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Abstract

Background

Vestibular symptoms/signs frequently coexist with migraine, but the mechanisms of migraine-related vestibular dysfunction remain to be elucidated. This study aimed to determine altered brain metabolism in vestibular migraine.

Methods

Two patients with vestibular migraine underwent ¹⁸F-fluorodeoxy glucose (FDG) positron-emission tomography (PET) during and between attacks of vestibular migraine in addition to detailed neurotological evaluation. We analyzed the regional brain metabolism of the patients in comparison with that of age-matched healthy controls in each patient. We also compared ictal with interictal FDG PET using a subtraction method.

Results

During the attacks, both patients showed an activation of the bilateral cerebellum and frontal cortices, and deactivation of the bilateral posterior parietal and occipitotemporal areas. One patient also showed hypermetabolism in the dorsal pons and midbrain, right posterior insula, and right temporal cortex while the other patient had an additional activation of the left temporal cortex. Compared with interictal images, ictal PET showed increased metabolism in the bilateral cerebellum, frontal cortices, temporal cortex, posterior insula, and thalami.

Conclusion

During the attacks of vestibular migraine, the increased metabolism in the temporo-parieto-insular areas and bilateral thalami indicates activation of the vestibulo-thalamo-cortical pathway, and decreased metabolism in the occipital cortex may represent reciprocal inhibition between the visual and vestibular systems.

Keywords

Migraine vertigo vestibular migraine PET metabolism

Introduction

Vestibular symptoms/signs frequently coexist with migraine and include dizziness/vertigo, motion sickness and imbalance (1 –5). Only recently, the Committee for Classification of Vestibular Disorders of the Bárány Society and the Migraine Classification Subcommittee of the International Headache Society (IHS) have jointly formulated diagnostic criteria for “vestibular migraine” that was also termed as “migraine-associated vertigo” or “migrainous vertigo.” However, the mechanisms of migraine-related vestibular dysfunction remain to be elucidated. There have been several hypotheses on the pathophysiology of vestibular symptoms/signs in migraine. The vestibular nuclei receive noradrenergic inputs from the locus ceruleus (6) and serotoninergic inputs from the dorsal raphe nucleus (7). Accordingly, activation of these nuclei during migraine attacks may give rise to vestibular symptoms. Since the trigeminal nucleus caudalis also has reciprocal connections with the vestibular nuclei, and neurogenic inflammation of the trigeminal system is believed to be a mechanism of migraine (8), trigeminal activation may provoke vestibular symptoms during migraine attacks. Otherwise, cortical spreading depression may influence the vestibular nuclei via direct projections from the posterior parietal cortex (2). The direct vasodilator effect of substance P, neurokinin A and calcitonin gene-related peptide from the trigeminal and eighth cranial nerve fibers is another hypothesis (9). Since trigeminal sensory innervations are prominent in the inner ear structures, such as the stria vascularis and crista ampularis (10), direct activation of the inner ear structures by neuropeptides may also give rise to dizziness/vertigo and otologic findings (11) during migraine attacks. Other explanations include vasospasm-induced ischemia of the labyrinth (12), and genetic abnormalities of the calcium channels, as have been found in episodic ataxia type 2 and familial hemiplegic migraine that may develop migraine and vertigo in common (13).

Functional imaging of the brain during and between migraine attacks may provide insights into the pathophysiology of migraine. Previously, positron-emission tomography (PET) revealed hypermetabolism of the locus cereleus and dorsal raphe nucleus during migraine attacks. Also, activation of the cingulate, bilateral insulae and cerebellum has been noted during the attacks. Another study also lateralized the hypermetabolic pontine area on the side of headache (14,15). Recently, functional magnetic resonance imaging (MRI) also demonstrated ictal hypermetabolism in the red nucleus, substantia nigra, pons, medial longitudinal fasciculus and periaqueductal gray (PAG) in migraineuers (16). In contrast, patients with migraine without aura showed hypoperfusion of the postcentral, inferior temporal and inferior frontal gyri (17), and posterior cerebral cortex (18,19).

According to the findings described above, activation of the dorsal brainstem appears to be involved in the generation of migraine. The dorsal raphe nucleus and PAG constitute the descending nociceptive pathways and contribute to autonomic control via norepinephrinergic and serotoninergic projections (20). Hyperactivation of the dorsal brainstem nuclei leads to pain by modulation of the central pain pathway, vasodilation of the dural arteries, plasma extravasation and release of vasoactive substances (21).

However, altered brain metabolism has not been sought during attacks of vestibular migraine. Herein, we report findings of ictal PET in two patients with vestibular migraine in comparison with interictal brain metabolism.

Materials and methods

Subjects

Patient 1

This 30-year-old woman had suffered from migrainous headaches for 15 years. The headache was pulsating mostly on both sides, and was accompanied by nausea, vomiting, phonophobia, photophobia, and vertigo. She frequently experienced flashing lights in both eyes after the resolution of the headaches. Severe headaches tended to develop a couple of times a month and lasted a few hours to days. The headache and vertigo tended to develop simultaneously. The headaches partially responded to analgesics, and the headache frequency had decreased with a beta blocker (propranolol). She denied a family history of migraine. Between the attacks of migraine headaches, she showed subtle left-beating nystagmus without fixation that changed into right-beating nystagmus after horizontal head shaking. Horizontal smooth pursuit (SP) and saccades were normal. Other findings of neurological and neurotological examinations were nonrevealing. During the attacks of vestibular migraine, she showed similar findings except for prominent downbeat nystagmus after horizontal head shaking (perverted head-shaking nystagmus (HSN)). The patient had an ictal PET three days after the onset of headache when she still had the symptoms, and an interictal PET two weeks after the cessation of the headache when she was free of symptoms.

Patient 2

This 57-year-old woman had a history of migrainous headaches for about 40 years. The headache was throbbing usually in the right side. The headache began to accompany vertigo five years before. The headache and vertigo usually lasted several days with nausea and vomiting. She denied tinnitus, ear fullness, or hearing loss. The headache responded to triptan. She denied a familial history of migraine.

Between the attacks, she had no spontaneous or HSN, but showed subtle downbeat nystagmus during straight head hanging. Horizontal saccades and SP were normal. The results of cervical vestibular-evoked myogenic potential and bithermal caloric and rotatory chair tests were within normal range. During the ictus when the PET was taken, she had migrainous headache and vertigo. Examination showed subtle left-beating spontaneous nystagmus without fixation. Horizontal head impulse tests were normal. She also showed subtle left-beating horizontal-torsional nystagmus with a downbeat component during head turning to either side while supine and Dix-Hallpike maneuver in either direction. Horizontal saccades were normal, but horizontal SP was mildly impaired. The patient had an ictal PET two days after the headache onset when she still suffered from symptoms, and an interictal PET 10 days after cessation of the headache when the symptoms were completely resolved.

Both patients met the diagnostic criteria for vestibular migraine (22).

Oculography

In both patients, eye movements were recorded with a video-oculography system (SMI, Teltow, Germany) between and during the attacks of vestibular migraine. Patients had recording of spontaneous nystagmus with/without fixation and gaze-evoked nystagmus in the horizontal (±30°) and vertical (±20°) planes. HSN was induced using a passive head-shaking maneuver. After grasping the patient’s head firmly on both sides with the head pitched forward by approximately 30°, the head was shaken horizontally in a sinusoidal fashion at a rate of 2.8 Hz with an approximate amplitude of ±10° for 15 seconds. Detailed methods and normative data have been described previously (23).

To induce positional nystagmus, patients lied supine from sitting and turned their heads to either side while in supine. Then, patients were moved from a supine to a sitting position and the head was bent down. Patients were also subjected to right and left Dix-Hallpike maneuvers and straight head hanging test (24).

Horizontal saccades were generated by asking the patients to follow a target moving on a light bar with ranges of ±5°, ±10° and ±15°. For each saccade, latency, accuracy and peak velocity were computed and compared with the data from 50 normal controls. The stimulus for horizontal SP was a light target moving in a sinusoidal pattern at peak velocities of 10°/s and 20°/s. The amplitude of target motion was 20°. For gain, the peak eye velocity was compared with the target velocity after eliminating saccades. Then, average gain from the accepted cycles was compared with the values from 50 age-matched controls. Impaired SP was defined when the SP gain in the patient was less than the mean–2 standard deviations (SD) of that in the age-matched normal controls at either peak target velocity (25).

Brain ¹⁸F-fluorodeoxy glucose (FDG)-PET scan

Patients underwent FDG-PET twice: during an attack of vestibular migraine (ictal PET) and during the headache-free phase (interictal PET). The subjects had fasted for at least six hours before the PET study. The brain imaging was started 40 minutes after a bolus injection of 4.8 MBq/kg FDG and continued for 15 minutes. During the FDG equilibration period for 40 minutes, the patients were instructed to remain lying comfortably in a dimly lit, quiet waiting room. All studies were conducted using Allegro PET scanner (Philips Medical Systems, Cleveland, OH, USA) (26). Ten-minute emission scans and attenuation maps using a Cs-137 transmission source were obtained. Images were reconstructed using the three-dimensional (3D) row-action maximum-likelihood algorithm with a 3D image filter of 128 × 128 × 90 matrices with a pixel size of 2 × 2 × 2 mm³, and attenuation correction was performed.

Imaging preprocessing and statistical analyses were conducted using SPM 5 (Statistical Parametric Mapping 5; Wellcome Department of Cognitive Neurology, London, UK). In each patient, the regional abnormality of cerebral metabolic activity was determined by comparing the patient’s scan with those of 15 age-matched healthy women selected from our database. The mean age of the controls for patient 1 was 29.1 ± 4.9 years, and for patient 2 was 56.5 ± 3.5 years. The significance was considered when a cluster consisting of at least 100 contiguous voxels exceeded a threshold height of p < 0.005. And the differences in the regional metabolism between the ictal and interictal images for each patient were also assessed by subtracting the images from each other using Analyze 10.0 workspace (AnalyzeDirect Inc, KS, USA). The voxel values of the ictal and interictal scans were normalized to the mean values of the brain and subtracted. To find significant regional activation in the ictal scan, the threshold was set as 2 SD from the mean values in the subtraction image.

Results

Interictal PET

Between attacks of headache and vertigo, patient 1 showed hypometabolism in the right cerebellum, and hypermetabolism in the bilateral centrum semiovale, bilateral fronto-parietal cortices and temporo-occipital lobes. In contrast, patient 2 had hypometabolism in the bilateral fronto-parieto-occipital areas, and increased metabolism in bilateral cerebellum and left temporal lobe (Figure 1).

Figure 1.

Interictal brain metabolism in the patients. Compared with age-matched normal controls, patient 1 showed hypometabolism in the right cerebellum, and hypermetabolism in the bilateral centrum semiovale, bilateral fronto-parietal cortices, and temporo-occipital lobes (a). In contrast, patient 2 had hypometabolism in the bilateral fronto-parieto-occipital areas, and increased metabolism in bilateral cerebellum and left temporal lobe (b). For visualization of the t score statistics (SPM{t} map), the significant voxels (p < 0.005, k > 100) were superimposed on the T1-weighted MRI.

Ictal PET

During attacks of vestibular migraine, both patients showed an activation of the bilateral cerebellum, thalamus and frontal cortices. Patient 1 also showed hypermetabolism in the dorsal pons while patient 2 had an additional activation of left temporal cortex and the splenium of the corpus callosum. In contrast, both patients exhibited hypometabolism in the posterior parietal and occipitotemporal areas (Figure 2).

Figure 2.

Altered brain metabolism during attacks of vestibular migraine. Both patients showed an activation of the bilateral cerebellum, thalami and frontal cortices ((a) and (b)). Patient 1 also showed hypermetabolism in the dorsal pons (a) while patient 2 had an additional activation of the left temporal cortex and the splenium of the corpus callosum (b).

Comparison of interictal and ictal PET

Subtraction images demonstrated the differences between ictal and interictal regional metabolism. Compared with interictal images, ictal PET commonly showed increased metabolism of the bilateral cerebellum, frontal cortices and thalami in both patients (Figure 3). In contrast, the metabolism decreased in the bilateral occipitotemporal and posterior parietal cortices during the ictus. In patient 1, the bilateral cerebellum showed hypermetabolism even during the interictal period, but the intensity and extent of cerebellar hypermetabolism markedly increased during the ictus. In patient 2, the frontoparietal interictal hypometabolism became rather normalized during the ictal phase.

Figure 3.

Subtraction images of the ictal and interictal brain PET. In both patients, compared with interictal PET, ictal images also show significantly increased metabolism in bilateral cerebellum, medial thalami and frontotemporal cortices. Expressed on the T1-weighted MRIs are the regions with a change greater than 2 standard deviations of the mean value of subtracted ictal–interictal activities throughout the whole brain.

Discussion

Even though previous studies have reported altered brain metabolism in patients with migraine with or without aura (Tables 1 and 2), this is the first study on deranged brain metabolism in patients with vestibular migraine.

Table 1.

Brain metabolism between and during the ictus in our patients.

Patients	1/F/30	2/F/57
Interictal
Activation	Rt lower medulla	Bilateral cerebellum
	Bilateral temporo-occipital lobes	Lt temporal cortex.
	Bilateral frontoparietal cortices
	Bilateral corona radiata
	Rt cingulatecortex
Deactivation	Rt cerebellum	Bilateral fronto-parieto-occipital areas
Ictal
Activation	Rt cerebellum	Bilateral cerebellum
	Lt dorsalpons	Lt inferior temporal cortex
	Bilateral thalami	Lt frontal cortex
	Bilateral frontal cortices	Bilateral medial thalami
	Bilateral corona radiata	Lt temporal cortex
	Bilateral corona radiata	Splenium of the corpus callosum
Deactivation	Bilateral fronto-parieto-occipital areas	Bilateral occipitoparietal cortices
Ictal vs interictal
Activation	Bilateral cerebellum	Bilateral cerebellum
	Bilateral thalami	Right medial thalamus
	Bilateral frontal cortices	Bilateral frontoparietal cortices
	Bilateral frontal cortices	Lt perisylvian temporal cortex

F: female; Lt: left; Rt: right.

Table 2.

Altered brain metabolism during the ictus in the previous reports on migraine.

Study	Subjects/symptom	Activation sites
Woods et al. (1994) (19)	Without aura (n = 1)	Bilateral occipitotemporal areas.
Weiller et al. (1995) (15)	Without aura (n = 9)	Dorsoraphe nucleus
		Locus ceruleus
		Cingulate cortex
Cutrer et al. (1998) (37)	With visual aura (n = 4)	Contralateral visual cortex.
Sanchez et al. (1999) (18)	With (n = 14) and without (n = 14) aura	Occipital cortex contralateral to headache area
Bahra et al. (2001) (36)	Without aura (n = 1)	Rostral brain stem
		Intra and extracranial vessels
		Cingulate cortex
		Prefrontal and posterior insular areas
		Bilateral cerebellar cortices
		Thalamus
		Superior parietal cortex
		Supplementary motor cortex
		Lentiform nucleus
Cao et al. (2002) (16)	With (n = 23) and without (n = 3) aura	Red nucleus and substantia nigra Periaqueductal gray matter
Afridi et al. (2005) (14)	With (n = 8) and without (n = 16) aura	Dorsal lateral pons
		Cerebellum
		Insula
		Anterior cingulate
		Prefrontal cortex
		Putamen

Clinical findings

Neuro-otological findings of vestibular migraine have both central and peripheral features. In a previous study, 10 of 20 patients with vestibular migraine showed central features of vestibulopathy (11). Both our patients also showed subtle spontaneous nystagmus with normal head impulse test, and one of them exhibited perverted HSN during the vestibular migraine attacks, which also indicates a central type of vestibular dysfunction (27 –30).

Interictal brain metabolism

Between the vestibular migraine attacks, patient 2 showed increased metabolism in the bilateral cerebellum. Previously, the cerebellar hyperfunction between the attacks of vestibular migraine has been ascribed to an adaptive mechanism to suppress the hyperactive vestibular system (31). Of interest, this patient with basal cerebellar hypermetabolism did not show interictal activation of the brainstem and cortical structures involved in the generation of pain and processing of vestibular sensation. The scattered or diffuse hypometabolism in bilateral fronto-parieto-occipital areas may be related to interictal suppression of the structures related to perception of pain and vestibular symptoms.

Ictal activation of the brain

Patients with migraine may suffer from cerebellar symptoms such as dizziness, dysarthria and ataxia (32). Our patients showed normal or mildly increased cerebellar metabolism between migraine attacks, but markedly enhanced metabolism in the bilateral cerebellum during the ictus. Previously, ocular motor signs of the vestibulocerebellar dysfunction, such as saccadic pursuit and gaze-evoked nystagmus, have also been reported in vestibular migraine (11). However, in view of the increased tilt suppression of the vestibulo-ocular reflex in a previous study on migraineurs (31), the cerebellar hypermetabolism between or during attacks of vestibular migraine may be better explained by an adaptive cerebellar mechanism to suppress the hyperactive vestibular system in these patients.

Bilateral medial thalami were also activated in both patients. Hypermetabolism in the temporal cortex and thalamus may have been caused by activation of the vestibular nucleus and the vestibulo-cortical projections via the posterolateral thalamus. Indeed, patients with unilateral vestibular neuritis showed activation of bilateral thalami in addition to vestibular cortical areas (33).

The left temporal cortex was activated in patient 2 during the vestibular migraine. In humans, vestibular processing involves the posterior insula, superficial part of the temporoparietal junction, superior temporal regions, sensorimotor cortex, hippocampus and fronto-parieto-occipital areas (34). However, electrical stimulation of human brain cortex found that the temporo-perisylvian cortex is particularly sensitive for dizziness (35). Unilateral vestibular stimulation in healthy volunteers also induces activation of both temporo-parieto-insular areas, dominantly in the stimulated side (33). So, the activation of the vestibular corticies in our patient is consistent with the vestibular symptoms during the attacks. The hypermetabolism in the perisylvian temporal cortex, which had not been found in the previous studies on the patients with migraine, supports the vestibulo-cortical activation in our patients (35). A previous study reported hypermetabolism of the posterior insula and thalamus in patients with migraine even though there was no description of dizziness (36).

One of our patients showed an activation of the right dorsal pons, which was also found in previous studies (14,15). Since the locus ceruleus and the dorsal raphe nucleus have noradrenergic and serotoninergic projections to the vestibular nuclei (7), activation of the dorsal pons in the areas of the locus ceruleus and dorsal raphe nucleus may affect the central vestibular structures and cause dizziness.

Ictal deactivation of the brain

Our patients also showed hypometabolism of bilateral occipitotemporal areas. Patients with visual aura showed a perfusion defect in the unilateral occipital area contralateral to the visual symptoms (18,37), which is explained by spreading depression or ischemia (38). However, our patients did not report visual aura during the attacks, and the occipitotemporal hypoperfusion was bilateral. Previously, patients with vestibular neuritis also showed deactivations in the bilateral visual cortices (33). Accordingly, the occipitotemporal deactivation observed in our patients may be better explained by reciprocal inhibition between the visual and vestibular systems (39).

Limitation of the study

This study involved only two patients, which limits the generalization of the results to explain the pathophysiology of migraine, and of vestibular migraine in particular, in the general population. The preliminary nature of our results should be supplemented by future studies with a larger number of migraineurs with or without vestibular symptoms.

Furthermore, the metabolic changes observed during the ictus cannot be solely attributed to headache and vertigo since the associated photophobia and phonophobia may have affected the cortical excitability (40,41). Indeed, the ictal hyperactivation of the temporoperisylvian cortex in patient 1 might have been related to the phonophobia experienced by the patient during the ictus even though occipital hypometabolism is not consistent with the metabolic changes observed in photophobia (15,42,43). This issue would be resolved with a comparison of the metabolism among migraineurs with and without vertigo, which again remains a subject of future studies.

Conclusion

During attacks of vestibular migraine, the increased metabolism of the temporo-parieto-insular areas and bilateral thalami indicates activation of the vestibulo-thalamo-vestibulocortical pathway, and decreased metabolism in the occipital cortex may represent reciprocal inhibition between the visual and vestibular systems.

Clinical implications

This is the first study on deranged brain metabolism in patients with vestibular migraine.

Footnotes

Author contributions

J.H. Shin analyzed and interpreted the data and wrote the manuscript. Y.K. Kim and H.-J. Kim analyzed and interpreted the data, and revised the manuscript. J.-S. Kim, MD, as the corresponding author, conducted the design and conceptualization of the study, interpretation of the data, and drafting and revising of the manuscript.

Funding

This study was supported by a grant from the Korea Health 21 R&D Project, Ministry of Health & Welfare, Republic of Korea (A080750).

Conflicts of interest

J.-S. Kim serves as an associate editor of Frontiers in Neuro-otology and on the editorial boards of the Journal of Korean Society of Clinical Neurophysiology, Research in Vestibular Science, Journal of Clinical Neurology, Frontiers in Neuro-ophthalmology, Journal of Neuro-ophthalmology, and Case Reports in Ophthalmological Medicine; and has received research support from SK Chemicals Co. Ltd.

J.H. Shin, Y.K. Kim and H.-J. Kim have nothing to declare.

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Altered brain metabolism in vestibular migraine: Comparison of interictal and ictal findings

Abstract

Background

Methods

Results

Conclusion

Keywords

Introduction

Materials and methods

Subjects

Patient 1

Patient 2

Oculography

Brain 18F-fluorodeoxy glucose (FDG)-PET scan

Results

Interictal PET

Ictal PET

Comparison of interictal and ictal PET

Discussion

Clinical findings

Interictal brain metabolism

Ictal activation of the brain

Ictal deactivation of the brain

Limitation of the study

Conclusion

Clinical implications

Footnotes

Author contributions

Funding

Conflicts of interest

References

Brain ¹⁸F-fluorodeoxy glucose (FDG)-PET scan