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Scale-free functional connectivity of the brain is maintained in anesthetized healthy participants but not in patients with unresponsive wakefulness syndrome.

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.

SUBMITTER: Liu X

PROVIDER: S-EPMC3960221 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Scale-free functional connectivity of the brain is maintained in anesthetized healthy participants but not in patients with unresponsive wakefulness syndrome.

Liu Xiaolin X Ward B Douglas BD Binder Jeffrey R JR Li Shi-Jiang SJ Hudetz Anthony G AG

PloS one 20140319 3

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 ...[more]

PMID: 24647227

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Project description:IntroductionBehavioral and cerebral dissociation has been now clearly established in some patients with acquired disorders of consciousness (DoC). Altogether, these studies mainly focused on the preservation of high-level cognitive markers in prolonged DoC, but did not specifically investigate lower but key-cognitive functions to consciousness emergence, such as the ability to take a first-person perspective, notably at the acute stage of coma. We made the hypothesis that the preservation of self-recognition (i) is independent of the behavioral impairment of consciousness, and (ii) can reflect the ability to recover consciousness.MethodsHence, using bedside Electroencephalography (EEG) recordings, we acquired, in a large cohort of 129 severely brain damaged patients, the brain response to the passive listening of the subject's own name (SON) and unfamiliar other first names (OFN). One hundred and twelve of them (mean age ± SD = 46 ± 18.3 years, sex ratio M/F: 71/41) could be analyzed for the detection of an individual and significant discriminative P3 event-related brain response to the SON as compared to OFN ('SON effect', primary endpoint assessed by temporal clustering permutation tests).ResultsPatients were either coma (n = 38), unresponsive wakefulness syndrome (UWS, n = 30) or minimally conscious state (MCS, n = 44), according to the revised version of the Coma Recovery Scale (CRS-R). Overall, 33 DoC patients (29%) evoked a 'SON effect'. This electrophysiological index was similar between coma (29%), MCS (23%) and UWS (34%) patients (p = 0.61). MCS patients at the time of enrolment were more likely to emerged from MCS (EMCS) at 6 months than coma and UWS patients (p = 0.013 for comparison between groups). Among the 72 survivors' patients with event-related responses recorded within 3 months after brain injury, 75% of the 16 patients with a SON effect were EMCS at 6 months, while 59% of the 56 patients without a SON effect evolved to this favorable behavioral outcome.DiscussionAbout 30% of severely brain-damaged patients suffering from DoC are capable to process salient self-referential auditory stimuli, even in case of absence of behavioral detection of self-conscious processing. We suggest that self-recognition covert brain ability could be an index of consciousness recovery, and thus could help to predict good outcome.

Project description:The extent to which people ascribe mind to others has been shown to predict the extent to which human rights are conferred. Therefore, in the context of disorders of consciousness (DOC), mind ascription can influence end of life decisions. A previous US-American study indicated that participants ascribed even less mind to patients with unresponsive-wakefulness-syndrome (UWS) than to the dead. Results were explained in terms of implicit dualism and religious beliefs, as highly religious people ascribed least mind to UWS. Here, we addresses mind ascription to UWS patients in Germany.We investigate the perception of UWS patients in a large German sample (N?=?910) and compare the results to the previous US data, addressing possible cultural differences. We further assess effects of medical expertise, age, gender, socio-economic status and subjective knowledge about UWS in the German sample.Unlike the US sample, German participants did not perceive UWS patients as "more dead than dead", ascribing either equal (on 3 of 5 items) or more (on 2 items) mental abilities to UWS patients than to the dead. Likewise, an effect of implicit dualism was not replicated and German medically trained participants ascribed more capabilities to UWS patients than did a non-medical sample. Within the German sample, age, gender, religiosity and socio-economic status explained about 15% of the variability of mind ascription. Age and religiosity were individually significant predictors, younger and more religious people ascribing more mind. Gender had no effect.Results are consistent with cross-cultural differences in the perception of UWS between Germany and the USA, Germans ascribing more mind to UWS patients. The German sample ascribed as much or more but not less mind to a UWS patient than to a deceased, although within group variance was large, calling for further research. Mind ascription is vital, because, in times of declining resources for healthcare systems, and an increasing legalization of euthanasia, public opinion will influence UWS patients' rights and whether 'the right to die' will be the only right conceded to them.

Dataset Information

Scale-free functional connectivity of the brain is maintained in anesthetized healthy participants but not in patients with unresponsive wakefulness syndrome.

Publications

Scale-free functional connectivity of the brain is maintained in anesthetized healthy participants but not in patients with unresponsive wakefulness syndrome.

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