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

TY - JOUR

T1 - Brain Processing of Visual Self-Motion Stimuli in Patients With Migraine

T2 - An fMRI Study

AU - Carvalho, Gabriela F

AU - Mehnert, Jan

AU - Basedau, Hauke

AU - Luedtke, Kerstin

AU - May, Arne

N1 - © 2021 American Academy of Neurology.

PY - 2021/9/7

Y1 - 2021/9/7

N2 - 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.

AB - 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.

KW - Adult

KW - Brain/physiopathology

KW - Cross-Sectional Studies

KW - Female

KW - Humans

KW - Magnetic Resonance Imaging

KW - Male

KW - Migraine Disorders/physiopathology

KW - Motion Perception/physiology

U2 - 10.1212/WNL.0000000000012443

DO - 10.1212/WNL.0000000000012443

M3 - SCORING: Journal article

C2 - 34290130

VL - 97

SP - e996-e1006

JO - NEUROLOGY

JF - NEUROLOGY

SN - 0028-3878

IS - 10

ER -