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February 28, 2017; 88 (9) Article

Antisaccades in Parkinson disease

A new marker of postural control?

Claire Ewenczyk, Salma Mesmoudi, Cécile Gallea, Marie-Laure Welter, Bertrand Gaymard, Adèle Demain, Lydia Yahia Cherif, Bertrand Degos, Habib Benali, Pierre Pouget, Cyril Poupon, Stéphane Lehericy, Sophie Rivaud-Péchoux, Marie Vidailhet
First published January 27, 2017, DOI: https://doi.org/10.1212/WNL.0000000000003658
Claire Ewenczyk
From APHP (C.E., M.-L.W., B.D., M.V.), Département de neurologie, Hôpital Pitié-Salpêtrière; Sorbonne Universités (C.E., C.G., M.-L.W., L.Y.C., B.D., P.P., S.L., S.R.-P., M.V.), UPMC Université Paris 06, Inserm U1127, CNRS UMR 7225, UM 75, ICM; APHP (C.E., A.D., M.V.), INSERM, ICM, Centre d’Investigation Clinique Pitié Neurosciences, CIC-1422, Département des Maladies du Système Nerveux, Hôpital Pitié-Salpêtrière; Equipex MATRICE (S.M.), Université Paris 1 Panthéon-Sorbonne; Centre de Neuroimagerie de Recherche (C.G., L.Y.C., S.L.), Institut du Cerveau et de la Moelle Epinière; Centre Inter-Régional de Coordination de la Maladie de Parkinson (M.-L.W., B.D., M.V.) and Département de Neurophysiologie clinique (B.G.), Hôpital Pitié-Salpêtrière; Inserm UMR-S 678 (H.B.), Laboratoire d'Imagerie Fonctionnelle, UPMC-Paris 6, Paris; and CEA (C.P.), NeuroSpin, Gif-Sur-Yvette, France.
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Salma Mesmoudi
From APHP (C.E., M.-L.W., B.D., M.V.), Département de neurologie, Hôpital Pitié-Salpêtrière; Sorbonne Universités (C.E., C.G., M.-L.W., L.Y.C., B.D., P.P., S.L., S.R.-P., M.V.), UPMC Université Paris 06, Inserm U1127, CNRS UMR 7225, UM 75, ICM; APHP (C.E., A.D., M.V.), INSERM, ICM, Centre d’Investigation Clinique Pitié Neurosciences, CIC-1422, Département des Maladies du Système Nerveux, Hôpital Pitié-Salpêtrière; Equipex MATRICE (S.M.), Université Paris 1 Panthéon-Sorbonne; Centre de Neuroimagerie de Recherche (C.G., L.Y.C., S.L.), Institut du Cerveau et de la Moelle Epinière; Centre Inter-Régional de Coordination de la Maladie de Parkinson (M.-L.W., B.D., M.V.) and Département de Neurophysiologie clinique (B.G.), Hôpital Pitié-Salpêtrière; Inserm UMR-S 678 (H.B.), Laboratoire d'Imagerie Fonctionnelle, UPMC-Paris 6, Paris; and CEA (C.P.), NeuroSpin, Gif-Sur-Yvette, France.
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Cécile Gallea
From APHP (C.E., M.-L.W., B.D., M.V.), Département de neurologie, Hôpital Pitié-Salpêtrière; Sorbonne Universités (C.E., C.G., M.-L.W., L.Y.C., B.D., P.P., S.L., S.R.-P., M.V.), UPMC Université Paris 06, Inserm U1127, CNRS UMR 7225, UM 75, ICM; APHP (C.E., A.D., M.V.), INSERM, ICM, Centre d’Investigation Clinique Pitié Neurosciences, CIC-1422, Département des Maladies du Système Nerveux, Hôpital Pitié-Salpêtrière; Equipex MATRICE (S.M.), Université Paris 1 Panthéon-Sorbonne; Centre de Neuroimagerie de Recherche (C.G., L.Y.C., S.L.), Institut du Cerveau et de la Moelle Epinière; Centre Inter-Régional de Coordination de la Maladie de Parkinson (M.-L.W., B.D., M.V.) and Département de Neurophysiologie clinique (B.G.), Hôpital Pitié-Salpêtrière; Inserm UMR-S 678 (H.B.), Laboratoire d'Imagerie Fonctionnelle, UPMC-Paris 6, Paris; and CEA (C.P.), NeuroSpin, Gif-Sur-Yvette, France.
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Marie-Laure Welter
From APHP (C.E., M.-L.W., B.D., M.V.), Département de neurologie, Hôpital Pitié-Salpêtrière; Sorbonne Universités (C.E., C.G., M.-L.W., L.Y.C., B.D., P.P., S.L., S.R.-P., M.V.), UPMC Université Paris 06, Inserm U1127, CNRS UMR 7225, UM 75, ICM; APHP (C.E., A.D., M.V.), INSERM, ICM, Centre d’Investigation Clinique Pitié Neurosciences, CIC-1422, Département des Maladies du Système Nerveux, Hôpital Pitié-Salpêtrière; Equipex MATRICE (S.M.), Université Paris 1 Panthéon-Sorbonne; Centre de Neuroimagerie de Recherche (C.G., L.Y.C., S.L.), Institut du Cerveau et de la Moelle Epinière; Centre Inter-Régional de Coordination de la Maladie de Parkinson (M.-L.W., B.D., M.V.) and Département de Neurophysiologie clinique (B.G.), Hôpital Pitié-Salpêtrière; Inserm UMR-S 678 (H.B.), Laboratoire d'Imagerie Fonctionnelle, UPMC-Paris 6, Paris; and CEA (C.P.), NeuroSpin, Gif-Sur-Yvette, France.
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Bertrand Gaymard
From APHP (C.E., M.-L.W., B.D., M.V.), Département de neurologie, Hôpital Pitié-Salpêtrière; Sorbonne Universités (C.E., C.G., M.-L.W., L.Y.C., B.D., P.P., S.L., S.R.-P., M.V.), UPMC Université Paris 06, Inserm U1127, CNRS UMR 7225, UM 75, ICM; APHP (C.E., A.D., M.V.), INSERM, ICM, Centre d’Investigation Clinique Pitié Neurosciences, CIC-1422, Département des Maladies du Système Nerveux, Hôpital Pitié-Salpêtrière; Equipex MATRICE (S.M.), Université Paris 1 Panthéon-Sorbonne; Centre de Neuroimagerie de Recherche (C.G., L.Y.C., S.L.), Institut du Cerveau et de la Moelle Epinière; Centre Inter-Régional de Coordination de la Maladie de Parkinson (M.-L.W., B.D., M.V.) and Département de Neurophysiologie clinique (B.G.), Hôpital Pitié-Salpêtrière; Inserm UMR-S 678 (H.B.), Laboratoire d'Imagerie Fonctionnelle, UPMC-Paris 6, Paris; and CEA (C.P.), NeuroSpin, Gif-Sur-Yvette, France.
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Adèle Demain
From APHP (C.E., M.-L.W., B.D., M.V.), Département de neurologie, Hôpital Pitié-Salpêtrière; Sorbonne Universités (C.E., C.G., M.-L.W., L.Y.C., B.D., P.P., S.L., S.R.-P., M.V.), UPMC Université Paris 06, Inserm U1127, CNRS UMR 7225, UM 75, ICM; APHP (C.E., A.D., M.V.), INSERM, ICM, Centre d’Investigation Clinique Pitié Neurosciences, CIC-1422, Département des Maladies du Système Nerveux, Hôpital Pitié-Salpêtrière; Equipex MATRICE (S.M.), Université Paris 1 Panthéon-Sorbonne; Centre de Neuroimagerie de Recherche (C.G., L.Y.C., S.L.), Institut du Cerveau et de la Moelle Epinière; Centre Inter-Régional de Coordination de la Maladie de Parkinson (M.-L.W., B.D., M.V.) and Département de Neurophysiologie clinique (B.G.), Hôpital Pitié-Salpêtrière; Inserm UMR-S 678 (H.B.), Laboratoire d'Imagerie Fonctionnelle, UPMC-Paris 6, Paris; and CEA (C.P.), NeuroSpin, Gif-Sur-Yvette, France.
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Lydia Yahia Cherif
From APHP (C.E., M.-L.W., B.D., M.V.), Département de neurologie, Hôpital Pitié-Salpêtrière; Sorbonne Universités (C.E., C.G., M.-L.W., L.Y.C., B.D., P.P., S.L., S.R.-P., M.V.), UPMC Université Paris 06, Inserm U1127, CNRS UMR 7225, UM 75, ICM; APHP (C.E., A.D., M.V.), INSERM, ICM, Centre d’Investigation Clinique Pitié Neurosciences, CIC-1422, Département des Maladies du Système Nerveux, Hôpital Pitié-Salpêtrière; Equipex MATRICE (S.M.), Université Paris 1 Panthéon-Sorbonne; Centre de Neuroimagerie de Recherche (C.G., L.Y.C., S.L.), Institut du Cerveau et de la Moelle Epinière; Centre Inter-Régional de Coordination de la Maladie de Parkinson (M.-L.W., B.D., M.V.) and Département de Neurophysiologie clinique (B.G.), Hôpital Pitié-Salpêtrière; Inserm UMR-S 678 (H.B.), Laboratoire d'Imagerie Fonctionnelle, UPMC-Paris 6, Paris; and CEA (C.P.), NeuroSpin, Gif-Sur-Yvette, France.
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Bertrand Degos
From APHP (C.E., M.-L.W., B.D., M.V.), Département de neurologie, Hôpital Pitié-Salpêtrière; Sorbonne Universités (C.E., C.G., M.-L.W., L.Y.C., B.D., P.P., S.L., S.R.-P., M.V.), UPMC Université Paris 06, Inserm U1127, CNRS UMR 7225, UM 75, ICM; APHP (C.E., A.D., M.V.), INSERM, ICM, Centre d’Investigation Clinique Pitié Neurosciences, CIC-1422, Département des Maladies du Système Nerveux, Hôpital Pitié-Salpêtrière; Equipex MATRICE (S.M.), Université Paris 1 Panthéon-Sorbonne; Centre de Neuroimagerie de Recherche (C.G., L.Y.C., S.L.), Institut du Cerveau et de la Moelle Epinière; Centre Inter-Régional de Coordination de la Maladie de Parkinson (M.-L.W., B.D., M.V.) and Département de Neurophysiologie clinique (B.G.), Hôpital Pitié-Salpêtrière; Inserm UMR-S 678 (H.B.), Laboratoire d'Imagerie Fonctionnelle, UPMC-Paris 6, Paris; and CEA (C.P.), NeuroSpin, Gif-Sur-Yvette, France.
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Habib Benali
From APHP (C.E., M.-L.W., B.D., M.V.), Département de neurologie, Hôpital Pitié-Salpêtrière; Sorbonne Universités (C.E., C.G., M.-L.W., L.Y.C., B.D., P.P., S.L., S.R.-P., M.V.), UPMC Université Paris 06, Inserm U1127, CNRS UMR 7225, UM 75, ICM; APHP (C.E., A.D., M.V.), INSERM, ICM, Centre d’Investigation Clinique Pitié Neurosciences, CIC-1422, Département des Maladies du Système Nerveux, Hôpital Pitié-Salpêtrière; Equipex MATRICE (S.M.), Université Paris 1 Panthéon-Sorbonne; Centre de Neuroimagerie de Recherche (C.G., L.Y.C., S.L.), Institut du Cerveau et de la Moelle Epinière; Centre Inter-Régional de Coordination de la Maladie de Parkinson (M.-L.W., B.D., M.V.) and Département de Neurophysiologie clinique (B.G.), Hôpital Pitié-Salpêtrière; Inserm UMR-S 678 (H.B.), Laboratoire d'Imagerie Fonctionnelle, UPMC-Paris 6, Paris; and CEA (C.P.), NeuroSpin, Gif-Sur-Yvette, France.
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Pierre Pouget
From APHP (C.E., M.-L.W., B.D., M.V.), Département de neurologie, Hôpital Pitié-Salpêtrière; Sorbonne Universités (C.E., C.G., M.-L.W., L.Y.C., B.D., P.P., S.L., S.R.-P., M.V.), UPMC Université Paris 06, Inserm U1127, CNRS UMR 7225, UM 75, ICM; APHP (C.E., A.D., M.V.), INSERM, ICM, Centre d’Investigation Clinique Pitié Neurosciences, CIC-1422, Département des Maladies du Système Nerveux, Hôpital Pitié-Salpêtrière; Equipex MATRICE (S.M.), Université Paris 1 Panthéon-Sorbonne; Centre de Neuroimagerie de Recherche (C.G., L.Y.C., S.L.), Institut du Cerveau et de la Moelle Epinière; Centre Inter-Régional de Coordination de la Maladie de Parkinson (M.-L.W., B.D., M.V.) and Département de Neurophysiologie clinique (B.G.), Hôpital Pitié-Salpêtrière; Inserm UMR-S 678 (H.B.), Laboratoire d'Imagerie Fonctionnelle, UPMC-Paris 6, Paris; and CEA (C.P.), NeuroSpin, Gif-Sur-Yvette, France.
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Cyril Poupon
From APHP (C.E., M.-L.W., B.D., M.V.), Département de neurologie, Hôpital Pitié-Salpêtrière; Sorbonne Universités (C.E., C.G., M.-L.W., L.Y.C., B.D., P.P., S.L., S.R.-P., M.V.), UPMC Université Paris 06, Inserm U1127, CNRS UMR 7225, UM 75, ICM; APHP (C.E., A.D., M.V.), INSERM, ICM, Centre d’Investigation Clinique Pitié Neurosciences, CIC-1422, Département des Maladies du Système Nerveux, Hôpital Pitié-Salpêtrière; Equipex MATRICE (S.M.), Université Paris 1 Panthéon-Sorbonne; Centre de Neuroimagerie de Recherche (C.G., L.Y.C., S.L.), Institut du Cerveau et de la Moelle Epinière; Centre Inter-Régional de Coordination de la Maladie de Parkinson (M.-L.W., B.D., M.V.) and Département de Neurophysiologie clinique (B.G.), Hôpital Pitié-Salpêtrière; Inserm UMR-S 678 (H.B.), Laboratoire d'Imagerie Fonctionnelle, UPMC-Paris 6, Paris; and CEA (C.P.), NeuroSpin, Gif-Sur-Yvette, France.
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Stéphane Lehericy
From APHP (C.E., M.-L.W., B.D., M.V.), Département de neurologie, Hôpital Pitié-Salpêtrière; Sorbonne Universités (C.E., C.G., M.-L.W., L.Y.C., B.D., P.P., S.L., S.R.-P., M.V.), UPMC Université Paris 06, Inserm U1127, CNRS UMR 7225, UM 75, ICM; APHP (C.E., A.D., M.V.), INSERM, ICM, Centre d’Investigation Clinique Pitié Neurosciences, CIC-1422, Département des Maladies du Système Nerveux, Hôpital Pitié-Salpêtrière; Equipex MATRICE (S.M.), Université Paris 1 Panthéon-Sorbonne; Centre de Neuroimagerie de Recherche (C.G., L.Y.C., S.L.), Institut du Cerveau et de la Moelle Epinière; Centre Inter-Régional de Coordination de la Maladie de Parkinson (M.-L.W., B.D., M.V.) and Département de Neurophysiologie clinique (B.G.), Hôpital Pitié-Salpêtrière; Inserm UMR-S 678 (H.B.), Laboratoire d'Imagerie Fonctionnelle, UPMC-Paris 6, Paris; and CEA (C.P.), NeuroSpin, Gif-Sur-Yvette, France.
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Sophie Rivaud-Péchoux
From APHP (C.E., M.-L.W., B.D., M.V.), Département de neurologie, Hôpital Pitié-Salpêtrière; Sorbonne Universités (C.E., C.G., M.-L.W., L.Y.C., B.D., P.P., S.L., S.R.-P., M.V.), UPMC Université Paris 06, Inserm U1127, CNRS UMR 7225, UM 75, ICM; APHP (C.E., A.D., M.V.), INSERM, ICM, Centre d’Investigation Clinique Pitié Neurosciences, CIC-1422, Département des Maladies du Système Nerveux, Hôpital Pitié-Salpêtrière; Equipex MATRICE (S.M.), Université Paris 1 Panthéon-Sorbonne; Centre de Neuroimagerie de Recherche (C.G., L.Y.C., S.L.), Institut du Cerveau et de la Moelle Epinière; Centre Inter-Régional de Coordination de la Maladie de Parkinson (M.-L.W., B.D., M.V.) and Département de Neurophysiologie clinique (B.G.), Hôpital Pitié-Salpêtrière; Inserm UMR-S 678 (H.B.), Laboratoire d'Imagerie Fonctionnelle, UPMC-Paris 6, Paris; and CEA (C.P.), NeuroSpin, Gif-Sur-Yvette, France.
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Marie Vidailhet
From APHP (C.E., M.-L.W., B.D., M.V.), Département de neurologie, Hôpital Pitié-Salpêtrière; Sorbonne Universités (C.E., C.G., M.-L.W., L.Y.C., B.D., P.P., S.L., S.R.-P., M.V.), UPMC Université Paris 06, Inserm U1127, CNRS UMR 7225, UM 75, ICM; APHP (C.E., A.D., M.V.), INSERM, ICM, Centre d’Investigation Clinique Pitié Neurosciences, CIC-1422, Département des Maladies du Système Nerveux, Hôpital Pitié-Salpêtrière; Equipex MATRICE (S.M.), Université Paris 1 Panthéon-Sorbonne; Centre de Neuroimagerie de Recherche (C.G., L.Y.C., S.L.), Institut du Cerveau et de la Moelle Epinière; Centre Inter-Régional de Coordination de la Maladie de Parkinson (M.-L.W., B.D., M.V.) and Département de Neurophysiologie clinique (B.G.), Hôpital Pitié-Salpêtrière; Inserm UMR-S 678 (H.B.), Laboratoire d'Imagerie Fonctionnelle, UPMC-Paris 6, Paris; and CEA (C.P.), NeuroSpin, Gif-Sur-Yvette, France.
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Full PDF
Citation
Antisaccades in Parkinson disease
A new marker of postural control?
Claire Ewenczyk, Salma Mesmoudi, Cécile Gallea, Marie-Laure Welter, Bertrand Gaymard, Adèle Demain, Lydia Yahia Cherif, Bertrand Degos, Habib Benali, Pierre Pouget, Cyril Poupon, Stéphane Lehericy, Sophie Rivaud-Péchoux, Marie Vidailhet
Neurology Feb 2017, 88 (9) 853-861; DOI: 10.1212/WNL.0000000000003658

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Abstract

Objective: To describe the relation between gaze and posture/gait control in Parkinson disease (PD) and to determine the role of the mesencephalic locomotor region (MLR) and cortex-MLR connection in saccadic behavior because this structure is a major area involved in both gait/postural control and gaze control networks.

Methods: We recruited 30 patients with PD with or without altered postural control and 25 age-matched healthy controls (HCs). We assessed gait, balance, and neuropsychological status and separately recorded gait initiation and eye movements (visually guided saccades and volitional antisaccades). We identified correlations between the clinical and physiologic parameters that best characterized patients with postural instability. We measured resting-state functional connectivity in 2 pathways involving the frontal oculomotor cortices and the MLR and sought correlations with saccadic behavior.

Results: Patients with PD with postural instability showed altered antisaccade latencies that correlated with the stand-walk-sit time (r = 0.78, p < 0.001) and the duration of anticipatory postural adjustments before gait initiation (r = 0.61, p = 0.001). Functional connectivity between the pedunculopontine nucleus (PPN) and the frontal eye field correlated with antisaccade latency in the HCs (r = −0.54, p = 0.02) but not in patients with PD.

Conclusions: In PD, impairment of antisaccade latencies, a simple and robust parameter, may be an indirect marker correlated with impaired release of anticipatory postural program. PPN alterations may account for both antisaccade and postural impairments.

GLOSSARY

APA=
anticipatory postural adjustments;
BR=
bootstrap ratio;
CN=
cuneiform nucleus;
FC=
functional connectivity;
FEF=
frontal eye field;
FP=
fixation point;
HC=
healthy control;
MLR=
mesencephalic locomotor region;
PCA=
principal component analysis;
PD=
Parkinson disease;
PDPI−=
Parkinson disease without postural instability;
PDPI+=
Parkinson disease with postural instability;
PI=
postural instability;
PPN=
pedunculopontine nucleus;
ROI=
region of interest;
SC=
superior colliculus;
SEF=
supplementary eye field;
SMA=
supplementary motor area;
SWST=
stand-walk-sit time;
UPDRS=
Unified Parkinson's Disease Rating Scale;
VGS=
visually guided saccades

Footnotes

  • ↵* These authors contributed equally to this work.

  • 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.

  • Supplemental data at Neurology.org

  • Received June 8, 2016.
  • Accepted in final form November 29, 2016.
  • © 2017 American Academy of Neurology
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