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Functional neuroanatomy underlying the clinical subcategorization of minimally conscious state patients

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Abstract

Patients in a minimally conscious state (MCS) show restricted signs of awareness but are unable to communicate. We assessed cerebral glucose metabolism in MCS patients and tested the hypothesis that this entity can be subcategorized into MCS− (i.e., patients only showing nonreflex behavior such as visual pursuit, localization of noxious stimulation and/or contingent behavior) and MCS+ (i.e., patients showing command following).

Patterns of cerebral glucose metabolism were studied using [18F]-fluorodeoxyglucose-PET in 39 healthy volunteers (aged 46 ± 18 years) and 27 MCS patients of whom 13 were MCS− (aged 49 ± 19 years; 4 traumatic; 21 ± 23 months post injury) and 14 MCS+ (aged 43 ± 19 years; 5 traumatic; 19 ± 26 months post injury). Results were thresholded for significance at false discovery rate corrected p < 0.05.

We observed a metabolic impairment in a bilateral subcortical (thalamus and caudate) and cortical (fronto-temporo-parietal) network in nontraumatic and traumatic MCS patients. Compared to MCS−, patients in MCS+ showed higher cerebral metabolism in left-sided cortical areas encompassing the language network, premotor, presupplementary motor, and sensorimotor cortices. A functional connectivity study showed that Broca’s region was disconnected from the rest of the language network, mesiofrontal and cerebellar areas in MCS− as compared to MCS+ patients.

The proposed subcategorization of MCS based on the presence or absence of command following showed a different functional neuroanatomy. MCS− is characterized by preserved right hemispheric cortical metabolism interpreted as evidence of residual sensory consciousness. MCS+ patients showed preserved metabolism and functional connectivity in language networks arguably reflecting some additional higher order or extended consciousness albeit devoid of clinical verbal or nonverbal expression.

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Acknowledgments

The funding sources had no role in the study design, data collection, data analysis, data interpretation, or writing of this report. All authors had full access to all the data in the study and had final responsibility for the decision to submit for publication. This research was funded by the Belgian National Funds for Scientific Research (FNRS), the European Commission (Mindbridge, DISCOS, Marie-Curie Actions, DECODER & COST), the James McDonnell Foundation, the Mind Science Foundation, the French Speaking Community Concerted Research Action (ARC-06/11-340), the Fondation Médicale Reine Elisabeth, and the University of Liège. SL and MAB participated in the conception and design of this study. MAB, AV, CS, OG, PB, and MK acquired the data. SL, MAB, and MB analyzed and interpreted the data. MAB and SL drafted the manuscript. AV, CS, AD, OG, MS, GM, and RH revised the manuscript for intellectual content. SL and GM obtained funding. RH and GM provided administrative, technical, or material support, and SL supervised the study.

Conflict of interest

The authors declare that they have no competing interests.

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Authors and Affiliations

  1. Coma Science Group, Cyclotron Research Center, University of Liège, Sart-Tilman B30, 4000, Liège, Belgium

    Marie-Aurélie Bruno, Mélanie Boly, Audrey Vanhaudenhuyse, Caroline Schnakers, Olivia Gosseries, Pierre Boveroux, Murielle Kirsch, Athena Demertzi, Gustave Moonen & Steven Laureys

  2. Department of Neurology, University Hospital of Liège, Liège, Belgium

    Mélanie Boly, Gustave Moonen & Steven Laureys

  3. Research Center for Cognitive and Behavioral Neuroscience, University of Liège, Liège, Belgium

    Steve Majerus

  4. Department of Nuclear Medicine, University Hospital of Liège, Liège, Belgium

    Claire Bernard & Roland Hustinx

  5. Fund for Scientific Research FNRS, Brussels, Belgium

    Marie-Aurélie Bruno, Steve Majerus, Mélanie Boly, Audrey Vanhaudenhuyse, Caroline Schnakers, Olivia Gosseries & Steven Laureys

Authors
  1. Marie-Aurélie Bruno
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  2. Steve Majerus
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  3. Mélanie Boly
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  4. Audrey Vanhaudenhuyse
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  5. Caroline Schnakers
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  7. Pierre Boveroux
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  8. Murielle Kirsch
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  13. Steven Laureys
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Correspondence to Steven Laureys.

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Bruno, MA., Majerus, S., Boly, M. et al. Functional neuroanatomy underlying the clinical subcategorization of minimally conscious state patients. J Neurol 259, 1087–1098 (2012). https://doi.org/10.1007/s00415-011-6303-7

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  • DOI: https://doi.org/10.1007/s00415-011-6303-7

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