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September 24, 2019; 93 (13) Article

Disruption of the ascending arousal network in acute traumatic disorders of consciousness

Samuel B. Snider, Yelena G. Bodien, Marta Bianciardi, Emery N. Brown, Ona Wu, Brian L. Edlow
First published September 4, 2019, DOI: https://doi.org/10.1212/WNL.0000000000008163
Samuel B. Snider
From the Center for Neurotechnology and Neurorecovery (S.B.S., Y.G.B., B.L.E.), Department of Neurology, and Department of Anesthesiology (E.N.B.), Massachusetts General Hospital, Boston; Department of Physical Medicine and Rehabilitation (Y.G.B.), Spaulding Rehabilitation Hospital, Charlestown, MA; Department of Radiology (M.B., O.W., B.L.E.), Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown; Department of Brain and Cognitive Sciences (E.N.B.), Massachusetts Institute of Technology; and Harvard-MIT Division of Health Science and Technology (E.N.B.), Cambridge, MA.
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Yelena G. Bodien
From the Center for Neurotechnology and Neurorecovery (S.B.S., Y.G.B., B.L.E.), Department of Neurology, and Department of Anesthesiology (E.N.B.), Massachusetts General Hospital, Boston; Department of Physical Medicine and Rehabilitation (Y.G.B.), Spaulding Rehabilitation Hospital, Charlestown, MA; Department of Radiology (M.B., O.W., B.L.E.), Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown; Department of Brain and Cognitive Sciences (E.N.B.), Massachusetts Institute of Technology; and Harvard-MIT Division of Health Science and Technology (E.N.B.), Cambridge, MA.
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Marta Bianciardi
From the Center for Neurotechnology and Neurorecovery (S.B.S., Y.G.B., B.L.E.), Department of Neurology, and Department of Anesthesiology (E.N.B.), Massachusetts General Hospital, Boston; Department of Physical Medicine and Rehabilitation (Y.G.B.), Spaulding Rehabilitation Hospital, Charlestown, MA; Department of Radiology (M.B., O.W., B.L.E.), Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown; Department of Brain and Cognitive Sciences (E.N.B.), Massachusetts Institute of Technology; and Harvard-MIT Division of Health Science and Technology (E.N.B.), Cambridge, MA.
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Emery N. Brown
From the Center for Neurotechnology and Neurorecovery (S.B.S., Y.G.B., B.L.E.), Department of Neurology, and Department of Anesthesiology (E.N.B.), Massachusetts General Hospital, Boston; Department of Physical Medicine and Rehabilitation (Y.G.B.), Spaulding Rehabilitation Hospital, Charlestown, MA; Department of Radiology (M.B., O.W., B.L.E.), Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown; Department of Brain and Cognitive Sciences (E.N.B.), Massachusetts Institute of Technology; and Harvard-MIT Division of Health Science and Technology (E.N.B.), Cambridge, MA.
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Ona Wu
From the Center for Neurotechnology and Neurorecovery (S.B.S., Y.G.B., B.L.E.), Department of Neurology, and Department of Anesthesiology (E.N.B.), Massachusetts General Hospital, Boston; Department of Physical Medicine and Rehabilitation (Y.G.B.), Spaulding Rehabilitation Hospital, Charlestown, MA; Department of Radiology (M.B., O.W., B.L.E.), Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown; Department of Brain and Cognitive Sciences (E.N.B.), Massachusetts Institute of Technology; and Harvard-MIT Division of Health Science and Technology (E.N.B.), Cambridge, MA.
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Brian L. Edlow
From the Center for Neurotechnology and Neurorecovery (S.B.S., Y.G.B., B.L.E.), Department of Neurology, and Department of Anesthesiology (E.N.B.), Massachusetts General Hospital, Boston; Department of Physical Medicine and Rehabilitation (Y.G.B.), Spaulding Rehabilitation Hospital, Charlestown, MA; Department of Radiology (M.B., O.W., B.L.E.), Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown; Department of Brain and Cognitive Sciences (E.N.B.), Massachusetts Institute of Technology; and Harvard-MIT Division of Health Science and Technology (E.N.B.), Cambridge, MA.
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Disruption of the ascending arousal network in acute traumatic disorders of consciousness
Samuel B. Snider, Yelena G. Bodien, Marta Bianciardi, Emery N. Brown, Ona Wu, Brian L. Edlow
Neurology Sep 2019, 93 (13) e1281-e1287; DOI: 10.1212/WNL.0000000000008163

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Abstract

Objective To determine whether ascending arousal network (AAn) connectivity is reduced in patients presenting with traumatic coma.

Methods We performed high-angular-resolution diffusion imaging in 16 patients with acute severe traumatic brain injury who were comatose on admission and in 16 matched controls. We used probabilistic tractography to measure the connectivity probability (CP) of AAn axonal pathways linking the brainstem tegmentum to the hypothalamus, thalamus, and basal forebrain. To assess the spatial specificity of CP differences between patients and controls, we also measured CP within 4 subcortical pathways outside the AAn.

Results Compared to controls, patients showed a reduction in AAn pathways connecting the brainstem tegmentum to a region of interest encompassing the hypothalamus, thalamus, and basal forebrain. When each pathway was examined individually, brainstem-hypothalamus and brainstem-thalamus CPs, but not brainstem-forebrain CP, were significantly reduced in patients. Only 1 subcortical pathway outside the AAn showed reduced CP in patients.

Conclusions We provide initial evidence for the reduced integrity of axonal pathways linking the brainstem tegmentum to the hypothalamus and thalamus in patients presenting with traumatic coma. Our findings support current conceptual models of coma as being caused by subcortical AAn injury. AAn connectivity mapping provides an opportunity to advance the study of human coma and consciousness.

Glossary

AAn=
ascending arousal network;
CP=
connectivity probability;
HARDI=
high-angular-resolution diffusion imaging;
ICU=
intensive care unit;
IQR=
interquartile range;
MNI=
Montreal Neurological Institute;
ROI=
region of interest;
TBI=
traumatic brain injury

Footnotes

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

  • Received December 13, 2018.
  • Accepted in final form April 30, 2019.
  • © 2019 American Academy of Neurology
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Letters: Rapid online correspondence

  • Author response: Disruption of the ascending arousal network in acute traumatic disorders of consciousness
    • Brian L. Edlow, Neurocritical Care Physician, Massachusetts General Hospital
    • Samuel B. Snider, Neurocritical Care Physician, Massachusetts General Hospital
    Submitted October 16, 2019
  • Reader response: Disruption of the ascending arousal network in acute traumatic disorders of consciousness
    • Calixto Machado, Senior Professor and Researcher of Neurology, Institute of Neurology and Neurosurgery (Havana, Cuba)
    Submitted September 30, 2019
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