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June 04, 2019; 92 (23) Article

Abnormal thalamocortical network dynamics in migraine

View ORCID ProfileYiheng Tu, Zening Fu, Fang Zeng, Nasim Maleki, Lei Lan, Zhengjie Li, Joel Park, Georgia Wilson, Yujie Gao, Mailan Liu, Vince Calhoun, Fanrong Liang, Jian Kong
First published May 10, 2019, DOI: https://doi.org/10.1212/WNL.0000000000007607
Yiheng Tu
From the Department of Psychiatry (Y.T., N.M., J.P., G.W., J.K.), Massachusetts General Hospital and Harvard Medical School, Charlestown; The Mind Research Network (Z.F., V.C.), Albuquerque, NM; Acupuncture and Tuina School/3rd Teaching Hospital (F.Z., L.L., Z.L., F.L.), Chengdu University of Traditional Chinese Medicine, Chengdu; Traditional Chinese Medicine School (Y.G.), Ningxia Medical University, Yinchuan; and The Acupuncture and Tuina School (M.L.), Hunan University of Chinese Medicine, Changsha, China.
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  • ORCID record for Yiheng Tu
Zening Fu
From the Department of Psychiatry (Y.T., N.M., J.P., G.W., J.K.), Massachusetts General Hospital and Harvard Medical School, Charlestown; The Mind Research Network (Z.F., V.C.), Albuquerque, NM; Acupuncture and Tuina School/3rd Teaching Hospital (F.Z., L.L., Z.L., F.L.), Chengdu University of Traditional Chinese Medicine, Chengdu; Traditional Chinese Medicine School (Y.G.), Ningxia Medical University, Yinchuan; and The Acupuncture and Tuina School (M.L.), Hunan University of Chinese Medicine, Changsha, China.
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Fang Zeng
From the Department of Psychiatry (Y.T., N.M., J.P., G.W., J.K.), Massachusetts General Hospital and Harvard Medical School, Charlestown; The Mind Research Network (Z.F., V.C.), Albuquerque, NM; Acupuncture and Tuina School/3rd Teaching Hospital (F.Z., L.L., Z.L., F.L.), Chengdu University of Traditional Chinese Medicine, Chengdu; Traditional Chinese Medicine School (Y.G.), Ningxia Medical University, Yinchuan; and The Acupuncture and Tuina School (M.L.), Hunan University of Chinese Medicine, Changsha, China.
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Nasim Maleki
From the Department of Psychiatry (Y.T., N.M., J.P., G.W., J.K.), Massachusetts General Hospital and Harvard Medical School, Charlestown; The Mind Research Network (Z.F., V.C.), Albuquerque, NM; Acupuncture and Tuina School/3rd Teaching Hospital (F.Z., L.L., Z.L., F.L.), Chengdu University of Traditional Chinese Medicine, Chengdu; Traditional Chinese Medicine School (Y.G.), Ningxia Medical University, Yinchuan; and The Acupuncture and Tuina School (M.L.), Hunan University of Chinese Medicine, Changsha, China.
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Lei Lan
From the Department of Psychiatry (Y.T., N.M., J.P., G.W., J.K.), Massachusetts General Hospital and Harvard Medical School, Charlestown; The Mind Research Network (Z.F., V.C.), Albuquerque, NM; Acupuncture and Tuina School/3rd Teaching Hospital (F.Z., L.L., Z.L., F.L.), Chengdu University of Traditional Chinese Medicine, Chengdu; Traditional Chinese Medicine School (Y.G.), Ningxia Medical University, Yinchuan; and The Acupuncture and Tuina School (M.L.), Hunan University of Chinese Medicine, Changsha, China.
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Zhengjie Li
From the Department of Psychiatry (Y.T., N.M., J.P., G.W., J.K.), Massachusetts General Hospital and Harvard Medical School, Charlestown; The Mind Research Network (Z.F., V.C.), Albuquerque, NM; Acupuncture and Tuina School/3rd Teaching Hospital (F.Z., L.L., Z.L., F.L.), Chengdu University of Traditional Chinese Medicine, Chengdu; Traditional Chinese Medicine School (Y.G.), Ningxia Medical University, Yinchuan; and The Acupuncture and Tuina School (M.L.), Hunan University of Chinese Medicine, Changsha, China.
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Joel Park
From the Department of Psychiatry (Y.T., N.M., J.P., G.W., J.K.), Massachusetts General Hospital and Harvard Medical School, Charlestown; The Mind Research Network (Z.F., V.C.), Albuquerque, NM; Acupuncture and Tuina School/3rd Teaching Hospital (F.Z., L.L., Z.L., F.L.), Chengdu University of Traditional Chinese Medicine, Chengdu; Traditional Chinese Medicine School (Y.G.), Ningxia Medical University, Yinchuan; and The Acupuncture and Tuina School (M.L.), Hunan University of Chinese Medicine, Changsha, China.
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Georgia Wilson
From the Department of Psychiatry (Y.T., N.M., J.P., G.W., J.K.), Massachusetts General Hospital and Harvard Medical School, Charlestown; The Mind Research Network (Z.F., V.C.), Albuquerque, NM; Acupuncture and Tuina School/3rd Teaching Hospital (F.Z., L.L., Z.L., F.L.), Chengdu University of Traditional Chinese Medicine, Chengdu; Traditional Chinese Medicine School (Y.G.), Ningxia Medical University, Yinchuan; and The Acupuncture and Tuina School (M.L.), Hunan University of Chinese Medicine, Changsha, China.
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Yujie Gao
From the Department of Psychiatry (Y.T., N.M., J.P., G.W., J.K.), Massachusetts General Hospital and Harvard Medical School, Charlestown; The Mind Research Network (Z.F., V.C.), Albuquerque, NM; Acupuncture and Tuina School/3rd Teaching Hospital (F.Z., L.L., Z.L., F.L.), Chengdu University of Traditional Chinese Medicine, Chengdu; Traditional Chinese Medicine School (Y.G.), Ningxia Medical University, Yinchuan; and The Acupuncture and Tuina School (M.L.), Hunan University of Chinese Medicine, Changsha, China.
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Mailan Liu
From the Department of Psychiatry (Y.T., N.M., J.P., G.W., J.K.), Massachusetts General Hospital and Harvard Medical School, Charlestown; The Mind Research Network (Z.F., V.C.), Albuquerque, NM; Acupuncture and Tuina School/3rd Teaching Hospital (F.Z., L.L., Z.L., F.L.), Chengdu University of Traditional Chinese Medicine, Chengdu; Traditional Chinese Medicine School (Y.G.), Ningxia Medical University, Yinchuan; and The Acupuncture and Tuina School (M.L.), Hunan University of Chinese Medicine, Changsha, China.
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Vince Calhoun
From the Department of Psychiatry (Y.T., N.M., J.P., G.W., J.K.), Massachusetts General Hospital and Harvard Medical School, Charlestown; The Mind Research Network (Z.F., V.C.), Albuquerque, NM; Acupuncture and Tuina School/3rd Teaching Hospital (F.Z., L.L., Z.L., F.L.), Chengdu University of Traditional Chinese Medicine, Chengdu; Traditional Chinese Medicine School (Y.G.), Ningxia Medical University, Yinchuan; and The Acupuncture and Tuina School (M.L.), Hunan University of Chinese Medicine, Changsha, China.
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Fanrong Liang
From the Department of Psychiatry (Y.T., N.M., J.P., G.W., J.K.), Massachusetts General Hospital and Harvard Medical School, Charlestown; The Mind Research Network (Z.F., V.C.), Albuquerque, NM; Acupuncture and Tuina School/3rd Teaching Hospital (F.Z., L.L., Z.L., F.L.), Chengdu University of Traditional Chinese Medicine, Chengdu; Traditional Chinese Medicine School (Y.G.), Ningxia Medical University, Yinchuan; and The Acupuncture and Tuina School (M.L.), Hunan University of Chinese Medicine, Changsha, China.
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Jian Kong
From the Department of Psychiatry (Y.T., N.M., J.P., G.W., J.K.), Massachusetts General Hospital and Harvard Medical School, Charlestown; The Mind Research Network (Z.F., V.C.), Albuquerque, NM; Acupuncture and Tuina School/3rd Teaching Hospital (F.Z., L.L., Z.L., F.L.), Chengdu University of Traditional Chinese Medicine, Chengdu; Traditional Chinese Medicine School (Y.G.), Ningxia Medical University, Yinchuan; and The Acupuncture and Tuina School (M.L.), Hunan University of Chinese Medicine, Changsha, China.
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Abnormal thalamocortical network dynamics in migraine
Yiheng Tu, Zening Fu, Fang Zeng, Nasim Maleki, Lei Lan, Zhengjie Li, Joel Park, Georgia Wilson, Yujie Gao, Mailan Liu, Vince Calhoun, Fanrong Liang, Jian Kong
Neurology Jun 2019, 92 (23) e2706-e2716; DOI: 10.1212/WNL.0000000000007607

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Abstract

Objective To investigate the dynamic functional connectivity of thalamocortical networks in interictal migraine patients and whether clinical features are associated with abnormal connectivity.

Methods We investigated dynamic functional network connectivity (dFNC) of the migraine brain in 89 interictal migraine patients and 70 healthy controls. We focused on the temporal properties of thalamocortical connectivity using sliding window cross-correlation, clustering state analysis, and graph-theory methods. Relationships between clinical symptoms and abnormal dFNC were evaluated using a multivariate linear regression model.

Results Five dFNC brain states were identified to characterize and compare dynamic functional connectivity patterns. We demonstrated that migraineurs spent more time in a strongly interconnected between-network state, but they spent less time in a sparsely connected state. Interestingly, we found that abnormal posterior thalamus (pulvinar nucleus) dFNC with the visual cortex and the precuneus were significantly correlated with headache frequency of migraine. Further topologic measures revealed that migraineurs had significantly lower efficiency of information transfer in both global and local dFNC.

Conclusion Our results demonstrated a transient pathologic state with atypical thalamocortical connectivity in migraineurs and extended current findings regarding abnormal thalamocortical networks and dysrhythmia in migraine.

Glossary

AUC=
area under the curve;
AUD=
auditory domain;
CC=
cognitive control domain;
dFNC=
dynamic functional network connectivity;
DM=
default mode domain;
FC=
functional connectivity;
FDR=
false discovery rate;
GICA=
group independent component analysis;
HC=
healthy controls;
ICHD=
International Classification of Headache Disorders;
ICN=
intrinsic component network;
IRB=
institutional review board;
MIG=
migraine without aura patients;
MNI=
Montreal Neurologic Institute;
rsFC=
resting-state functional connectivity;
SAS=
self-rating anxiety scale;
SC=
subcortical domain;
SDS=
self-rating depression scale;
SM=
sensorimotor domain;
TCD=
thalamocortical dysrhythmia;
TE=
echo time;
TR=
repetition time;
VS=
visual domain

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.

  • ↵* These authors contributed equally to this work.

  • Received August 9, 2018.
  • Accepted in final form February 1, 2019.
  • © 2019 American Academy of Neurology
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