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Research Article

Hubs of brain functional networks are radically reorganized in comatose patients

Sophie Achard, Chantal Delon-Martin, Petra E. Vértes, Félix Renard, Maleka Schenck, Francis Schneider, Christian Heinrich, Stéphane Kremer, and Edward T. Bullmore
  1. aCentre National de la Recherche Scientifique, Grenoble Image Parole Signal Automatique, 38402 Grenoble, France;
  2. bInstitut National de la Santé et de la Recherche Médicale, U836, BP 170, F-38042 Grenoble Cedex 9, France;
  3. cUniversité Joseph Fourier, Grenoble Institut des Neurosciences, BP 170, F-38042 Grenoble Cedex 9, France;
  4. dBehavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge CB2 0SZ, United Kingdom;
  5. eService de Réanimation Médicale, Hôpital de Hautepierre, Centre Hospitalier Universitaire de Strasbourg, Université de Strasbourg, 67098 Strasbourg, France;
  6. fLaboratoire des Sciences et de l'Image, de l'Informatique et de la Télédétection, Université de Strasbourg, 67412 Illkirch, France;
  7. gService de Radiologie 2, Hôpital de Hautepierre, Centre Hospitalier Universitaire de Strasbourg, Université de Strasbourg, 67098 Strasbourg, France;
  8. hCambridgeshire and Peterborough National Health Service Foundation Trust, Cambridge CB21 5EF, United Kingdom; and
  9. iClinical Unit Cambridge, GlaxoSmithKline, Cambridge CB2 0QQ, United Kingdom

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PNAS first published November 26, 2012; https://doi.org/10.1073/pnas.1208933109
Sophie Achard
aCentre National de la Recherche Scientifique, Grenoble Image Parole Signal Automatique, 38402 Grenoble, France;
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  • For correspondence: sophie.achard@gipsa-lab.grenoble-inp.fr
Chantal Delon-Martin
bInstitut National de la Santé et de la Recherche Médicale, U836, BP 170, F-38042 Grenoble Cedex 9, France;
cUniversité Joseph Fourier, Grenoble Institut des Neurosciences, BP 170, F-38042 Grenoble Cedex 9, France;
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Petra E. Vértes
dBehavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge CB2 0SZ, United Kingdom;
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Félix Renard
aCentre National de la Recherche Scientifique, Grenoble Image Parole Signal Automatique, 38402 Grenoble, France;
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Maleka Schenck
eService de Réanimation Médicale, Hôpital de Hautepierre, Centre Hospitalier Universitaire de Strasbourg, Université de Strasbourg, 67098 Strasbourg, France;
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Francis Schneider
eService de Réanimation Médicale, Hôpital de Hautepierre, Centre Hospitalier Universitaire de Strasbourg, Université de Strasbourg, 67098 Strasbourg, France;
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Christian Heinrich
fLaboratoire des Sciences et de l'Image, de l'Informatique et de la Télédétection, Université de Strasbourg, 67412 Illkirch, France;
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Stéphane Kremer
gService de Radiologie 2, Hôpital de Hautepierre, Centre Hospitalier Universitaire de Strasbourg, Université de Strasbourg, 67098 Strasbourg, France;
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Edward T. Bullmore
dBehavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge CB2 0SZ, United Kingdom;
hCambridgeshire and Peterborough National Health Service Foundation Trust, Cambridge CB21 5EF, United Kingdom; and
iClinical Unit Cambridge, GlaxoSmithKline, Cambridge CB2 0QQ, United Kingdom
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  1. Edited by Marcus E. Raichle, Washington University in St. Louis, St. Louis, MO, and approved October 19, 2012 (received for review June 9, 2012)

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Abstract

Human brain networks have topological properties in common with many other complex systems, prompting the following question: what aspects of brain network organization are critical for distinctive functional properties of the brain, such as consciousness? To address this question, we used graph theoretical methods to explore brain network topology in resting state functional MRI data acquired from 17 patients with severely impaired consciousness and 20 healthy volunteers. We found that many global network properties were conserved in comatose patients. Specifically, there was no significant abnormality of global efficiency, clustering, small-worldness, modularity, or degree distribution in the patient group. However, in every patient, we found evidence for a radical reorganization of high degree or highly efficient “hub” nodes. Cortical regions that were hubs of healthy brain networks had typically become nonhubs of comatose brain networks and vice versa. These results indicate that global topological properties of complex brain networks may be homeostatically conserved under extremely different clinical conditions and that consciousness likely depends on the anatomical location of hub nodes in human brain networks.

  • connectome
  • consciousness disorders
  • neuroimaging
  • wavelet
  • brain injury

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: sophie.achard{at}gipsa-lab.grenoble-inp.fr.
  • Author contributions: S.A., C.D.-M., M.S., F.S., S.K., and E.T.B. designed research; S.A., M.S., S.K., and E.T.B. performed research; S.A., P.E.V., F.R., C.H., and E.T.B. contributed new reagents/analytic tools; S.A., C.D.-M., P.E.V., and E.T.B. analyzed data; M.S. in charge of patients and data acquisition; F.S. in charge of patients; S.K. performed data acquisition; and S.A., C.D.-M., P.E.V., F.S., S.K., and E.T.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1208933109/-/DCSupplemental.

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Reorganization of brain network hubs in coma
Sophie Achard, Chantal Delon-Martin, Petra E. Vértes, Félix Renard, Maleka Schenck, Francis Schneider, Christian Heinrich, Stéphane Kremer, Edward T. Bullmore
Proceedings of the National Academy of Sciences Nov 2012, 201208933; DOI: 10.1073/pnas.1208933109

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Reorganization of brain network hubs in coma
Sophie Achard, Chantal Delon-Martin, Petra E. Vértes, Félix Renard, Maleka Schenck, Francis Schneider, Christian Heinrich, Stéphane Kremer, Edward T. Bullmore
Proceedings of the National Academy of Sciences Nov 2012, 201208933; DOI: 10.1073/pnas.1208933109
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