The missing link: Enhanced functional connectivity between amygdala and visceroceptive cortex in migraine

Hadjikhani, Nouchine; Ward, Noreen; Boshyan, Jasmine; Napadow, Vitaly; Maeda, Yümi; Truini, Andrea; Caramia, Francesca; Tinelli, Emanuele; Mainero, Caterina

doi:10.1177/0333102413490344

Cited by 136 publications

(127 citation statements)

References 15 publications

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“…For instance, the decrease in tissue density and activation found in areas belonging to the so-called pain matrix (the lateral pain system, thalamus, insula, cingulate…) is a well-known feature in chronic pain disorders. By contrast, connectivity changes of limbic areas and basal ganglia might be related more closely to CM, the more so that some of them have also been reported in EM but not in other cephalic pains [27]. Regarding the changes in limbic structures, one has to keep in mind, however, that depression is a major risk factor for CM [46].…”

Section: Chronic Migraine Pathophysiologymentioning

confidence: 99%

“…It is generally accepted that the common forms of migraine with or without aura (Table 2): abnormal thickness, connectivity and/or activation of certain cortical and subcortical areas [24][25][26][27], increased transmitter [28] or iron content [29][30][31], decreased ATP content [32,33] and an abnormal pattern of sensory processing [34,35]. The latter is characterized by low amplitude of initial responses and hyperresponsivity with lack of habituation of late responses during repeated sensory stimuli [36], and has been attributed to a thalamocortical dysrhythmia caused by deficient monoaminergic control by brain stem nuclei (review in [37]).…”

Section: Chronic Migraine Pathophysiologymentioning

confidence: 99%

“…cortical sensitivity and % responsivity to sensory stimuli [35,36] % fractional anisotropy thalamus (MR-DTI) [43] ! cortical thickness and activation S1, temporal lobe [26] % cortical thickness and/or activation insula, cingulate, visual areas [24,26] % rs connectivity amygdala-insula [27] % iron content PAG and globus pallidus [29][30][31] % rs connectivity PAG-precuneus, visual [25] % tissue density in PAG [129] ! olfaction-induced trigeminal nucleus activation % pre-ictally [130] % subclinical posterior circulation infarcts [30] Chronic migraine % cortical sensitivity and !…”

Section: Episodic Migraine (Interictal)mentioning

confidence: 99%

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Diagnosis, pathophysiology and management of chronic migraine: a proposal of the Belgian Headache Society

Paemeleire

Louis²,

Magis

et al. 2014

Acta Neurol Belg

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Chronic migraine (CM) is a disabling neurological condition affecting 0.5-2 % of the population. In the current third edition of the International Classification of Headache Disorders, medication overuse is no longer an exclusion criterion and CM is diagnosed in patients suffering from at least 15 headache days per month of which at least eight are related to migraine. CM is difficult to treat, and preventive treatment options are limited. We provide a pathogenetic model for CM, integrating the latest findings from neurophysiological and neuroimaging studies. On behalf of the Belgian Headache Society, we present a management algorithm for CM based on the international literature and adapted to the Belgian situation. Pharmacological treatment options are discussed, and recent data on transcranial and invasive neuromodulation studies in CM are reviewed. An integrated multimodal treatment programme may be beneficial to refractory patients, but at present, this approach is only supported by a limited number of observational studies and quite variable between centres

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Section: Chronic Migraine Pathophysiologymentioning

confidence: 99%

Section: Chronic Migraine Pathophysiologymentioning

confidence: 99%

Section: Episodic Migraine (Interictal)mentioning

confidence: 99%

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Diagnosis, pathophysiology and management of chronic migraine: a proposal of the Belgian Headache Society

Paemeleire

Louis²,

Magis

et al. 2014

Acta Neurol Belg

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“…5,6 Other studies used region-of-interest (ROI) analysis, focusing on pain-related regions such as the periaqueductal gray or amygdala and found increased connectivity in these networks. [7][8][9] Still others have used differences identified with voxel-based morphometry to seed ROI-based connectivity studies. [10][11][12][13] This approach has identified differences between females and males in cortical thickness and connectivity of the posterior insula and precuneus.…”

mentioning

confidence: 99%

The anterior insula shows heightened interictal intrinsic connectivity in migraine without aura

et al. 2015

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Objective: We sought to explore whether patients with migraine show heightened interictal intrinsic connectivity within primary sensory networks, the salience network, and a network anchored by the dorsal pons, a region known to be active during migraine attacks.Methods: Using task-free fMRI and a region-of-interest analysis, we compared intrinsic connectivity patterns in 15 migraineurs without aura to 15 age-and sex-matched healthy controls, focusing on networks anchored by the calcarine cortex, Heschl gyrus, right anterior insula, and dorsal pons, a region active during migraine attacks. We also examined the relationship between network connectivity, migraine frequency, and sensory sensitivity symptoms.Results: Migraineurs showed increased connectivity between primary visual and auditory cortices and the right dorsal anterior insula, between the dorsal pons and the bilateral anterior insulae, and between the right and left ventral anterior insulae. Increased connectivity showed no clinical correlation with migraine frequency or sensory sensitivity. Conclusions:Patients with migraine display interictal changes in the topology of intrinsic connections, with greater connectivity between primary sensory cortices, the pons, and the anterior insula, a region involved in representing and coordinating responses to emotional salience. Migraine is a common, disabling primary headache disorder whose pathophysiology is incompletely understood.1 Migraine attacks often feature an alteration in sensory processing such that normally well-tolerated stimuli become unpleasant, manifesting most frequently as photophobia and phonophobia. These sensory changes may persist between attacks, as migraineurs have lower interictal thresholds for light-and sound-induced discomfort than controls. 2,3Task-free fMRI identifies brain regional ensembles, termed intrinsic connectivity networks (ICNs), 4 that exhibit correlated low-frequency blood oxygen level-dependent signal fluctuations. Previous task-free fMRI studies using independent component analysis revealed altered connectivity of the "executive," "default mode," and "salience" ICNs in migraineurs, although the direction of changes differed between studies. 5,6 Other studies used region-of-interest (ROI) analysis, focusing on pain-related regions such as the periaqueductal gray or amygdala and found increased connectivity in these networks. [7][8][9] Still others have used differences identified with voxel-based morphometry to seed ROI-based connectivity studies. [10][11][12][13] This approach has identified differences between females and males in cortical thickness and connectivity of the posterior insula and precuneus. 12 We studied interictal migraineurs with task-free fMRI to evaluate ICNs relevant to primary sensory processing, nociception, and salience. Given the increased salience of sensory stimuli in migraineurs, we hypothesized that migraineurs would have increased connectivity between the salience network, thought to be involved in identifying homeostatically releva...

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“…Imaging studies provide further evidence that activity within the amygdala contributes to migraine pain. Functional MRI connectivity analysis between the amygdala and cortex in migraine patients identified atypical and increased functional connectivity between these brain regions, which was surprisingly independent of aura, and absent in other chronic pain cohorts and healthy controls [97]. Interestingly, Dehbandi and colleagues [98] reported that synaptic plasticity in the amygdala is induced by CSD propagation, an effect modulated by dopamine D2, but not dopamine D1 receptors.…”

Section: Does the Amygdala Contribute To Migraine Pain?mentioning

confidence: 98%

Migraine and Reward System—Or Is It Aversive?

Cahill¹,

Cook

Pickens

2014

Curr Pain Headache Rep

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Migraine is a debilitating neurological disorder with grave consequences for both the individual and society. This review will focus on recent literature investigating how brain structures implicated in reward and aversion contribute to the genesis of migraine pain. There exist many overlapping and interacting brain regions within pain and reward circuitry that contribute to negative affect and subjective experience of pain. The emotional component of pain has been argued to be a greater metric of quality of life than its sensory component, and thus understanding the processes that influence this pain characteristic is essential to developing novel treatment strategies for mitigating migraine pain. We emphasize and provide evidence that abnormalities within the mesolimbic cortical reward pathways contribute to migraine pain and that there are structural and functional neuroplasticity within the overlapping brain regions common to both pain and reward.

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The missing link: Enhanced functional connectivity between amygdala and visceroceptive cortex in migraine

Cited by 136 publications

References 15 publications

Diagnosis, pathophysiology and management of chronic migraine: a proposal of the Belgian Headache Society

Diagnosis, pathophysiology and management of chronic migraine: a proposal of the Belgian Headache Society

The anterior insula shows heightened interictal intrinsic connectivity in migraine without aura

Migraine and Reward System—Or Is It Aversive?

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