Article

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

University of British Columbia, Canada
PLoS ONE (Impact Factor: 3.53). 10/2011; 6(10):e25155. DOI: 10.1371/journal.pone.0025155
Source: PubMed

ABSTRACT 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.
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.
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.

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    • "Prior preclinical studies of anterior-posterior connectivity in rat brain identified a selective inhibition of frontal-to-posterior transfer entropy in the gamma bandwidth in association with isoflurane-induced unconsciousness (Imas et al., 2005). Our laboratory first demonstrated anesthetic inhibition of frontal-to-parietal connectivity in human volunteers (Lee et al., 2009) and surgical patients (Ku et al., 2011); inhibition of functional, directional, and effective connectivity in frontal-parietal networks in association with propofol-induced unconsciousness has been identified by studies from multiple research groups using multiple analytic methods (Boveroux et al., 2010; Schrouff et al., 2011; Boly et al., 2012; Jordan et al., 2013). Of note, the recent study of Jordan et al used combined electroencephalography and functional magnetic resonance imaging with no a priori assumptions regarding connectivity and found that the selective loss of frontal-to-parietal connectivity (as measured by symbolic transfer entropy) was the best discriminator between consciousness and propofol-induced unconsciousness (Jordan et al., 2013). "
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    • "Functional connectivity changes in both thalamocortical (Alkire et al., 2000; Liu et al., 2013c; White and Alkire, 2003) and corticocortical networks (Alkire and Miller, 2005; Boly et al., 2012; Boveroux et al., 2010; Ferrarelli et al., 2010; Hudetz, 2012; Schrouff et al., 2011; Soddu et al., 2012) have been detected. A reduction in the coherence and information transfer among select frontal, parietal, and occipital cortical regions has been found using electrophysiological techniques (Ku et al., 2011; Lee et al., 2009b, 2013). More generally, anesthetics have been thought to target subcortical mechanisms (Brown et al., 2010; Guldenmund et al., 2013; Mhuircheartaigh et al., 2010) including the natural sleep promoting circuits (Franks and Zecharia, 2011; Zecharia and Franks, 2009), and the neocortex itself (Hentschke et al., 2005; Hudetz, 2006; Seth et al., 2005; Velly et al., 2007). "
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    • "The utility of our model lies first and foremost in its simplicity—in both practical application and interpretation. While electroencephalographic studies may require application of complex statistical methods to resolve the underlying dynamics (Ku et al., 2011), the cortical slice strips away much of this complexity to give a more intuitive visualisation of the results. The source localisation procedure described in this study was potentially confounded by three matters. "
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