Abstract
Loss of consciousness in anesthetized healthy participants and in patients with unresponsive wakefulness syndrome (UWS) is associated with substantial alterations of functional connectivity across large-scale brain networks. Yet, a prominent distinction between the two cases is that after anesthesia, brain connectivity and consciousness are spontaneously restored, whereas in patients with UWS this restoration fails to occur, but why? A possible explanation is that the self-organizing capability of the brain is compromised in patients with UWS but not in healthy participants undergoing anesthesia. According to the theory of self-organized criticality, many natural complex systems, including the brain, evolve spontaneously to a critical state wherein system behaviors display spatial and/or temporal scale-invariant characteristics. Here we tested the hypothesis that the scale-free property of brain network organization is in fact fundamentally different between anesthetized healthy participants and UWS patients. We introduced a novel, computationally efficient approach to determine anatomical-functional parcellation of the whole-brain network at increasingly finer spatial scales. We found that in healthy participants, scale-free distributions of node size and node degree were present across wakefulness, propofol sedation, and recovery, despite significant propofol-induced functional connectivity changes. In patients with UWS, the scale-free distribution of node degree was absent, reflecting a fundamental difference between the two groups in adaptive reconfiguration of functional interaction between network components. The maintenance of scale-invariance across propofol sedation in healthy participants suggests the presence of persistent, on-going self-organizing processes to a critical state – a capacity that is compromised in patients with UWS.
Highlights
An essential feature of the healthy brain is that anestheticinduced loss of consciousness in general anesthesia is spontaneously and completely reversible after the withdrawal of the anesthetic
Given the similarity of functional alterations in various unconscious conditions, a critical question is whether there is a further aspect of network organization that allows the healthy brain to recover consciousness, for example, after general anesthesia, but whose absence impedes the recovery in severe neuropathological conditions, such as unresponsive wakefulness syndrome (UWS)
The power of the brain to self-organize may be relevant to the subject of consciousness [39], with respect to the question of why consciousness spontaneously recovers in the healthy brain after general anesthesia or deep sleep, but does not in brains under severe neuropathological conditions
Summary
An essential feature of the healthy brain is that anestheticinduced loss of consciousness in general anesthesia is spontaneously and completely reversible after the withdrawal of the anesthetic. Spontaneous restoration of consciousness is, absent in patients with UWS ( known as persistent vegetative state). During the past two decades, numerous neuroimaging studies have been conducted to determine neural correlates of unconsciousness in general anesthesia, coma, vegetative state, sleep, and seizure, focusing on the integrity and reversibility of large-scale functional networks of the brain [1,2,3,4,5,6]. One possible explanation is that for the healthy brain, the spontaneous restoration of consciousness after anesthesia is a consequence of the self-organizing ability of neural networks, which allows organization towards wakeful baseline consciousness to occur without any predefined plans or external manipulation of system parameters.
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