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      Impaired intrinsic functional connectivity between the thalamus and visual cortex in migraine without aura

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          Abstract

          Background

          Resting-state functional magnetic resonance imaging (fMRI) has confirmed disrupted visual network connectivity in migraine without aura (MwoA). The thalamus plays a pivotal role in a number of pain conditions, including migraine. However, the significance of altered thalamo-visual functional connectivity (FC) in migraine remains unknown. The goal of this study was to explore thalamo-visual FC integrity in patients with MwoA and investigate its clinical significance.

          Methods

          Resting-state fMRI data were acquired from 33 patients with MwoA and 22 well-matched healthy controls. After identifying the visual network by independent component analysis, we compared neural activation in the visual network and thalamo-visual FC and assessed whether these changes were linked to clinical characteristics. We used voxel-based morphometry to determine whether functional differences were dependent on structural differences.

          Results

          The visual network exhibited significant differences in regions (bilateral cunei, right lingual gyrus and left calcarine sulcus) by inter-group comparison. The patients with MwoA showed significantly increased FC between the left thalami and bilateral cunei and between the right thalamus and the contralateral calcarine sulcus and right cuneus. Furthermore, the neural activation of the left calcarine sulcus was positively correlated with visual analogue scale scores ( r = 0.319, p = 0.043), and enhanced FC between the left thalamus and right cuneus in migraine patients was negatively correlated with Generalized Anxiety Disorder scores ( r = − 0.617, p = 0.005).

          Conclusion

          Our data suggest that migraine distress is exacerbated by aberrant feedback projections to the visual network, playing a crucial role in migraine physiological mechanisms. The current study provides further insights into the complex scenario of migraine mechanisms.

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          Most cited references33

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          Migraine pathophysiology: anatomy of the trigeminovascular pathway and associated neurological symptoms, cortical spreading depression, sensitization, and modulation of pain.

          Scientific evidence supports the notion that migraine pathophysiology involves inherited alteration of brain excitability, intracranial arterial dilatation, recurrent activation, and sensitization of the trigeminovascular pathway, and consequential structural and functional changes in genetically susceptible individuals. Evidence of altered brain excitability emerged from clinical and preclinical investigation of sensory auras, ictal and interictal hypersensitivity to visual, auditory, and olfactory stimulation, and reduced activation of descending inhibitory pain pathways. Data supporting the activation and sensitization of the trigeminovascular system include the progressive development of cephalic and whole-body cutaneous allodynia during a migraine attack. In addition, structural and functional alterations include the presence of subcortical white mater lesions, thickening of cortical areas involved in processing sensory information, and cortical neuroplastic changes induced by cortical spreading depression. Here, we review recent anatomical data on the trigeminovascular pathway and its activation by cortical spreading depression, a novel understanding of the neural substrate of migraine-type photophobia, and modulation of the trigeminovascular pathway by the brainstem, hypothalamus and cortex. Copyright © 2013 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved.
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            The pathophysiology of migraine: implications for clinical management

            The understanding of migraine pathophysiology is advancing rapidly. Improved characterisation and diagnosis of its clinical features have led to the view of migraine as a complex, variable disorder of nervous system function rather than simply a vascular headache. Recent studies have provided important new insights into its genetic causes, anatomical and physiological features, and pharmacological mechanisms. The identification of new migraine-associated genes, the visualisation of brain regions that are activated at the earliest stages of a migraine attack, a greater appreciation of the potential role of the cervical nerves, and the recognition of the crucial role for neuropeptides are among the advances that have led to novel targets for migraine therapy. Future management of migraine will have the capacity to tailor treatments based on the distinct mechanisms of migraine that affect individual patients.
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              A neural mechanism for exacerbation of headache by light

              The perception of migraine headache, which is mediated by nociceptive signals transmitted from the cranial dura mater to the brain, is uniquely exacerbated by exposure to light. Here we show that exacerbation of migraine headache by light is prevalent among blind persons who maintain non-image-forming photoregulation in the face of massive rod/cone degeneration. Using single-unit recording and neural tract-tracing in the rat, we identified dura-sensitive neurons in the posterior thalamus, whose activity was distinctly modulated by light, and whose axons projected extensively across layers I through V of somatosensory, visual and associative cortices. The cell bodies and dendrites of such dura/light-sensitive neurons were apposed by axons originating from retinal ganglion cells, predominantly from intrinsically-photosensitive retinal ganglion cells – the principle conduit of non-image-forming photoregulation. We propose that photoregulation of migraine headache is exerted by a non-image-forming retinal pathway that modulates the activity of dura-sensitive thalamocortical neurons.
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                Author and article information

                Contributors
                weihengle0528@163.com
                59360443@qq.com
                chenyuchen1989@126.com
                yayiba2063@163.com
                gxstream@163.com
                896882188@qq.com
                dzhouqingqing@163.com
                123understand@163.com
                y.163yy@163.com
                liry612@126.com
                jnyyfsk@126.com
                Journal
                J Headache Pain
                J Headache Pain
                The Journal of Headache and Pain
                Springer Milan (Milan )
                1129-2369
                1129-2377
                19 December 2019
                19 December 2019
                2019
                : 20
                : 1
                : 116
                Affiliations
                [1 ]ISNI 0000 0000 9255 8984, GRID grid.89957.3a, Department of Radiology, , The Affiliated Jiangning Hospital of Nanjing Medical University, ; No.169, Hushan Road, Nanjing, Jiangsu Province, 211100 China
                [2 ]ISNI 0000 0000 9255 8984, GRID grid.89957.3a, Department of Neurology, , The Affiliated Jiangning Hospital of Nanjing Medical University, ; No.169, Hushan Road, Nanjing, Jiangsu Province, 211100 China
                [3 ]Department of Radiology, Nanjing First Hospital, Nanjing Medical University, Nanjing, Jiangsu Province, 210006 China
                Article
                1065
                10.1186/s10194-019-1065-1
                6924083
                31856703
                4f47ac69-5f3a-4122-ae6f-afb324547729
                © The Author(s). 2019

                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
                : 28 September 2019
                : 3 December 2019
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Anesthesiology & Pain management
                migraine,thalamus,visual network,functional magnetic resonance imaging

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