Brain structural investigation and hippocampal tractography in medication overuse headache: a native space analysis

M Meyer, G Di Scala, M Edde, B Dilharreguy, F Radat, M Allard, S Chanraud, M Meyer, G Di Scala, M Edde, B Dilharreguy, F Radat, M Allard, S Chanraud

Abstract

Background: Spatial normalization of brain images, a prerequisite for voxel based morphometry analysis, may account for the large variability of the volumetric data in medication overuse headache (MOH); possibly because this disease concerns patients differing on both sex and age, and hence with different brain size and shape.

Methods: The present study aimed at providing a subject-based analysis of macrostructure using a native space volumes segmentation (Freesurfer), and microstructure using a region of interest (ROI: i.e. hippocampus) tractography approach in MOH patients.

Results: The results show that MOH patients had decreased volumes of left hemisphere temporal gyri (temporal superior, fusiform) and occipital middle gyrus, together with an increased volume of the left inferior (temporal) lateral ventricle. The left temporal volume was negatively correlated with depression score and medication dependence parameters. Seed-based tractography of the hippocampus revealed a decreased number of reconstructed fibers passing through the left hippocampus.

Conclusion: To our knowledge, these alterations have not been described with methods involving brain normalization, and they indicate that left hemisphere temporal areas, including the hippocampus, may play a role in MOH pathophysiology. Trial registration number NCT00833209. Registered 29 January 2009.

Keywords: Asymmetry; Freesurfer; Hippocampus; Macrostructure; Migraine; Pain.

Figures

Fig. 1
Fig. 1
Example (from a control subject) of hippocampi masks as delimited on T2 scans and realigned on T1
Fig. 2
Fig. 2
Tractography of the hippocampus fibers in one healthy subject (left) and MOH subject (right). Results are overlaid onto 3d view in a oblique plane, b frontal plane and c axial plane. Right side (R) in red and left side (L) in blue
Fig. 3
Fig. 3
Significant relationships between volumetric data and either disease characteristics or neuropsychological data. a Relationship between the left temporal superior gyrus volume and the number of medication taken per month. b Relationship between the left temporal superior gyrus volume and the MDQ-H score. c Relationship between the left temporal superior gyrus volume and the BDI score

References

    1. Tepper SJ. Medication-overuse headache. Contin Minneap Minn. 2012;18:807–822.
    1. Riederer F, Marti M, Luechinger R, Lanzenberger R, von Meyenburg J, Gantenbein AR, et al. Grey matter changes associated with medication-overuse headache: correlations with disease related disability and anxiety. World J Biol Psychiatry. 2012;13:517–525. doi: 10.3109/15622975.2012.665175.
    1. Zheng Z, Xiao Z, Shi X, Ding M, Di W, Qi W, et al. White matter lesions in chronic migraine with medication overuse headache: a cross-sectional MRI study. J Neurol. 2014;261:784–790. doi: 10.1007/s00415-014-7267-1.
    1. Chanraud S, Di Scala G, Dilharreguy B, Schoenen J, Allard M, Radat F. Brain functional connectivity and morphology changes in medication-overuse headache: Clue for dependence-related processes? Cephalalgia. 2014;34:605–615. doi: 10.1177/0333102413519514.
    1. Matharu MS, Good CD, May A, Bahra A, Goadsby PJ. No change in the structure of the brain in migraine: a voxel-based morphometric study. Eur J Neurol. 2003;10:53–57. doi: 10.1046/j.1468-1331.2003.00510.x.
    1. Yassa MA, Stark CEL. A quantitative evaluation of cross-participant registration techniques for MRI studies of the medial temporal lobe. NeuroImage. 2009;44:319–327. doi: 10.1016/j.neuroimage.2008.09.016.
    1. Seibert TM, Brewer JB. Default network correlations analyzed on native surfaces. J Neurosci Methods. 2011;198:301–311. doi: 10.1016/j.jneumeth.2011.04.010.
    1. Beck AT, Beamesderfer A. Assessment of depression: the depression inventory. Mod Probl Pharmacopsychiatry. 1974;7:151–169. doi: 10.1159/000395074.
    1. Sullivan MJL, Bishop SR, Pivik J. The Pain Catastrophizing Scale: development and validation. Psychol Assess. 1995;7:524–532. doi: 10.1037/1040-3590.7.4.524.
    1. Spielberger CD, Gorsuch RL, Lushene RE. Manual for the State-Trait Anxiety Inventory. Palo Alto: Consult. Psychol. Press; 1970.
    1. Patton JH, Stanford MS, Barratt ES. Factor structure of the Barratt impulsiveness scale. J Clin Psychol. 1995;51:768–774. doi: 10.1002/1097-4679(199511)51:6<768::AID-JCLP2270510607>;2-1.
    1. Radat F, Irachabal S, Lafittau M, Creac’h C, Dousset V, Henry P. Construction of a medication dependence questionnaire in headache patients (MDQ-H) validation of the French version. Headache. 2006;46:233–239. doi: 10.1111/j.1526-4610.2006.00331.x.
    1. Bechara A, Damasio AR, Damasio H, Anderson SW. Insensitivity to future consequences following damage to human prefrontal cortex. Cognition. 1994;50:7–15. doi: 10.1016/0010-0277(94)90018-3.
    1. Fischl B, van der Kouwe A, Destrieux C, Halgren E, Ségonne F, Salat DH, et al. Automatically parcellating the human cerebral cortex. Cereb Cortex. 1991;2004(14):11–22.
    1. Destrieux C, Fischl B, Dale A, Halgren E. Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. NeuroImage. 2010;53:1–15. doi: 10.1016/j.neuroimage.2010.06.010.
    1. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 2002;33:341–355. doi: 10.1016/S0896-6273(02)00569-X.
    1. Duvernoy H, Cabanis E, Vannson J. The human brain: surface, three-dimensional sectional anatomy and MRI. Vienna: Springer; 1991.
    1. Wisse LEM, Biessels GJ, Geerlings MI. A critical appraisal of the hippocampal subfield segmentation package in FreeSurfer. Front Aging Neurosci. 2014;6:261. doi: 10.3389/fnagi.2014.00261.
    1. Perrin M, Poupon C, Rieul B, Leroux P, Constantinesco A, Mangin J-F, et al. Validation of q-ball imaging with a diffusion fibre-crossing phantom on a clinical scanner. Philos Trans R Soc Lond B Biol Sci. 2005;360:881–891. doi: 10.1098/rstb.2005.1650.
    1. Lazar M, Weinstein DM, Tsuruda JS, Hasan KM, Arfanakis K, Meyerand ME, et al. White matter tractography using diffusion tensor deflection. Hum Brain Mapp. 2003;18:306–321. doi: 10.1002/hbm.10102.
    1. Chamberland M, Whittingstall K, Fortin D, Mathieu D, Descoteaux M. Real-time multi-peak tractography for instantaneous connectivity display. Front Neuroinform. 2014;8:59. doi: 10.3389/fninf.2014.00059.
    1. Chanraud S, Martelli C, Delain F, Kostogianni N, Douaud G, Aubin H-J, et al. Brain morphometry and cognitive performance in detoxified alcohol-dependents with preserved psychosocial functioning. Neuropsychopharmacology. 2007;32:429–438. doi: 10.1038/sj.npp.1301219.
    1. He Y, Chen ZJ, Evans AC. Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb Cortex. 1991;2007(17):2407–2419.
    1. Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A. Neuroplasticity: changes in grey matter induced by training. Nature. 2004;427:311–312. doi: 10.1038/427311a.
    1. Hogstrom LJ, Westlye LT, Walhovd KB, Fjell AM. The structure of the cerebral cortex across adult life: age-related patterns of surface area, thickness, and gyrification. Cereb Cortex. 1991;2013(23):2521–2530.
    1. Rodriguez-Raecke R, Niemeier A, Ihle K, Ruether W, May A. Brain gray matter decrease in chronic pain is the consequence and not the cause of pain. J Neurosci. 2009;29:13746–13750. doi: 10.1523/JNEUROSCI.3687-09.2009.
    1. May A. Chronic pain may change the structure of the brain. Pain. 2008;137:7–15. doi: 10.1016/j.pain.2008.02.034.
    1. Schmidt-Wilcke T, Leinisch E, Straube A, Kämpfe N, Draganski B, Diener HC, et al. Gray matter decrease in patients with chronic tension type headache. Neurology. 2005;65:1483–1486. doi: 10.1212/01.wnl.0000183067.94400.80.
    1. Kim JH, Suh S-I, Seol HY, Oh K, Seo W-K, Yu S-W, et al. Regional grey matter changes in patients with migraine: a voxel-based morphometry study. Cephalalgia. 2008;28:598–604. doi: 10.1111/j.1468-2982.2008.01550.x.
    1. Syal S, Hattingh CJ, Fouché J-P, Spottiswoode B, Carey PD, Lochner C, et al. Grey matter abnormalities in social anxiety disorder: a pilot study. Metab Brain Dis. 2012;27:299–309. doi: 10.1007/s11011-012-9299-5.
    1. Tu P-C, Chen L-F, Hsieh J-C, Bai Y-M, Li C-T, Su T-P. Regional cortical thinning in patients with major depressive disorder: a surface-based morphometry study. Psychiatry Res. 2012;202:206–213. doi: 10.1016/j.pscychresns.2011.07.011.
    1. Kaag AM, Crunelle CL, van Wingen G, Homberg J, van den Brink W, Reneman L. Relationship between trait impulsivity and cortical volume, thickness and surface area in male cocaine users and non-drug using controls. Drug Alcohol Depend. 2014;144:210–217. doi: 10.1016/j.drugalcdep.2014.09.016.
    1. Förstl H, Zerfass R, Geiger-Kabisch C, Sattel H, Besthorn C, Hentschel F. Brain atrophy in normal ageing and Alzheimer’s disease: volumetric discrimination and clinical correlations. Br J Psychiatry. 1995;167:739–746. doi: 10.1192/bjp.167.6.739.
    1. Apostolova LG, Green AE, Babakchanian S, Hwang KS, Chou Y-Y, Toga AW, et al. Hippocampal atrophy and ventricular enlargement in normal aging, mild cognitive impairment and Alzheimer’s disease. Alzheimer Dis Assoc Disord. 2012;26:17–27. doi: 10.1097/WAD.0b013e3182163b62.
    1. Hu W, Guo J, Chen N, Guo J, He L. A meta-analysis of voxel-based morphometric studies on migraine. Int J Clin Exp Med. 2015;8:4311–4319.
    1. Neeb L, Bastian K, Villringer K, Gits HC, Israel H, Reuter U, et al. No microstructural white matter alterations in chronic and episodic migraineurs: a case–control diffusion tensor magnetic resonance imaging study. Headache. 2015;55:241–251. doi: 10.1111/head.12496.
    1. Chong CD, Schwedt TJ. Migraine affects white-matter tract integrity: a diffusion-tensor imaging study. Cephalalgia. 2015;35:1162–1171. doi: 10.1177/0333102415573513.
    1. Fischl B, Rajendran N, Busa E, Augustinack J, Hinds O, Yeo BTT, et al. Cortical folding patterns and predicting cytoarchitecture. Cereb Cortex. 1991;2008(18):1973–1980.
    1. Seibert TM, Majid DSA, Aron AR, Corey-Bloom J, Brewer JB. Stability of resting fMRI interregional correlations analyzed in subject-native space: a one-year longitudinal study in healthy adults and premanifest Huntington’s disease. NeuroImage. 2012;59:2452–2463. doi: 10.1016/j.neuroimage.2011.08.105.

Source: PubMed

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