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May 15, 2018; 90 (20) Article

Cortical and subcortical gray matter bases of cognitive deficits in REM sleep behavior disorder

Shady Rahayel, Ronald B. Postuma, Jacques Montplaisir, Daphné Génier Marchand, Frédérique Escudier, Malo Gaubert, Pierre-Alexandre Bourgouin, Julie Carrier, Oury Monchi, Sven Joubert, Frédéric Blanc, Jean-François Gagnon
First published April 18, 2018, DOI: https://doi.org/10.1212/WNL.0000000000005523
Shady Rahayel
From the Centre for Advanced Research in Sleep Medicine (S.R., R.B.P., J.M., D.G.M., M.G., P.-A.B., J.C., J.-F.G.), Hôpital du Sacré-Cœur de Montréal; Department of Psychology (S.R., D.G.M., M.G., P.-A.B., J.-F.G.), Université du Québec à Montréal; Department of Neurology (R.B.P.), Montreal General Hospital; Departments of Psychiatry (J.M.), Psychology (F.E., J.C., S.J.), and Radiology, Radio-Oncology, and Nuclear Medicine (O.M.), Université de Montréal; Research Centre (F.E., J.C., O.M., S.J., J.-F.G.), Institut universitaire de gériatrie de Montréal; Departments of Clinical Neurosciences and Radiology (O.M.), and Hotchkiss Brain Institute, University of Calgary, Canada; Université de Strasbourg and CNRS (F.B.), ICube UMR 7357 and FMTS (Fédération de Médecine Translationnelle de Strasbourg), Team IMIS, Strasbourg; and Saint François Day Hospital, Department of Geriatrics (F.B.), and Memory Resources and Research Centre (CM2R), Departments of Geriatrics and Neurology (F.B.), Hôpitaux Universitaires de Strasbourg, France.
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Ronald B. Postuma
From the Centre for Advanced Research in Sleep Medicine (S.R., R.B.P., J.M., D.G.M., M.G., P.-A.B., J.C., J.-F.G.), Hôpital du Sacré-Cœur de Montréal; Department of Psychology (S.R., D.G.M., M.G., P.-A.B., J.-F.G.), Université du Québec à Montréal; Department of Neurology (R.B.P.), Montreal General Hospital; Departments of Psychiatry (J.M.), Psychology (F.E., J.C., S.J.), and Radiology, Radio-Oncology, and Nuclear Medicine (O.M.), Université de Montréal; Research Centre (F.E., J.C., O.M., S.J., J.-F.G.), Institut universitaire de gériatrie de Montréal; Departments of Clinical Neurosciences and Radiology (O.M.), and Hotchkiss Brain Institute, University of Calgary, Canada; Université de Strasbourg and CNRS (F.B.), ICube UMR 7357 and FMTS (Fédération de Médecine Translationnelle de Strasbourg), Team IMIS, Strasbourg; and Saint François Day Hospital, Department of Geriatrics (F.B.), and Memory Resources and Research Centre (CM2R), Departments of Geriatrics and Neurology (F.B.), Hôpitaux Universitaires de Strasbourg, France.
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Jacques Montplaisir
From the Centre for Advanced Research in Sleep Medicine (S.R., R.B.P., J.M., D.G.M., M.G., P.-A.B., J.C., J.-F.G.), Hôpital du Sacré-Cœur de Montréal; Department of Psychology (S.R., D.G.M., M.G., P.-A.B., J.-F.G.), Université du Québec à Montréal; Department of Neurology (R.B.P.), Montreal General Hospital; Departments of Psychiatry (J.M.), Psychology (F.E., J.C., S.J.), and Radiology, Radio-Oncology, and Nuclear Medicine (O.M.), Université de Montréal; Research Centre (F.E., J.C., O.M., S.J., J.-F.G.), Institut universitaire de gériatrie de Montréal; Departments of Clinical Neurosciences and Radiology (O.M.), and Hotchkiss Brain Institute, University of Calgary, Canada; Université de Strasbourg and CNRS (F.B.), ICube UMR 7357 and FMTS (Fédération de Médecine Translationnelle de Strasbourg), Team IMIS, Strasbourg; and Saint François Day Hospital, Department of Geriatrics (F.B.), and Memory Resources and Research Centre (CM2R), Departments of Geriatrics and Neurology (F.B.), Hôpitaux Universitaires de Strasbourg, France.
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Daphné Génier Marchand
From the Centre for Advanced Research in Sleep Medicine (S.R., R.B.P., J.M., D.G.M., M.G., P.-A.B., J.C., J.-F.G.), Hôpital du Sacré-Cœur de Montréal; Department of Psychology (S.R., D.G.M., M.G., P.-A.B., J.-F.G.), Université du Québec à Montréal; Department of Neurology (R.B.P.), Montreal General Hospital; Departments of Psychiatry (J.M.), Psychology (F.E., J.C., S.J.), and Radiology, Radio-Oncology, and Nuclear Medicine (O.M.), Université de Montréal; Research Centre (F.E., J.C., O.M., S.J., J.-F.G.), Institut universitaire de gériatrie de Montréal; Departments of Clinical Neurosciences and Radiology (O.M.), and Hotchkiss Brain Institute, University of Calgary, Canada; Université de Strasbourg and CNRS (F.B.), ICube UMR 7357 and FMTS (Fédération de Médecine Translationnelle de Strasbourg), Team IMIS, Strasbourg; and Saint François Day Hospital, Department of Geriatrics (F.B.), and Memory Resources and Research Centre (CM2R), Departments of Geriatrics and Neurology (F.B.), Hôpitaux Universitaires de Strasbourg, France.
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Frédérique Escudier
From the Centre for Advanced Research in Sleep Medicine (S.R., R.B.P., J.M., D.G.M., M.G., P.-A.B., J.C., J.-F.G.), Hôpital du Sacré-Cœur de Montréal; Department of Psychology (S.R., D.G.M., M.G., P.-A.B., J.-F.G.), Université du Québec à Montréal; Department of Neurology (R.B.P.), Montreal General Hospital; Departments of Psychiatry (J.M.), Psychology (F.E., J.C., S.J.), and Radiology, Radio-Oncology, and Nuclear Medicine (O.M.), Université de Montréal; Research Centre (F.E., J.C., O.M., S.J., J.-F.G.), Institut universitaire de gériatrie de Montréal; Departments of Clinical Neurosciences and Radiology (O.M.), and Hotchkiss Brain Institute, University of Calgary, Canada; Université de Strasbourg and CNRS (F.B.), ICube UMR 7357 and FMTS (Fédération de Médecine Translationnelle de Strasbourg), Team IMIS, Strasbourg; and Saint François Day Hospital, Department of Geriatrics (F.B.), and Memory Resources and Research Centre (CM2R), Departments of Geriatrics and Neurology (F.B.), Hôpitaux Universitaires de Strasbourg, France.
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Malo Gaubert
From the Centre for Advanced Research in Sleep Medicine (S.R., R.B.P., J.M., D.G.M., M.G., P.-A.B., J.C., J.-F.G.), Hôpital du Sacré-Cœur de Montréal; Department of Psychology (S.R., D.G.M., M.G., P.-A.B., J.-F.G.), Université du Québec à Montréal; Department of Neurology (R.B.P.), Montreal General Hospital; Departments of Psychiatry (J.M.), Psychology (F.E., J.C., S.J.), and Radiology, Radio-Oncology, and Nuclear Medicine (O.M.), Université de Montréal; Research Centre (F.E., J.C., O.M., S.J., J.-F.G.), Institut universitaire de gériatrie de Montréal; Departments of Clinical Neurosciences and Radiology (O.M.), and Hotchkiss Brain Institute, University of Calgary, Canada; Université de Strasbourg and CNRS (F.B.), ICube UMR 7357 and FMTS (Fédération de Médecine Translationnelle de Strasbourg), Team IMIS, Strasbourg; and Saint François Day Hospital, Department of Geriatrics (F.B.), and Memory Resources and Research Centre (CM2R), Departments of Geriatrics and Neurology (F.B.), Hôpitaux Universitaires de Strasbourg, France.
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Pierre-Alexandre Bourgouin
From the Centre for Advanced Research in Sleep Medicine (S.R., R.B.P., J.M., D.G.M., M.G., P.-A.B., J.C., J.-F.G.), Hôpital du Sacré-Cœur de Montréal; Department of Psychology (S.R., D.G.M., M.G., P.-A.B., J.-F.G.), Université du Québec à Montréal; Department of Neurology (R.B.P.), Montreal General Hospital; Departments of Psychiatry (J.M.), Psychology (F.E., J.C., S.J.), and Radiology, Radio-Oncology, and Nuclear Medicine (O.M.), Université de Montréal; Research Centre (F.E., J.C., O.M., S.J., J.-F.G.), Institut universitaire de gériatrie de Montréal; Departments of Clinical Neurosciences and Radiology (O.M.), and Hotchkiss Brain Institute, University of Calgary, Canada; Université de Strasbourg and CNRS (F.B.), ICube UMR 7357 and FMTS (Fédération de Médecine Translationnelle de Strasbourg), Team IMIS, Strasbourg; and Saint François Day Hospital, Department of Geriatrics (F.B.), and Memory Resources and Research Centre (CM2R), Departments of Geriatrics and Neurology (F.B.), Hôpitaux Universitaires de Strasbourg, France.
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Julie Carrier
From the Centre for Advanced Research in Sleep Medicine (S.R., R.B.P., J.M., D.G.M., M.G., P.-A.B., J.C., J.-F.G.), Hôpital du Sacré-Cœur de Montréal; Department of Psychology (S.R., D.G.M., M.G., P.-A.B., J.-F.G.), Université du Québec à Montréal; Department of Neurology (R.B.P.), Montreal General Hospital; Departments of Psychiatry (J.M.), Psychology (F.E., J.C., S.J.), and Radiology, Radio-Oncology, and Nuclear Medicine (O.M.), Université de Montréal; Research Centre (F.E., J.C., O.M., S.J., J.-F.G.), Institut universitaire de gériatrie de Montréal; Departments of Clinical Neurosciences and Radiology (O.M.), and Hotchkiss Brain Institute, University of Calgary, Canada; Université de Strasbourg and CNRS (F.B.), ICube UMR 7357 and FMTS (Fédération de Médecine Translationnelle de Strasbourg), Team IMIS, Strasbourg; and Saint François Day Hospital, Department of Geriatrics (F.B.), and Memory Resources and Research Centre (CM2R), Departments of Geriatrics and Neurology (F.B.), Hôpitaux Universitaires de Strasbourg, France.
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Oury Monchi
From the Centre for Advanced Research in Sleep Medicine (S.R., R.B.P., J.M., D.G.M., M.G., P.-A.B., J.C., J.-F.G.), Hôpital du Sacré-Cœur de Montréal; Department of Psychology (S.R., D.G.M., M.G., P.-A.B., J.-F.G.), Université du Québec à Montréal; Department of Neurology (R.B.P.), Montreal General Hospital; Departments of Psychiatry (J.M.), Psychology (F.E., J.C., S.J.), and Radiology, Radio-Oncology, and Nuclear Medicine (O.M.), Université de Montréal; Research Centre (F.E., J.C., O.M., S.J., J.-F.G.), Institut universitaire de gériatrie de Montréal; Departments of Clinical Neurosciences and Radiology (O.M.), and Hotchkiss Brain Institute, University of Calgary, Canada; Université de Strasbourg and CNRS (F.B.), ICube UMR 7357 and FMTS (Fédération de Médecine Translationnelle de Strasbourg), Team IMIS, Strasbourg; and Saint François Day Hospital, Department of Geriatrics (F.B.), and Memory Resources and Research Centre (CM2R), Departments of Geriatrics and Neurology (F.B.), Hôpitaux Universitaires de Strasbourg, France.
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Sven Joubert
From the Centre for Advanced Research in Sleep Medicine (S.R., R.B.P., J.M., D.G.M., M.G., P.-A.B., J.C., J.-F.G.), Hôpital du Sacré-Cœur de Montréal; Department of Psychology (S.R., D.G.M., M.G., P.-A.B., J.-F.G.), Université du Québec à Montréal; Department of Neurology (R.B.P.), Montreal General Hospital; Departments of Psychiatry (J.M.), Psychology (F.E., J.C., S.J.), and Radiology, Radio-Oncology, and Nuclear Medicine (O.M.), Université de Montréal; Research Centre (F.E., J.C., O.M., S.J., J.-F.G.), Institut universitaire de gériatrie de Montréal; Departments of Clinical Neurosciences and Radiology (O.M.), and Hotchkiss Brain Institute, University of Calgary, Canada; Université de Strasbourg and CNRS (F.B.), ICube UMR 7357 and FMTS (Fédération de Médecine Translationnelle de Strasbourg), Team IMIS, Strasbourg; and Saint François Day Hospital, Department of Geriatrics (F.B.), and Memory Resources and Research Centre (CM2R), Departments of Geriatrics and Neurology (F.B.), Hôpitaux Universitaires de Strasbourg, France.
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Frédéric Blanc
From the Centre for Advanced Research in Sleep Medicine (S.R., R.B.P., J.M., D.G.M., M.G., P.-A.B., J.C., J.-F.G.), Hôpital du Sacré-Cœur de Montréal; Department of Psychology (S.R., D.G.M., M.G., P.-A.B., J.-F.G.), Université du Québec à Montréal; Department of Neurology (R.B.P.), Montreal General Hospital; Departments of Psychiatry (J.M.), Psychology (F.E., J.C., S.J.), and Radiology, Radio-Oncology, and Nuclear Medicine (O.M.), Université de Montréal; Research Centre (F.E., J.C., O.M., S.J., J.-F.G.), Institut universitaire de gériatrie de Montréal; Departments of Clinical Neurosciences and Radiology (O.M.), and Hotchkiss Brain Institute, University of Calgary, Canada; Université de Strasbourg and CNRS (F.B.), ICube UMR 7357 and FMTS (Fédération de Médecine Translationnelle de Strasbourg), Team IMIS, Strasbourg; and Saint François Day Hospital, Department of Geriatrics (F.B.), and Memory Resources and Research Centre (CM2R), Departments of Geriatrics and Neurology (F.B.), Hôpitaux Universitaires de Strasbourg, France.
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Jean-François Gagnon
From the Centre for Advanced Research in Sleep Medicine (S.R., R.B.P., J.M., D.G.M., M.G., P.-A.B., J.C., J.-F.G.), Hôpital du Sacré-Cœur de Montréal; Department of Psychology (S.R., D.G.M., M.G., P.-A.B., J.-F.G.), Université du Québec à Montréal; Department of Neurology (R.B.P.), Montreal General Hospital; Departments of Psychiatry (J.M.), Psychology (F.E., J.C., S.J.), and Radiology, Radio-Oncology, and Nuclear Medicine (O.M.), Université de Montréal; Research Centre (F.E., J.C., O.M., S.J., J.-F.G.), Institut universitaire de gériatrie de Montréal; Departments of Clinical Neurosciences and Radiology (O.M.), and Hotchkiss Brain Institute, University of Calgary, Canada; Université de Strasbourg and CNRS (F.B.), ICube UMR 7357 and FMTS (Fédération de Médecine Translationnelle de Strasbourg), Team IMIS, Strasbourg; and Saint François Day Hospital, Department of Geriatrics (F.B.), and Memory Resources and Research Centre (CM2R), Departments of Geriatrics and Neurology (F.B.), Hôpitaux Universitaires de Strasbourg, France.
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Citation
Cortical and subcortical gray matter bases of cognitive deficits in REM sleep behavior disorder
Shady Rahayel, Ronald B. Postuma, Jacques Montplaisir, Daphné Génier Marchand, Frédérique Escudier, Malo Gaubert, Pierre-Alexandre Bourgouin, Julie Carrier, Oury Monchi, Sven Joubert, Frédéric Blanc, Jean-François Gagnon
Neurology May 2018, 90 (20) e1759-e1770; DOI: 10.1212/WNL.0000000000005523

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Abstract

Objective To investigate cortical and subcortical gray matter abnormalities underlying cognitive impairment in patients with REM sleep behavior disorder (RBD) with or without mild cognitive impairment (MCI).

Methods Fifty-two patients with RBD, including 17 patients with MCI, were recruited and compared to 41 controls. All participants underwent extensive clinical assessments, neuropsychological examination, and 3-tesla MRI acquisition of T1 anatomical images. Vertex-based cortical analyses of volume, thickness, and surface area were performed to investigate cortical abnormalities between groups, whereas vertex-based shape analysis was performed to investigate subcortical structure surfaces. Correlations were performed to investigate associations between cortical and subcortical metrics, cognitive domains, and other markers of neurodegeneration (color discrimination, olfaction, and autonomic measures).

Results Patients with MCI had cortical thinning in the frontal, cingulate, temporal, and occipital cortices, and abnormal surface contraction in the lenticular nucleus and thalamus. Patients without MCI had cortical thinning restricted to the frontal cortex. Lower patient performance in cognitive domains was associated with cortical and subcortical abnormalities. Moreover, impaired performance on olfaction, color discrimination, and autonomic measures was associated with thinning in the occipital lobe.

Conclusions Cortical and subcortical gray matter abnormalities are associated with cognitive status in patients with RBD, with more extensive patterns in patients with MCI. Our results highlight the importance of distinguishing between subgroups of patients with RBD according to cognitive status in order to better understand the neurodegenerative process in this population.

Glossary

AUC=
area under the curve;
DLB=
dementia with Lewy bodies;
FM-100=
Farnsworth-Munsell 100;
MCI=
mild cognitive impairment;
MNI=
Montreal Neurological Institute;
PD=
Parkinson disease;
RBD=
REM sleep behavior disorder;
ROC=
receiver operating characteristic;
UPSIT=
University of Pennsylvania Smell Identification Test

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.

  • Editorial, page 909

  • Received September 13, 2017.
  • Accepted in final form February 20, 2018.
  • © 2018 American Academy of Neurology
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