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Clinical neuroscience 257 Altered resting-state ascending/descending pathways associated with the posterior thalamus in migraine without aura Ting Wanga,b, Wang Zhane, Qin Chenc, Ning Chenc, Junpeng Zhanga, Qi Liua, Li Hec, Junran Zhanga,b, Hua Huanga and Qiyong Gongd This study aimed to investigate the dysfunctional thalamus and these cortical regions indicate a disrupted ascending/descending pain pathways at the thalamic level pain modulation in affective and sensory domains, which in patients with migraine without aura (MWoA) using the suggests a disequilibrium of pain inhibition and facilitation effective connectivity analysis of the resting-state functional in MWoA. These findings may help to shed light on the MRI. Twenty MWoA and 25 matched healthy controls pathophysiologic mechanisms of migraine. NeuroReport participated in the resting-state functional MRI scans. The 27:257–263 Copyright © 2016 Wolters Kluwer Health, Inc. directional interactions between the posterior thalamus All rights reserved. (PTH) and other brain regions were investigated using the NeuroReport 2016, 27:257–263 Granger causality analysis and choosing bilateral PTH as two individual seeds. Pearson’s correlation analysis was Keywords: effective connectivity, Granger causality analysis, migraine, posterior thalamus, resting-state functional magnetic resonance imaging carried out between the abnormal effective connectivity and the headache duration and pain intensity of MWoA. aDepartment of Medical Information Engineering, School of Electrical Engineering and Information, Sichuan University, bDepartment of Radiology, Huaxi MR Compared with healthy controls, MWoA showed decreased Research Center (HMRRC), cDepartment of Neurology, West China Hospital of inflows to the bilateral PTH from the ventromedial prefrontal Sichuan University, dDepartment of Psychology, School of Public Administration, Sichuan University, Chengdu, People’s Republic of China and eNeuroimaging cortex and the left precuneus/posterior cingulate cortex, Center, University of Maryland, College Park, Maryland decreased outflow from the left PTH to the ipsilateral Correspondence to Junran Zhang, PhD, Department of Medical Information dorsomedial prefrontal cortex, and increased inflow to the Engineering, School of Electrical Engineering and Information, Sichuan University, right PTH from the ipsilateral dorsolateral prefrontal cortex. No. 24, South Section One, First Ring Road, Chengdu 610065, People’s Republic of China In addition, the abnormal inflows to the right PTH from the Tel: + 86 028 8540 5614; fax: + 86 028 8542 3503; ventromedial prefrontal cortex and the right dorsolateral e-mail: [email protected] prefrontal cortex correlated positively with the headache Received 7 December 2015 accepted 5 January 2016 duration and pain intensity, respectively. The abnormal ascending/descending pain pathways between the Introduction brain regions consistently activated by pain stimulation Migraine is a disabling neurological condition that man- [3,4]. ifests with attacks of headache, hypersensitivities to visual, auditory, olfactory, and somatosensory stimuli, In addition to a general activation of the trigeminal neu- nausea, and vomiting [1]. It affects about 12% of the rons in the thalamic nuclei in functional imaging studies of general population and causes substantial personal and migraine, a major network of trigeminovascular-sensitive social burden [2]. With the help of neuroimaging tech- neurons from the thalamus to widespread regions of the nology, our perception of migraine has transformed from cortex has also been identified [5]. The thalamus is a relay a vascular into a neurovascular and, most recently, into a region subserving both sensory and motor processing, with central nervous system disorder [3]. As such, many neu- nerve fibers not only projecting out to the cerebral cortex roimaging studies in migraine have documented struc- in all directions but also receiving feedback information tural and functional alterations in a variety of cortical from these multiple cortical areas [6]. These functionally (such as occipital, parietal, and temporal lobes, cingulate distinct and anatomically remote cortical areas that the cortex, prefrontal cortex, and insula) and subcortical (such thalamus projects to are involved in the processing of as thalamus, amygdala, hippocampus, basal ganglia, and sensory, cognitive, and affective information arising from brainstem) pain-processing regions. These areas are often the body [7]. Therefore, such a thalamocortical network referred to as being part of the ‘pain matrix’, a group of may play a role in the ascending and descending pain pathways responding for the transmission and modulation This is an open-access article distributed under the terms of the Creative of nociceptive signals, and explains some of the common Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC- ND), where it is permissible to download and share the work provided it is properly disturbances in neurological functions during migraine. cited. The work cannot be changed in any way or used commercially. However, how the thalamus affects these brain systems 0959-4965 Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved. DOI: 10.1097/WNR.0000000000000529 258 NeuroReport 2016, Vol 27 No 4 and whether it is affected by these brain regions in Participants had not had a migraine attack at least 72 h migraine are poorly understood. before scanning. In addition, patients were excluded if they had a migraine precipitated during the 2-day follow- Resting-state effective connectivity and functional con- up. Potential participants were excluded if they had any nectivity are two effective techniques to address the contraindication to MRI, had a previous brain injury, had integration of functionally specialized areas in human a neurologic disorder other than migraine, had a psy- brain. Both two methods allow the inference of com- chiatric disorder other than anxiety or depression, or if munication between spatially remote brain regions, they had any acute or chronic pain disorder other than whereas effective connectivity additionally allows infer- migraine. ring about the directionality of information transfer within functionally connected networks, utilizing infor- All patients were interviewed to determine the demo- mation on time-lagged relationships between brain graphic features (e.g. age, sex, and education). Additional regions [8]. Some resting-state functional connectivity information including the migraine history [e.g. onset studies in migraine have so far been documented by age, frequency and duration of attacks, and pain intensity choosing pain matrix regions such as periaqueductal gray, (evaluated using the visual analogue scale)] and the nucleus cuneiformis, and the affective regions (including impact of headache (evaluated with the Migraine the insula, anterior cingulate cortex, and amygdala) as Disability Assessment Scale and six-item Headache regions of interest (ROIs) (i.e. seeds), and abnormal Impact Test) was collected in participants with migraine functional connectivities between these seeds and tha- by two experienced neurologists. The Allodynia lamus have been found [9,10]. To date, little is known Symptom Checklist-12 (ASC-12) scale was administered about whether these reported abnormal functional con- to estimate the prevalence and severity of cutaneous nectivities are involved in the pain modulation during the allodynia in the migraine population. The yielding score migraine process. Therefore, studying the directed of each participant was placed into one of the four cate- influence (effective connectivity) of the thalamus with gories: 0–2 = no allodynia; 3–5 = mild allodynia; the other structures can strengthen our understanding of 6–8 = moderate allodynia; 9 or more = severe allodynia. the physiopathologic mechanism in migraine. For all participants, psychiatric assessments including the use of 24-item Hamilton Depression Scale (24-HAMD) In the present study, we sought to investigate the and 14-item Hamilton Anxiety Scale (14-HAMA) were effective connectivity patterns of the bilateral thalamus also performed to assess depression and anxiety state. with the rest of the brain in migraine using resting-state Demographic and clinical features between MWoA and functional MRI (rs-fMRI). Granger causality analysis HC were determined using an independent-sample t-test (GCA) is a special approach to explore such effective or the χ2-test, as appropriate. connectivity among regions, can drive the deductive network on the basis of a certain hypothetical seed Data acquisition and spatial processing region, and requires no previous knowledge [11]. We The experiment was conducted on a 3.0-T scanner (Trio construct an effective connectivity network associated Tim; Siemens, Erlangen, Germany) using a 16-channel with the thalamus using the GCA method on rs-fMRI birdcage head coil and tightly padded clamps were used data to test the hypothesis that abnormal ascending/ to minimize head motion. A routine T1-weighted ima- descending pathways at the thalamic level exist in ging was first obtained and then the rs-fMRI was migraine and are involved in the physiopathologic obtained using an echo-planar imaging sequence with the mechanism of migraine. following protocols: voxel size: 3.75 × 3.75 × 5mm3, TR: × 2 Participants and methods 2000 ms, TE: 30 ms, FOV: 240 240 mm , matrix: 64 × 64, and slice thickness: 5 mm with no gap. Participants Throughout
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