Elsevier

Consciousness and Cognition

Volume 18, Issue 4, December 2009, Pages 1069-1078
Consciousness and Cognition

The directionality and functional organization of frontoparietal connectivity during consciousness and anesthesia in humans

https://doi.org/10.1016/j.concog.2009.04.004Get rights and content

Abstract

Frontoparietal connectivity has been suggested to be important in conscious processing and its interruption is thought to be one mechanism of general anesthesia. Data in animals demonstrate that feedforward processing of information may persist during the anesthetized state, while feedback processing is inhibited. We investigated the directionality and functional organization of frontoparietal connectivity in 10 human subjects anesthetized with propofol on two separate occasions. Multichannel electroencephalography and a computational method of assessing directed functional connectivity were employed. We demonstrate that directed feedback connectivity is diminished with loss of consciousness and returns with responsiveness to verbal command. We also applied the Dendrogram classification method to assess the global organization of directed functional connectivity during consciousness and anesthesia. We demonstrate a state-specific hierarchy and subject-specific subhierarchy in functional organization. These data support the hypothesis that specific states of human consciousness are defined by specific states of frontoparietal connectivity.

Introduction

Cognitive binding is a fundamental requisite of unitary object perception and human consciousness (Singer, 1996). The capacity and structure of cognitive binding may also be associated with the degree and the quality of consciousness, respectively (Edelman, 1989, Tononi, 2004, Tononi and Sporns, 2003). Based on these theoretical assumptions, it has been suggested that a distinct network structure translates into a unique functional consequence that may directly correspond to a state of consciousness (Buzsaki, 2007).

The prefrontal and posterior parietal association cortices, as well as information integration across the frontoparietal network, have been suggested to play an important role in consciousness (Mesulam, 1998, Naghavi and Nyberg, 2005, Rees et al., 2002, Sarter et al., 2001). In the frontoparietal network, feedforward (FF) projections represent and analyze incoming sensory data, while feedback (FB) projections play a modulatory role in selection and contextual interpretation of information (Crick and Koch, 2003, Imas et al., 2005, Lamme and Roelfsema, 2000, Naghavi and Nyberg, 2005, Pascual-Leone and Walsh, 2001, Shao and Burkhalter, 1996).

Here we investigated the relationship between the frontoparietal connectivity of normal human subjects and states of consciousness. Three different states were examined: baseline consciousness, general anesthesia (defined as loss of responsiveness to verbal command) and recovery (defined as a return of responsiveness to verbal command). In order to analyze functional changes associated with these states, the functional connectivity of the brain was represented with a computational method that quantifies both directionality and coherence.

Section snippets

Subjects

After obtaining the approval of the institutional review board of Asan Medical Center (Seoul, Korea) and written informed consent, 10 male volunteers participated in this study. Each volunteer fasted for 8 h before study drug administration. Exclusion criteria were allergy to propofol (Diprivan®, AstraZeneca, London, UK), medical problems, abnormal laboratory findings with clinical significance, or body weight that was not within 30% of ideal. The average age was 23 ± 2 yr (range, 20–28 yr).

An

Feedback (FB) and feedforward (FF) functional connections across multiple states of consciousness

We investigated the FB and FF functional connections in the frontoparietal network and their relationships to states of consciousness (awake, anesthetized, and recovering). Fig. 1a represents the FB and FF functional connections with cij¯ and Fig. 1b presents the mean directionality index D¯ between the frontal and parietal areas. Since the subjects have an individual response time to anesthetic induction, the LOC and ROC points were chosen as the references for averaging over all subjects.

Discussion

Here we report that changes of FB and FF functional connections in the frontoparietal network are associated with changes in states of human consciousness. Furthermore, we demonstrate that consciousness and anesthesia have distinguishable patterns of global functional connectivity, with a further suborganization that varies according to subject. These data suggest that specific functional connections in the frontoparietal network correspond to specific states of consciousness. In experiments

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Disclosures: The authors have no conflicts of interest to declare.

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