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September 07, 2021; 97 (10) Research Article

Brain Processing of Visual Self-Motion Stimuli in Patients With Migraine

An fMRI Study

Gabriela F. Carvalho, View ORCID ProfileJan Mehnert, View ORCID ProfileHauke Basedau, Kerstin Luedtke, View ORCID ProfileArne May
First published July 21, 2021, DOI: https://doi.org/10.1212/WNL.0000000000012443
Gabriela F. Carvalho
From the Institute of Health Sciences (G.F.C., K.L.) Department of Physiotherapy, University of Lübeck, Germany; and Department of Systems Neuroscience (G.F.C., J.M., H.B., K.L., A.M.), University Medical Center Eppendorf, Hamburg, Germany.
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Jan Mehnert
From the Institute of Health Sciences (G.F.C., K.L.) Department of Physiotherapy, University of Lübeck, Germany; and Department of Systems Neuroscience (G.F.C., J.M., H.B., K.L., A.M.), University Medical Center Eppendorf, Hamburg, Germany.
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Hauke Basedau
From the Institute of Health Sciences (G.F.C., K.L.) Department of Physiotherapy, University of Lübeck, Germany; and Department of Systems Neuroscience (G.F.C., J.M., H.B., K.L., A.M.), University Medical Center Eppendorf, Hamburg, Germany.
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Kerstin Luedtke
From the Institute of Health Sciences (G.F.C., K.L.) Department of Physiotherapy, University of Lübeck, Germany; and Department of Systems Neuroscience (G.F.C., J.M., H.B., K.L., A.M.), University Medical Center Eppendorf, Hamburg, Germany.
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Arne May
From the Institute of Health Sciences (G.F.C., K.L.) Department of Physiotherapy, University of Lübeck, Germany; and Department of Systems Neuroscience (G.F.C., J.M., H.B., K.L., A.M.), University Medical Center Eppendorf, Hamburg, Germany.
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Brain Processing of Visual Self-Motion Stimuli in Patients With Migraine
An fMRI Study
Gabriela F. Carvalho, Jan Mehnert, Hauke Basedau, Kerstin Luedtke, Arne May
Neurology Sep 2021, 97 (10) e996-e1006; DOI: 10.1212/WNL.0000000000012443

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Abstract

Objective To investigate the behavioral and neuronal responses of patients with migraine to a visual simulation of self-motion through a virtual roller coaster ride in comparison to controls.

Methods Twenty consecutive patients with migraine from a university-based hospital headache clinic and 20 controls were included. Participants underwent an experiment where a visually displayed self-motion paradigm was presented based on customized roller coaster videos during fMRI. Within each video, blocks of motion stimulation were interleaved with low-speed upward motion in a random order. In the scanning intervals and after the experiment, participants rated their perceived level of vestibular symptoms and motion sickness during the videos. We hypothesized that patients with migraine will perceive more motion sickness and that it correlates with different central processing and brain responses.

Results Compared to controls, patients with migraine reported more dizziness (65% vs 30%; p = 0.03) and motion sickness (Simulator Sickness Questionnaire score 47.3 [95% confidence interval (CI), 37.1, 57.5] vs 24.3 [95% CI, 18.2, 30.4]) as well as longer symptom duration (01:19 minutes [95% CI, 00:51, 01:48] vs 00:27 minutes [95% CI, 00:03, 00:51]) and intensity (visual analogue scale score 0–100, 22.0 [95% CI, 14.8, 29.2] vs 9.9 [95% CI, 4.9, 14.7]) during the virtual roller coaster ride. Neuronal activity in patients with migraine was more pronounced in clusters within the superior (contrast estimate 3.005 [90% CI, 1.817, 4.194]) and inferior occipital gyrus (contrast estimate 1.759 [90% CI, 1.062, 2.456]), pontine nuclei (contrast estimate 0.665 [90% CI, 0.383, 0.946]), and within the cerebellar lobules V/VI (contrast estimate 0.672 [90% CI, 0.380, 0.964]), while decreased activity was seen in the cerebellar lobule VIIb (contrast estimate 0.787 [90% CI, 0.444, 1.130]) and in the middle frontal gyrus (contrast estimate 0.962 [90% CI, 0.557, 1.367]). These activations correlated with migraine disability (r = −0.46, p = 0.04) and motion sickness scores (r = 0.32, p = 0.04). We found enhanced connectivity between the pontine nuclei, cerebellar areas V/VI, and interior and superior occipital gyrus with numerous cortical areas in patients with migraine but not in controls.

Conclusions Migraine is related to abnormal modulation of visual motion stimuli within superior and inferior occipital gyrus, middle frontal gyrus, pontine nuclei, and cerebellar lobules V, VI, and VIIb. These abnormalities relate to migraine disability and motion sickness susceptibility.

Glossary

CI=
confidence interval;
DHI-G=
German version of the Dizziness Handicap Inventory;
EPI=
echoplanar imaging;
FOV=
field of view;
GLM=
general linear model;
MIDAS=
Migraine Disability Assessment Questionnaire;
MNI=
Montreal Neurological Institute;
MSSQ=
Motion Sickness Susceptibility Questionnaire;
PHQ-8=
Patient Health Questionnaire;
ROI=
region of interest;
SSQ=
Simulator Sickness Questionnaire

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.

  • ↵* G.F. Carvalho and J. Mehnert contributed equally as co–first authors.

  • CME Course: NPub.org/cmelist

  • Received January 27, 2021.
  • Accepted in final form June 7, 2021.
  • © 2021 American Academy of Neurology
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Letters: Rapid online correspondence

  • Reader Response: Brain Processing of a Visual Self-Motion Study in Patients With Migraine: An fMRI Study
    • VINOD K. Gupta, Medical Director-Physician, Migraine-Headache Institute, Gupta Medical Centre, S-407, Greater Kailash-Part Two, New Delhi, INDIA-110048
    Submitted July 24, 2021
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