Fronto-Parietal Connectivity Is a Non-Static Phenomenon with Characteristic Changes during Unconsciousness

Background It has been previously shown that loss of consciousness is associated with a breakdown of dominating fronto-parietal feedback connectivity as assessed by electroencephalogram (EEG) recordings. Structure and strength of network connectivity may change over time. Aim of the current study is to investigate cortico-cortical connectivity at different time intervals during consciousness and unconsciousness. For this purpose, EEG symbolic transfer entropy (STEn) was calculated to indicate cortico-cortical information transfer at different transfer times. Methods The study was performed in 15 male volunteers. 29-channel EEG was recorded during consciousness and propofol-induced unconsciousness. EEG data were analyzed by STEn, which quantifies intensity and directionality of the mutual information flow between two EEG channels. STEn was computed over fronto-parietal channel pair combinations (10 s length, 0.5–45 Hz total bandwidth) to analyze changes of intercortical directional connectivity. Feedback (fronto → parietal) and feedforward (parieto → frontal) connectivity was calculated for transfer times from 25 ms to 250 ms in 5 ms steps. Transfer times leading to maximum directed interaction were identified to detect changes of cortical information transfer (directional connectivity) induced by unconsciousness (p<0.05). Results The current analyses show that fronto-parietal connectivity is a non-static phenomenon. Maximum detected interaction occurs at decreased transfer times during propofol-induced unconsciousness (feedback interaction: 60 ms to 40 ms, p = 0.002; feedforward interaction: 65 ms to 45 ms, p = 0.001). Strength of maximum feedback interaction decreases during unconsciousness (p = 0.026), while no effect of propofol was observed on feedforward interaction. During both consciousness and unconsciousness, intensity of fronto-parietal interaction fluctuates with increasing transfer times. Conclusion Non-stationarity of directional connectivity may play a functional role for cortical network communication as it shows characteristic changes during propofol-induced unconsciousness.

[1]  Alan C. Evans,et al.  Brain Mechanisms of Propofol-Induced Loss of Consciousness in Humans: a Positron Emission Tomographic Study , 1999, The Journal of Neuroscience.

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

[3]  R. Guillery,et al.  Thalamic Relay Functions and Their Role in Corticocortical Communication Generalizations from the Visual System , 2002, Neuron.

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

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

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

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

[8]  W. Singer,et al.  Synchronization of Neural Activity across Cortical Areas Correlates with Conscious Perception , 2007, The Journal of Neuroscience.

[9]  S Laureys,et al.  Intrinsic Brain Activity in Altered States of Consciousness , 2008, Annals of the New York Academy of Sciences.

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

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

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

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

[14]  J. Roca-Dorda,et al.  Effects of propofol anesthesia on nonlinear properties of EEG: Time-lag and embedding dimension , 2009 .

[15]  Fabrice Wendling,et al.  Impaired consciousness during temporal lobe seizures is related to increased long-distance cortical-subcortical synchronization. , 2009, Brain : a journal of neurology.

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

[17]  Catie Chang,et al.  Time–frequency dynamics of resting-state brain connectivity measured with fMRI , 2010, NeuroImage.

[18]  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.

[19]  Xiao-Jing Wang Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[20]  G. Deco,et al.  Emerging concepts for the dynamical organization of resting-state activity in the brain , 2010, Nature Reviews Neuroscience.

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

[22]  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.

[23]  Andreas K. Engel,et al.  Oscillatory Synchronization in Large-Scale Cortical Networks Predicts Perception , 2011, Neuron.

[24]  Jérôme Prado,et al.  Variations of response time in a selective attention task are linked to variations of functional connectivity in the attentional network , 2011, NeuroImage.

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

[26]  Bong Jae Lee,et al.  Propofol and Etomidate Depress Cortical, Thalamic, and Reticular Formation Neurons During Anesthetic-Induced Unconsciousness , 2012, Anesthesia and analgesia.

[27]  Karl J. Friston,et al.  Behavioral / Systems / Cognitive Connectivity Changes Underlying Spectral EEG Changes during Propofol-Induced Loss of Consciousness , 2012 .

[28]  Laura D. Lewis,et al.  Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness , 2012, Proceedings of the National Academy of Sciences.

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

[30]  Enzo Tagliazucchi,et al.  Dynamic BOLD functional connectivity in humans and its electrophysiological correlates , 2012, Front. Hum. Neurosci..

[31]  Ravi S. Menon,et al.  Resting-state connectivity identifies distinct functional networks in macaque cingulate cortex. , 2012, Cerebral cortex.

[32]  Julius Georgiou,et al.  EEG-Based Automatic Classification of ‘Awake’ versus ‘Anesthetized’ State in General Anesthesia Using Granger Causality , 2012, PloS one.

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

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

[35]  Viola Priesemann,et al.  Measuring Information-Transfer Delays , 2013, PloS one.

[36]  Bernhard Hemmer,et al.  Simultaneous Electroencephalographic and Functional Magnetic Resonance Imaging Indicate Impaired Cortical Top–Down Processing in Association with Anesthetic-induced Unconsciousness , 2013, Anesthesiology.