Comparison of gray matter volume between migraine and “strict-criteria” tension-type headache

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Abstract

Background

Despite evidently distinct symptoms, tension-type headache (TTH) and migraine are highly comorbid and exhibit many similarities in clinical practice. The purpose of this study was to investigate whether both types of headaches are similar in brain morphology.

Methods

Consecutive patients with TTH and age- and sex-matched patients with migraine and healthy controls were enrolled for brain magnetic resonance imaging examination. Patients with TTH were excluded if they reported any headache features or associated symptoms of migraine. Changes in gray matter (GM) volume associated with headache diagnosis (TTH vs. migraine) and frequency (episodic vs. chronic) were examined using voxel-based morphometry. The correlation with headache profile and the discriminative ability between TTH and migraine were also investigated for these GM changes.

Results

In comparison with controls ( n = 43), the patients with TTH (25 episodic and 24 chronic) exhibited a GM volume increase in the anterior cingulate cortex, supramarginal gyrus, temporal pole, lateral occipital cortex, and caudate. The patients with migraine (31 episodic and 25 chronic) conversely exhibited a GM volume decrease in the orbitofrontal cortex. These GM changes did not correlate with any headache profile. A voxel-wise 2 × 2 factorial analysis further revealed the substantial effects of headache types and frequency in the comparison of GM volume between TTH and migraine. Specifically, the migraine group (vs. TTH) had a GM decrease in the superior and middle frontal gyri, cerebellum, dorsal striatum, and precuneus. The chronic group (vs. episodic group) otherwise demonstrated a GM decrease in the bilateral insula and anterior cingulate cortex. In receiver operating characteristic analysis, the GM volumes of the left superior frontal gyrus and right cerebellum V combined had good discriminative ability for distinguishing TTH and migraine (area under the curve = 0.806).

Conclusions

TTH and migraine are separate headache disorders with different characteristics in relation to GM changes. The major morphological difference between the two types of headaches is the relative GM decrease of the prefrontal and cerebellar regions in migraine, which may reflect a higher allostatic load associated with this disabling headache.

Electronic supplementary material

The online version of this article (10.1186/s10194-018-0834-6) contains supplementary material, which is available to authorized users.

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Most cited references 51

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Functional imaging of brain responses to pain. A review and meta-analysis (2000).

R Peyron, L García-Larrea, B Laurent (2000)

Brain responses to pain, assessed through positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) are reviewed. Functional activation of brain regions are thought to be reflected by increases in the regional cerebral blood flow (rCBF) in PET studies, and in the blood oxygen level dependent (BOLD) signal in fMRI. rCBF increases to noxious stimuli are almost constantly observed in second somatic (SII) and insular regions, and in the anterior cingulate cortex (ACC), and with slightly less consistency in the contralateral thalamus and the primary somatic area (SI). Activation of the lateral thalamus, SI, SII and insula are thought to be related to the sensory-discriminative aspects of pain processing. SI is activated in roughly half of the studies, and the probability of obtaining SI activation appears related to the total amount of body surface stimulated (spatial summation) and probably also by temporal summation and attention to the stimulus. In a number of studies, the thalamic response was bilateral, probably reflecting generalised arousal in reaction to pain. ACC does not seem to be involved in coding stimulus intensity or location but appears to participate in both the affective and attentional concomitants of pain sensation, as well as in response selection. ACC subdivisions activated by painful stimuli partially overlap those activated in orienting and target detection tasks, but are distinct from those activated in tests involving sustained attention (Stroop, etc.). In addition to ACC, increased blood flow in the posterior parietal and prefrontal cortices is thought to reflect attentional and memory networks activated by noxious stimulation. Less noted but frequent activation concerns motor-related areas such as the striatum, cerebellum and supplementary motor area, as well as regions involved in pain control such as the periaqueductal grey. In patients, chronic spontaneous pain is associated with decreased resting rCBF in contralateral thalamus, which may be reverted by analgesic procedures. Abnormal pain evoked by innocuous stimuli (allodynia) has been associated with amplification of the thalamic, insular and SII responses, concomitant to a paradoxical CBF decrease in ACC. It is argued that imaging studies of allodynia should be encouraged in order to understand central reorganisations leading to abnormal cortical pain processing. A number of brain areas activated by acute pain, particularly the thalamus and anterior cingulate, also show increases in rCBF during analgesic procedures. Taken together, these data suggest that hemodynamic responses to pain reflect simultaneously the sensory, cognitive and affective dimensions of pain, and that the same structure may both respond to pain and participate in pain control. The precise biochemical nature of these mechanisms remains to be investigated.

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The orbitofrontal cortex and reward.

E Rolls (2000)

The primate orbitofrontal cortex contains the secondary taste cortex, in which the reward value of taste is represented. It also contains the secondary and tertiary olfactory cortical areas, in which information about the identity and also about the reward value of odors is represented. The orbitofrontal cortex also receives information about the sight of objects and faces from the temporal lobe cortical visual areas, and neurons in it learn and reverse the visual stimulus to which they respond when the association of the visual stimulus with a primary reinforcing stimulus (such as a taste reward) is reversed. However, the orbitofrontal cortex is involved in representing negative reinforcers (punishers) too, such as aversive taste, and in rapid stimulus-reinforcement association learning for both positive and negative primary reinforcers. In complementary neuroimaging studies in humans it is being found that areas of the orbitofrontal cortex (and connected subgenual cingulate cortex) are activated by pleasant touch, by painful touch, by rewarding and aversive taste, and by odor. Damage to the orbitofrontal cortex in humans can impair the learning and reversal of stimulus- reinforcement associations, and thus the correction of behavioral responses when these are no longer appropriate because previous reinforcement contingencies change. This evidence thus shows that the orbitofrontal cortex is involved in decoding and representing some primary reinforcers such as taste and touch; in learning and reversing associations of visual and other stimuli to these primary reinforcers; and in controlling and correcting reward-related and punishment-related behavior, and thus in emotion.

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Understanding migraine through the lens of maladaptive stress responses: a model disease of allostatic load.

David Borsook, Nasim Maleki, Lino Becerra … (2012)

The brain and body respond to potential and actual stressful events by activating hormonal and neural mediators and modifying behaviors to adapt. Such responses help maintain physiological stability ("allostasis"). When behavioral or physiological stressors are frequent and/or severe, allostatic responses can become dysregulated and maladaptive ("allostatic load"). Allostatic load may alter brain networks both functionally and structurally. As a result, the brain's responses to continued/subsequent stressors are abnormal, and behavior and systemic physiology are altered in ways that can, in a vicious cycle, lead to further allostatic load. Migraine patients are continually exposed to such stressors, resulting in changes to central and peripheral physiology and function. Here we review how changes in brain states that occur as a result of repeated migraines may be explained by a maladaptive feedforward allostatic cascade model and how understanding migraine within the context of allostatic load model suggests alternative treatments for this often-debilitating disease. Copyright © 2012 Elsevier Inc. All rights reserved.

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Author and article information

Contributors

Wei-Ta Chen:

ORCID: http://orcid.org/0000-0003-2355-3540

+886-2-2871212 , wtchen@vghtpe.gov.tw

Journal

Journal ID (nlm-ta): J Headache Pain

Journal ID (iso-abbrev): J Headache Pain

Title: The Journal of Headache and Pain

Publisher: Springer Milan (Milan )

ISSN (Print): 1129-2369

ISSN (Electronic): 1129-2377

Publication date (Electronic): 15 January 2018

Publication date PMC-release: 15 January 2018

Publication date Collection: 2018

Volume: 19

Issue: 1

Electronic Location Identifier: 4

Affiliations

[1 ]ISNI 0000 0001 0425 5914, GRID grid.260770.4, Department of Neurology, School of Medicine, , National Yang-Ming University, ; Taipei, Taiwan

[2 ]ISNI 0000 0004 0604 5314, GRID grid.278247.c, The Neurological Institute, Taipei Veterans General Hospital, ; Taipei, Taiwan

[3 ]ISNI 0000 0001 0425 5914, GRID grid.260770.4, Brain Research Center, , National Yang-Ming University, ; Taipei, Taiwan

[4 ]ISNI 0000 0001 0425 5914, GRID grid.260770.4, Institute of Brain Science, School of Medicine, , National Yang-Ming University, ; Taipei, Taiwan

[5 ]ISNI 0000 0001 0425 5914, GRID grid.260770.4, Institute of Neuroscience, , National Yang-Ming University, ; Taipei, Taiwan

[6 ]ISNI 0000 0001 0425 5914, GRID grid.260770.4, Department of Biomedical Imaging and Radiological Sciences, , National Yang-Ming University, ; Taipei, Taiwan

Author information

Wei-Ta Chen http://orcid.org/0000-0003-2355-3540

Article

Publisher ID: 834

DOI: 10.1186/s10194-018-0834-6

PMC ID: 5768588

PubMed ID: 29335889

SO-VID: 065df3c7-467a-4534-87aa-c3e781912687

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

History

Date received : 4 December 2017

Date accepted : 2 January 2018

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100004663, Ministry of Science and Technology, Taiwan;

Award ID: NSC101-2314-B-075-068-MY2, MOST 106-2321-B-010-009-, and MOST 106-2314-B-075-026-

Award ID: 103-2321-B-010-017, 102-2321-B-010-030, 100-2314-B-010-018-MY3, 104-2745-B-010-003 and MOST 106-2321-B-010-009

Award Recipient : Wei-Ta Chen Shuu-Jiun Wang

Funded by: Taipei Veterans General Hospital

Award ID: V105C-092, V105E9-005-MY2-1, and VGHUST104-G7-1-3

Award ID: VGHUST105-G7-1-1, V105C-127, V105E9-001-MY2-1, and VTA105-V1-1-1

Award Recipient : Wei-Ta Chen Shuu-Jiun Wang

Custom metadata

ScienceOpen disciplines: Anesthesiology & Pain management

Keywords: tension-type headache,migraine,gray matter,voxel-based morphometry,magnetic resonance imaging (mri)

Data availability:

ScienceOpen disciplines: Anesthesiology & Pain management

Keywords: tension-type headache, migraine, gray matter, voxel-based morphometry, magnetic resonance imaging (mri)

Comparison of gray matter volume between migraine and “strict-criteria” tension-type headache

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Abstract

Background

Methods

Results

Conclusions

Electronic supplementary material

Related collections

Stroke MRI

Most cited references 51

Functional imaging of brain responses to pain. A review and meta-analysis (2000).

The orbitofrontal cortex and reward.

Understanding migraine through the lens of maladaptive stress responses: a model disease of allostatic load.

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