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May 14, 2013; 80 (20) Article

Traumatic brain injury impairs small-world topology

Anand S. Pandit, Paul Expert, Renaud Lambiotte, Valerie Bonnelle, Robert Leech, Federico E. Turkheimer, David J. Sharp
First published April 17, 2013, DOI: https://doi.org/10.1212/WNL.0b013e3182929f38
Anand S. Pandit
From The Computational, Cognitive and Clinical Neuroimaging Laboratory (A.S.P., V.B., R.L., D.J.S.), The Division of Experimental Medicine, Imperial College London, Hammersmith Hospital Campus, London; Centre for Neuroimaging Sciences (P.E., F.E.T.), Institute of Psychiatry, London, UK; and Department of Mathematics/Naxys (R.L.), University of Namur, Namur, Belgium.
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Paul Expert
From The Computational, Cognitive and Clinical Neuroimaging Laboratory (A.S.P., V.B., R.L., D.J.S.), The Division of Experimental Medicine, Imperial College London, Hammersmith Hospital Campus, London; Centre for Neuroimaging Sciences (P.E., F.E.T.), Institute of Psychiatry, London, UK; and Department of Mathematics/Naxys (R.L.), University of Namur, Namur, Belgium.
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Renaud Lambiotte
From The Computational, Cognitive and Clinical Neuroimaging Laboratory (A.S.P., V.B., R.L., D.J.S.), The Division of Experimental Medicine, Imperial College London, Hammersmith Hospital Campus, London; Centre for Neuroimaging Sciences (P.E., F.E.T.), Institute of Psychiatry, London, UK; and Department of Mathematics/Naxys (R.L.), University of Namur, Namur, Belgium.
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Valerie Bonnelle
From The Computational, Cognitive and Clinical Neuroimaging Laboratory (A.S.P., V.B., R.L., D.J.S.), The Division of Experimental Medicine, Imperial College London, Hammersmith Hospital Campus, London; Centre for Neuroimaging Sciences (P.E., F.E.T.), Institute of Psychiatry, London, UK; and Department of Mathematics/Naxys (R.L.), University of Namur, Namur, Belgium.
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Robert Leech
From The Computational, Cognitive and Clinical Neuroimaging Laboratory (A.S.P., V.B., R.L., D.J.S.), The Division of Experimental Medicine, Imperial College London, Hammersmith Hospital Campus, London; Centre for Neuroimaging Sciences (P.E., F.E.T.), Institute of Psychiatry, London, UK; and Department of Mathematics/Naxys (R.L.), University of Namur, Namur, Belgium.
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Federico E. Turkheimer
From The Computational, Cognitive and Clinical Neuroimaging Laboratory (A.S.P., V.B., R.L., D.J.S.), The Division of Experimental Medicine, Imperial College London, Hammersmith Hospital Campus, London; Centre for Neuroimaging Sciences (P.E., F.E.T.), Institute of Psychiatry, London, UK; and Department of Mathematics/Naxys (R.L.), University of Namur, Namur, Belgium.
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David J. Sharp
From The Computational, Cognitive and Clinical Neuroimaging Laboratory (A.S.P., V.B., R.L., D.J.S.), The Division of Experimental Medicine, Imperial College London, Hammersmith Hospital Campus, London; Centre for Neuroimaging Sciences (P.E., F.E.T.), Institute of Psychiatry, London, UK; and Department of Mathematics/Naxys (R.L.), University of Namur, Namur, Belgium.
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Citation
Traumatic brain injury impairs small-world topology
Anand S. Pandit, Paul Expert, Renaud Lambiotte, Valerie Bonnelle, Robert Leech, Federico E. Turkheimer, David J. Sharp
Neurology May 2013, 80 (20) 1826-1833; DOI: 10.1212/WNL.0b013e3182929f38

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Abstract

Objective: We test the hypothesis that brain networks associated with cognitive function shift away from a “small-world” organization following traumatic brain injury (TBI).

Methods: We investigated 20 TBI patients and 21 age-matched controls. Resting-state functional MRI was used to study functional connectivity. Graph theoretical analysis was then applied to partial correlation matrices derived from these data. The presence of white matter damage was quantified using diffusion tensor imaging.

Results: Patients showed characteristic cognitive impairments as well as evidence of damage to white matter tracts. Compared to controls, the graph analysis showed reduced overall connectivity, longer average path lengths, and reduced network efficiency. A particular impact of TBI is seen on a major network hub, the posterior cingulate cortex. Taken together, these results confirm that a network critical to cognitive function shows a shift away from small-world characteristics.

Conclusions: We provide evidence that key brain networks involved in supporting cognitive function become less small-world in their organization after TBI. This is likely to be the result of diffuse white matter damage, and may be an important factor in producing cognitive impairment after TBI.

GLOSSARY

DMN=
default mode network;
DTI=
diffusion tensor imaging;
EN=
executive network;
FA=
fractional anisotropy;
fMRI=
functional MRI;
ICA=
independent component analysis;
MD=
mean diffusivity;
PCC=
posterior cingulate cortex;
TAI=
traumatic axonal injury;
TBI=
traumatic brain injury

Footnotes

  • Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Editorial, page 1822

  • Supplemental data at www.neurology.org

  • Received July 14, 2012.
  • Accepted in final form January 18, 2013.
  • © 2013 American Academy of Neurology
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