Decreased functional connectivity density in pain-related brain regions of female migraine patients without aura

Gao, Qing; Xu, Fei; Jiang, Cui; Chen, Zhifeng; Chen, Huafu; Liao, Huaqiang; Zhao, Ling

doi:10.1016/j.brainres.2015.12.007

Cited by 35 publications

(41 citation statements)

References 57 publications

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“…The NTS is known to send monosynaptic projections to higher brain regions such as the parabrachial nucleus, ventromedial medulla, periaqueductal gray, anterior cingulate and lateral prefrontal cortex [8; 64] - regions hypothesized to support VNS therapeutic effects [81]. Altered connectivity in these pain-processing regions has been noted in interictal migraine patients [25; 29; 55; 67; 79]. Abnormalities in insula connectivity are of particular relevance, given that this region integrates multimodal afference from somatosensory, nociceptive and visceral streams with activity in prefrontal cortex, limbic structures, and olfactory, visual and auditory processing regions [11].…”

Section: Discussionmentioning

confidence: 99%

Modulation of brainstem activity and connectivity by respiratory-gated auricular vagal afferent nerve stimulation in migraine patients

García

Lin

Lee

et al. 2017

Pain

106

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Migraine pathophysiology includes altered brainstem excitability, and recent neuromodulatory approaches aimed at controlling migraine episodes have targeted key brainstem relay and modulatory nuclei. In this study, we evaluated the impact of respiratory-gated auricular vagal afferent nerve stimulation (RAVANS), a novel neuromodulatory intervention based on an existing transcutaneous Vagus Nerve Stimulation approach, in the modulation of brainstem activity and connectivity in migraine patients. We applied 3T-functional magnetic resonance imaging with improved in-plane spatial resolution (2.62×2.62 mm) in episodic migraine (interictal) and age- and sex-matched healthy controls to evaluate brain response to RAVANS (gated to either inhalation or exhalation) and sham stimulation. We further investigated RAVANS modulation of tactile trigeminal sensory afference response in the brainstem using air-puff stimulation directed to the forehead during functional magnetic resonance imaging. Compared to sham and inhalatory-gated RAVANS (iRAVANS), exhalatory-gated RAVANS (eRAVANS) activated an ipsilateral pontomedullary region consistent with nucleus tractus solitarii (NTS). During eRAVANS, NTS connectivity was increased to anterior insula and anterior mid-cingulate cortex, compared to both sham and iRAVANS, in migraine patients. Increased connectivity was inversely correlated with relative time to the next migraine attack, suggesting clinical relevance to this change in connectivity. Post-stimulation effects were also noted immediately following eRAVANS, as we found increased activation in putative pontine serotonergic (i.e. nucleus raphe centralis) and noradrenergic (i.e. locus coeruleus) nuclei in response to trigeminal sensory afference. Regulation of activity and connectivity of brainstem and cortical regions involved in serotonergic and noradrenergic regulation and pain modulation may constitute an underlying mechanism supporting beneficial clinical outcomes for eRAVANS applied for episodic migraine.

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Section: Discussionmentioning

confidence: 99%

Modulation of brainstem activity and connectivity by respiratory-gated auricular vagal afferent nerve stimulation in migraine patients

García

Lin

Lee

et al. 2017

Pain

106

View full text Add to dashboard Cite

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“…Several studies have been performed on the basal ganglia for FC analyses in migraine patients 27, 57 . Atypical FC between the basal ganglia and several brain regions within nociceptive and somatosensory processing pathways was observed; and the findings are possibly associated with impaired pain processing and modulatory processes.…”

Section: Discussionmentioning

confidence: 99%

“…Resting-state functional connectivity (rs-FC) has been used to investigate the pathophysiology of neuropsychiatric disorders, such as Alzheimer’s disease 21 , schizophrenia 22 , and cluster headaches 23 . PAG seed-based rs-FC studies have been performed in interictal migraineurs 24–27 and have suggested that rs-FC may be useful in revealing the pathophysiology of migraine. Despite the important information obtained from imaging studies of migraineurs, no FC study has been reported in animal models of migraine for basic research.…”

Section: Introductionmentioning

confidence: 99%

Disrupted functional connectivity between the periaqueductal gray and other brain regions in a rat model of recurrent headache

Jia

Tang

Zhao

et al. 2017

Sci Rep

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Functional connectivity (FC) has been used to investigate the pathophysiology of migraine. We aimed to identify atypical FC between the periaqueductal gray (PAG) and other brain areas in rats induced by repeated meningeal nociception. The rat model was established by infusing an inflammatory soup (IS) through supradural catheters in conscious rats. Quiescent and face-grooming behaviors were observed to assess nociceptive behavior. FC analysis seeded on the PAG was performed on rats 21 days after IS infusion. The rats exhibited nociceptive behavior correlates of human behaviors associated with migraine after IS infusion. The PAG showed increased FC with the prefrontal cortex, cingulate gyrus, and motor cortex but decreased FC with the basal ganglia, dorsal lateral thalamus, internal capsule and prelimbic cortex in the rat model. The atypical FC of the PAG with brain regions in the rat model that are involved in nociception, somatosensory processing, emotional processing, and pain modulation are consistent with the clinical data from migraineurs, indicate that resting-state FC changes in migraine patients may be a consequence of headache attacks, and further validate this rat model of chronic migraine.

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“…Mounting evidence from structural and functional neuroimaging studies of migraine indicate alterations in a broad network of brain regions associated with pain processing, including several studies that have shown alterations in the hippocampus. [1][2][3][4] However, the relationship between the hippocampus with other brain regions involved in pain processing and the precise role of the hippocampus in the pathophysiology of migraine remain insufficiently understood. One way of interrogating intrinsic brain connectivity is to investigate how brain regions co-vary with one another in size, or in function.…”

mentioning

confidence: 99%

Structural Co‐Variance Patterns in Migraine: A Cross‐Sectional Study Exploring the Role of the Hippocampus

2017

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Objective To interrogate hippocampal morphology and structural co-variance patterns in migraine patients and to investigate whether structural co-variance patterns relate to migraine disease characteristics. Background Migraine is associated with structural alterations in widespread cortical and subcortical regions associated with the sensory, cognitive, and affective components of pain processing. Recent studies have shown that migraine patients have differences in hippocampal structure and function relative to healthy control subjects, but whether hippocampal structure relates to disease characteristics including frequency of attacks, years lived with migraine and symptoms of allodynia remains unknown. Furthermore, this study investigated hippocampal volume co-variance patterns in migraineurs, an indirect measure of brain network connectivity. Here, we explore differences in hippocampal volume and structural co-variance patterns in migraine patients relative to healthy controls and examine whether these hippocampal measures relate to migraine disease burden. Methods This study included 61 migraine patients and 57 healthy control subjects (healthy controls: median age=34.0, IQR=19.0; migraine patients: median age=35.0, IQR=17.5; p=0.65). Regional brain volumes were automatically calculated using FreeSurfer version 5.3. Symptoms of allodynia were determined using the Allodynia Symptom Checklist 12 (ASC-12). Structural covariance patterns were interrogated using pairwise correlations and group differences in correlation strength were estimated using Euclidian distance. A stepwise regression was used to investigate the relationship between structural co-variance patterns with migraine burden. Results Migraine patients had less left hippocampal volume (healthy controls: left hippocampal volume = 4276.8mm3, SD= 425.3mm3, migraine patients: left hippocampal volume= 4089.5mm3, SD= 453.9mm3, p= 0.02) and less total (right plus left) hippocampal volume (healthy controls: total hippocampal volume= 8690.8mm3, SD= 855.1mm3; migraine patients: total hippocampal volume= 8341.8mm3, SD=917.9mm3; p= 0.03) compared to healthy controls. Migraineurs had stronger structural covariance between the hippocampi and cortico-limbic regions in the frontal lobe (inferior opercular gyrus), temporal lobe (planum temporale, amygdala), parietal lobe (angular gyrus, precuneus,) and the cerebellar white matter. Results of a stepwise regression showed that hippocampal volumes and the interactions between hippocampal volumes with the volumes of other cortico-limbic regions associate with migraine-related allodynia but not with headache frequency or years lived with migraine. Conclusion Migraineurs have less hippocampal volume and stronger hippocampal-cortico-limbic connectivity compared to healthy controls. Hippocampal volumes and measures of hippocampal volume connectivity with other cortico-limbic network regions associate with symptoms of allodynia.

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Decreased functional connectivity density in pain-related brain regions of female migraine patients without aura

Cited by 35 publications

References 57 publications

Modulation of brainstem activity and connectivity by respiratory-gated auricular vagal afferent nerve stimulation in migraine patients

Modulation of brainstem activity and connectivity by respiratory-gated auricular vagal afferent nerve stimulation in migraine patients

Disrupted functional connectivity between the periaqueductal gray and other brain regions in a rat model of recurrent headache

Structural Co‐Variance Patterns in Migraine: A Cross‐Sectional Study Exploring the Role of the Hippocampus

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