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: 3.23). 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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    • "It is assumed that a functional correlate of unconsciousness is, besides other neuronal correlates, a disintegration of neuronal networks, meaning a cessation of information exchange across distant cortical and subcortical areas as well as a reduction of information capacity (Dehaene et al., 2006; Alkire et al., 2008; Boveroux et al., 2010; King et al., 2013). In particular, the disintegration of long-range connections seems to result in an impaired ability to process information and, consequently, the lapse of consciousness (Boly et al., 2011; Jordan et al., 2013; Ku et al., 2011; Lee et al., 2013). Still, the leading processes to the emergence or the loss of consciousness are largely unknown and remain a major field of research in neuroscience. "
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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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    • "By contrast, the top-down approach to ketamine-induced unconsciousness has successfully identified a common neural correlate of unconsciousness induced by propofol, ketamine, and sevoflurane that could have been predicted based on the neurobiology of consciousness (Lee et al., 2013) (Figure 6). Loss of effective connectivity from the frontal cortex to more posterior cortices has been consistently observed with all three drugs, suggesting inhibition of reentrant processing as a candidate for the common mediator of anesthetic effects on consciousness (Ku et al., 2011; Jordan et al., 2013). Furthermore, this loss of top-down information processing was selective, because feedforward processing (from posterior parietal to frontal area) appeared preserved. "
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