Interictal cortical hyperresponsiveness in migraine is directly related to the presence of aura

Datta, Ritobrato; Aguirre, Geoffrey K.; Hu, Siyuan; Detre, John A.; Cucchiara, Brett

doi:10.1177/0333102412474503

Cited by 111 publications

(169 citation statements)

References 36 publications

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“…Indeed, migraineurs with visual aura show elevated interictal BOLD responses to visual stimulation, but normal resting CBF, comparing to both migraineurs without aura and controls. 47 This could indicate that migraineurs with aura have normal CTH during rest, but fail to homogenize their capillary flows fully during functional activation where metabolic demands increase. Our analysis shows that the ability to homogenize capillary flow patterns may prove critical for tissue survival in relation to CSDs in injured tissue.…”

Section: May 2015mentioning

confidence: 99%

Neurovascular Coupling During Cortical Spreading Depolarization and –Depression

Østergaard

Dreier

Hadjikhani

et al. 2015

Stroke

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A B Figure 1. A, The importance of capillary flow patterns (yellow arrows) for the efficacy of oxygen extraction. Intravascular colors indicate blood saturation (red, fully oxygenated; darker blue, more deoxygenated) and surrounding darker blue colors indicate lower tissue oxygen tension-adapted from Østergaard et al. 23 Copyright ©2013, The Authors (see: http://creativecommons.org/licenses/by-nc-sa/3.0/). In the resting, normal brain (top), erythrocyte velocities vary greatly among capillaries, with little oxygen being extracted from fast-flowing blood. 22 As cerebral blood flow (CBF) increases (right), capillary flow patterns homogenize in parallel. 22 This phenomenon reduces the functional shunting that otherwise occurs when erythrocytes pass through capillaries at short transit times. Although the mean transit time (MTT) of blood through the capillary bed is related to CBF through the central volume theorem (MTT=CBV/CBF, where CBV is the capillary blood volume), capillary transit time heterogeneity (CTH) indicates the distribution of capillary transit times relative to this mean (eg, in terms of their standard deviation). Both MTT and CTH are measured in seconds, and the degree of functional shunting generally increases as CTH approaches MTT.24 Bottom, Capillary dysfunction, characterized by elevated CTH relative to MTT, and failure of capillary flow patterns to homogenize during hyperemia. The conditions may be the result of pericyte dysfunction, changes in blood viscosity or capillary wall morphology, or external capillary compression. These changes hinder the redistribution of blood across the capillary bed, with less affected capillary paths tending to act as functional shunts for oxygenated blood. Biophysically, the only means of attenuating the accompanying oxygen loss is to reduce transit times across all capillaries, that is, to attenuate CBF and CBF responses. 25 The accompanying reduction in net oxygen supply reduces tissue oxygen tension as cells continue to use oxygen, increasing blood-tissue concentration gradients and net oxygen extraction. 25 With flow responses attenuated, oxygen extraction can be increased from the 30% of normal brain up to near unity, and normal brain function maintained although capillary dysfunction becomes more severe. 25 It is important to note that current state-of-the-art algorithms to generate maps of transit time-related metrics based on perfusion-weighted magnetic resonance imaging or computed tomography cannot distinguish changes in tracer retention caused by prolonged MTT (reduced CBF) from changes caused by capillary flow disturbances (capillary dysfunction). 25 The effects of CTH must therefore be separately modeled to ascertain whether clinical signs of ischemia are indeed caused by limited blood supply or by capillary dysfunction.26 B, The acute changes in capillary morphology that accompany conditions in which CSD are common. In traumatic brain injury (TBI; i), massive swelling of the perivascular astrocytic end feet (AE) and flattening or compression of the...

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Section: May 2015mentioning

confidence: 99%

Neurovascular Coupling During Cortical Spreading Depolarization and –Depression

Østergaard

Dreier

Hadjikhani

et al. 2015

Stroke

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“…The study by Datta et al (2) published in the current issue of Cephalalgia tried to answer the last three questions by focusing on the neuroimaging correlate of visual cortical hyperresponsivity. To this purpose, they used multi-modality high-resolution (3 Tesla) functional magnetic resonance imaging (fMRI) to examine the hemodynamic brain response (BOLD) to light stimulation in a large cohort of migraine patients during the pain-free state, as well as in healthy controls.…”

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confidence: 99%

From neuroimaging to the bedside: Take the sheets off the thalamus

Coppola

2013

Cephalalgia

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The common migraine phenotypes, in their episodic forms with and without aura, are disorders that manifest with recurrent transient ictal dysfunctions without interictal sequelae. This helps us to understand, on the one hand, why the nature of migraine continues to be so elusive and why, on the other hand, it is one of the most studied pain syndromes. A complex mixture of genetics and environmental factors interact to determine migraine susceptibility, which may be conceptualized as a milieu of subtle factors that is able to cyclically ignite migraine by affecting the interaction between neuronal and vascular components within the brain. The logical consequence is that these elusive factors, if present, should also be detectable in the pain-free period as underlying dysfunctions. Many methods are available nowadays for assessing neural functions atraumatically in humans, contributing to the great advances made in understanding the pathophysiological facets of migraine. Since the most frequent aura symptoms are visual disturbances and because clinical hypersensitivity to environmental light stimuli, i.e. photophobia, is experienced by patients not just during the attack but even outside, several research groups are particularly focused on the study of the visual system in migraine. Above all, using electrophysiological techniques it was observed that migraineurs show an increase in cortical responsivity to any kind of sensory information, visually comprised, with respect to normal subjects (1). However, several relevant questions about cortical hyperresponsivity have not yet been answered, including: Could hyperresponsivity account for the peculiar migraineur propensity to develop attacks? What are the neuroanatomical correlates of cortical hyperresponsivity? Is there any relationship between interictal visual hyperresponsivity and the visual discomfort reported by patients? Could cortical responsivity differ between migraine with and without aura so that they should be considered as two separate entities?The study by Datta et al. (2) published in the current issue of Cephalalgia tried to answer the last three questions by focusing on the neuroimaging correlate of visual cortical hyperresponsivity. To this purpose, they used multi-modality high-resolution (3 Tesla) functional magnetic resonance imaging (fMRI) to examine the hemodynamic brain response (BOLD) to light stimulation in a large cohort of migraine patients during the pain-free state, as well as in healthy controls. This study is distinct from previous reports on the same topic for three reasons: (I) the authors collected a considerably larger cohort of migraineurs and healthy subjects; (II) they studied patients with (MA) and without aura (MO) separately, not pooled together; (III) they also measured baseline metabolic activity, as reflected by resting cerebral blood perfusion. However, certain limitations of the present study should be acknowledged. Although patients were attack free before and during the scanning session, they were not checked for sub...

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“…Subsequently, there has been a shift towards the study of ''functional abnormalities'' occurring between attacks both in MwA and MwoA. For example, interictal cortical response has been evaluated by means of different visual stimuli in MwA and MwoA patients confirming a tight connection between cortical hyperexcitability and migraine aura [25]. In the last years, many BOLD-fMRI studies have been performed using experimental pain stimulation to explore pain processing-related cerebral activity in migraine.…”

Section: Discussionmentioning

confidence: 99%

The role of BOLD-fMRI in elucidating migraine pathophysiology

et al. 2013

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Migraine is a neurologic disorder characterized by disabling attacks of throbbing headache with specific features and associated symptoms. Despite the recent discoveries in basic neurosciences, migraine pathophysiology is not completely understood. Nevertheless, in the last decades, advances in functional magnetic resonance imaging (fMRI) have significantly provided new insights into migraine mechanisms. Blood oxygen level dependent (BOLD) fMRI technique is the most commonly used method to explore brain function and connectivity due to high temporal and spatial resolution. The purpose of this review is to present a synthesis of recent BOLD-fMRI studies which have allowed us to elucidate the complex process involved in migraine pathophysiology.

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Interictal cortical hyperresponsiveness in migraine is directly related to the presence of aura

Cited by 111 publications

References 36 publications

Neurovascular Coupling During Cortical Spreading Depolarization and –Depression

Neurovascular Coupling During Cortical Spreading Depolarization and –Depression

From neuroimaging to the bedside: Take the sheets off the thalamus

The role of BOLD-fMRI in elucidating migraine pathophysiology

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