure of effective connectivity for the neurosciences , 2010, Journal of Computational Neuroscience.

[10]  Richard Rogers,et al.  Cortical and Subcortical Connectivity Changes during Decreasing Levels of Consciousness in Humans: A Functional Magnetic Resonance Imaging Study using Propofol , 2010, The Journal of Neuroscience.

[11]  Joachim Gross,et al.  The effect of filtering on Granger causality based multivariate causality measures , 2010, NeuroImage.

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

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

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

[15]  Matthäus Staniek,et al.  Symbolic transfer entropy: inferring directionality in biosignals , 2009, Biomedizinische Technik. Biomedical engineering.

[16]  Anthony G. Hudetz,et al.  Feedback suppression in anesthesia. Is it reversible? , 2009, Consciousness and Cognition.

[17]  George A Mashour,et al.  Processed electroencephalogram in depth of anesthesia monitoring , 2009, Current opinion in anaesthesiology.

[18]  Daniel Chicharro,et al.  Reliable detection of directional couplings using rank statistics. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[19]  Olga A Imas,et al.  Desflurane Selectively Suppresses Long-latency Cortical Neuronal Response to Flash in the Rat , 2009, Anesthesiology.

[20]  C. N. Boehler,et al.  Rapid recurrent processing gates awareness in primary visual cortex , 2008, Proceedings of the National Academy of Sciences.

[21]  Matthäus Staniek,et al.  Symbolic transfer entropy. , 2008, Physical review letters.

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

[23]  Johannes J. Fahrenfort,et al.  Masking Disrupts Reentrant Processing in Human Visual Cortex , 2007, Journal of Cognitive Neuroscience.

[24]  G. Rangarajan,et al.  Mitigating the effects of measurement noise on Granger causality. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[25]  Anthony G. Hudetz,et al.  Suppressing consciousness: Mechanisms of general anesthesia , 2006 .

[26]  Anthony G. Hudetz,et al.  Isoflurane disrupts anterio-posterior phase synchronization of flash-induced field potentials in the rat , 2006, Neuroscience Letters.

[27]  R. Zatorre,et al.  Cortical Processing of Complex Auditory Stimuli during Alterations of Consciousness with the General Anesthetic Propofol , 2006, Anesthesiology.

[28]  Anthony G. Hudetz,et al.  Volatile anesthetics disrupt frontal-posterior recurrent information transfer at gamma frequencies in rat , 2005, Neuroscience Letters.

[29]  L. Nyberg,et al.  Common fronto-parietal activity in attention, memory, and consciousness: Shared demands on integration? , 2005, Consciousness and Cognition.

[30]  Ralf Mrowka,et al.  Directionality of coupling of physiological subsystems: age-related changes of cardiorespiratory interaction during different sleep stages in babies. , 2003, American journal of physiology. Regulatory, integrative and comparative physiology.

[31]  J. Wolpaw,et al.  EMG contamination of EEG: spectral and topographical characteristics , 2003, Clinical Neurophysiology.

[32]  Tony Ro,et al.  Feedback Contributions to Visual Awareness in Human Occipital Cortex , 2003, Current Biology.

[33]  M. Rosenblum,et al.  Identification of coupling direction: application to cardiorespiratory interaction. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[34]  M. Rosenblum,et al.  Detecting direction of coupling in interacting oscillators. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[35]  Á. Pascual-Leone,et al.  Fast Backprojections from the Motion to the Primary Visual Area Necessary for Visual Awareness , 2001, Science.

[36]  V. Lamme,et al.  The distinct modes of vision offered by feedforward and recurrent processing , 2000, Trends in Neurosciences.

[37]  P. Sebel,et al.  Awareness during Anesthesia , 2000, Anesthesiology.

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

[39]  T. Schreiber,et al.  Surrogate time series , 1999, chao-dyn/9909037.

[40]  A. Burkhalter,et al.  Different Balance of Excitation and Inhibition in Forward and Feedback Circuits of Rat Visual Cortex , 1996, The Journal of Neuroscience.

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