[en] Over the past decade, human brain imaging investigations have reported altered regional cerebral blood flow (rCBF) in the interictal phase of migraine. However, there have been conflicting findings across different investigations, making the use of perfusion imaging in migraine pathophysiology more difficult to define. These inconsistencies may reflect technical constraints with traditional perfusion imaging methods such as single-photon emission computed tomography and positron emission tomography. Comparatively, pseudocontinuous arterial spin labeling (pCASL) is a recently developed magnetic resonance imaging technique that is noninvasive and offers superior spatial resolution and increased sensitivity. Using pCASL, we have previously shown increased rCBF within the primary somatosensory cortex (S1) in adult migraineurs, where blood flow was positively associated with migraine frequency. Whether these observations are present in pediatric and young adult populations remains unknown. This is an important question given the age-related variants of migraine prevalence, symptomology, and treatments. In this investigation, we used pCASL to quantitatively compare and contrast blood flow within S1 in pediatric and young adult migraineurs as compared with healthy controls. In migraine patients, we found significant resting rCBF increases within bilateral S1 as compared with healthy controls. Furthermore, within the right S1, we report a positive correlation between blood flow value with migraine attack frequency and cutaneous allodynia symptom profile. Our results reveal that pediatric and young adult migraineurs exhibit analogous rCBF changes with adult migraineurs, further supporting the possibility that these alterations within S1 are a consequence of repeated migraine attacks. Hum Brain Mapp 38:4078-4087, 2017. (c) 2017 Wiley Periodicals, Inc.
Disciplines :
Life sciences: Multidisciplinary, general & others
Author, co-author :
Youssef, Andrew M.
Ludwick, Allison
Wilcox, Sophie ; Université de Liège - ULiège > Neurosciences-Neuroendocrinology
Lebel, Alyssa
Peng, Ke
Colon, Elisabeth
Danehy, Amy
Burstein, Rami
Becerra, Lino
Borsook, David
Language :
English
Title :
In child and adult migraineurs the somatosensory cortex stands out ... again: An arterial spin labeling investigation.
Publication date :
2017
Journal title :
Human Brain Mapping
ISSN :
1065-9471
eISSN :
1097-0193
Publisher :
John Wiley & Sons, Hoboken, United States - New York
Ashkenazi A, Silberstein S, Jakubowski M, Burstein R (2007): Improved identification of allodynic migraine patients using a questionnaire. Cephalalgia 27:325–329. 2004. The International Classification of Headache Disorders: 2nd edition. Cephalalgia 24 Suppl 1:9–160.
Asllani I, Borogovac A, Brown TR (2008): Regression algorithm correcting for partial volume effects in arterial spin labeling MRI. Magn Reson Med 60:1362–1371.
Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA (2010): Glial and neuronal control of brain blood flow. Nature 468:232–243.
Barmettler G, Brawn J, Maleki N, Scrivani S, Burstein R, Becerra L, Borsook D (2015): A new electronic diary tool for mapping and tracking spatial and temporal head pain patterns in migraine. Cephalalgia 35:417–425.
Bartolini M, Baruffaldi R, Paolino I, Silvestrini M (2005): Cerebral blood flow changes in the different phases of migraine. Funct Neurol 20:209–211.
Bigal ME, Ashina S, Burstein R, Reed ML, Buse D, Serrano D, Lipton RB (2008): Prevalence and characteristics of allodynia in headache sufferers: A population study. Neurology 70:1525–1533.
Bornhövd K, Quante M, Glauche V, Bromm B, Weiller C, Büchel C (2002): Painful stimuli evoke different stimulus–response functions in the amygdala, prefrontal, insula and somatosensory cortex: A single-trial fMRI study. Brain 125:1326–1336.
Burstein R, Yarnitsky D, Goor-Aryeh I, Ransil BJ, Bajwa ZH (2000): An association between migraine and cutaneous allodynia. Ann Neurol 47:614–624.
Chen JJ, Rosas HD, Salat DH (2011): Age-associated reductions in cerebral blood flow are independent from regional atrophy. NeuroImage 55:468–478.
Cheng MH, Wen SL, Zhou HJ, Lian-Fang B, Li JF, Xie LJ (2013): Evaluation of headache and regional cerebral flood flow in patients with migraine. Clin Nucl Med 38:874–877.
Dai W, Garcia D, de Bazelaire C, Alsop DC (2008): Continuous flow-driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields. Magn Reson Med 60:1488–1497.
DaSilva AF, Granziera C, Snyder J, Hadjikhani N (2007a): Thickening in the somatosensory cortex of patients with migraine. Neurology 69:1990–1995.
DaSilva AF, Granziera C, Tuch DS, Snyder J, Vincent M, Hadjikhani N (2007b): Interictal alterations of the trigeminal somatosensory pathway and periaqueductal gray matter in migraine. Neuroreport 18:301–305.
DaSilva AFM, Becerra L, Makris N, Strassman AM, Gonzalez RG, Geatrakis N, Borsook D (2002): Somatotopic activation in the human trigeminal pain pathway. J Neurosci 22:8183–8192.
Datta R, Detre JA, Aguirre GK, Cucchiara B (2011): Absence of changes in cortical thickness in patients with migraine. Cephalalgia 31:1452–1458.
De Benedittis G, Da Passano CF, Granata G, Lorenzetti A, Giuffre R (1999): CBF changes during headache-free periods and spontaneous/induced attacks in migraine with and without aura: A TCD and SPECT comparison study. J Neurosurg Sci 43:141.
Fierstra J, Poublanc J, Han JS, Silver F, Tymianski M, Crawley AP, Fisher JA, Mikulis DJ (2010): Steal physiology is spatially associated with cortical thinning. J Neurol Neurosurg Psychiatry 81:290.
Fjell AM, Westlye LT, Amlien I, Espeseth T, Reinvang I, Raz N, Agartz I, Salat DH, Greve DN, Fischl B, Dale AM, Walhovd KB (2009): High consistency of regional cortical thinning in aging across multiple samples. Cereb Cortex 19:2001–2012.
Friston KJ, Holmes AP, Worsley KJ, Poline JP, Frith CD, Frackowiak RSJ (1994): Statistical parametric maps in functional imaging: A general linear approach. Hum Brain Mapp 2:189–210.
Hänggi J, Langer N, Lutz K, Birrer K, Mérillat S, Jäncke L (2015): Structural brain correlates associated with professional handball playing. PLoS One 10:e0124222.
Herscovitch P, Raichle ME (1985): What is the correct value for the brain–blood partition coefficient for water? J Cereb Blood Flow Metab 5:65–69.
Hodkinson DJ, Krause K, Khawaja N, Renton TF, Huggins JP, Vennart W, Thacker MA, Mehta MA, Zelaya FO, Williams SC, Howard MA (2013): Quantifying the test-retest reliability of cerebral blood flow measurements in a clinical model of on-going post-surgical pain: A study using pseudo-continuous arterial spin labelling. NeuroImage Clin 3:301–310.
Hodkinson DJ, Veggeberg R, Wilcox SL, Scrivani S, Burstein R, Becerra L, Borsook D (2015): Primary somatosensory cortices contain altered patterns of regional cerebral blood flow in the interictal phase of migraine. PLoS One 10:e0137971.
Hodkinson DJ, Wilcox SL, Veggeberg R, Noseda R, Burstein R, Borsook D, Becerra L (2016): Increased amplitude of thalamocortical low-frequency oscillations in patients with migraine. J Neurosci 36:8026–8036.
Hougaard A, Amin FM, Arngrim N, Vlachou M, Larsen VA, Larsson HB, Ashina M (2016): Sensory migraine aura is not associated with structural grey matter abnormalities. NeuroImage Clin 11:322–327.
Hubbard CS, Becerra L, Smith JH, DeLange JM, Smith RM, Black DF, Welker KM, Burstein R, Cutrer FM, Borsook D (2016): Brain changes in responders vs. non-responders in chronic migraine: Markers of disease reversal. Front Hum Neurosci 10:497.
Hutton C, Draganski B, Ashburner J, Weiskopf N (2009): A comparison between voxel-based cortical thickness and voxel-based morphometry in normal aging. NeuroImage 48:371–380.
Huttunen J, Wikstrom H, Salonen O, Ilmoniemi RJ (1999): Human somatosensory cortical activation strengths: Comparison between males and females and age-related changes. Brain Res 818:196–203.
Jakubowski M, Silberstein S, Ashkenazi A, Burstein R (2005): Can allodynic migraine patients be identified interictally using a questionnaire? Neurology 65:1419–1422.
Jin C, Yuan K, Zhao L, Zhao L, Yu D, von Deneen KM, Zhang M, Qin W, Sun W, Tian J (2013): Structural and functional abnormalities in migraine patients without aura. NMR Biomed 26:58–64.
Kassab M, Bakhtar O, Wack D, Bednarczyk E (2009): Resting brain glucose uptake in headache-free migraineurs. Headache 49:90–97.
Kim JH, Kim JB, Suh SI, Seo WK, Oh K, Koh SB (2014): Thickening of the somatosensory cortex in migraine without aura. Cephalalgia 34:1125–1133.
Kim JH, Kim S, Suh SI, Koh SB, Park KW, Oh K (2010): Interictal metabolic changes in episodic migraine: A voxel-based FDG-PET study. Cephalalgia 30:53–61.
Lang E, Kaltenhauser M, Neundorfer B, Seidler S (2004): Hyperexcitability of the primary somatosensory cortex in migraine–a magnetoencephalographic study. Brain 127:2459–2469.
Lipton RB, Bigal ME, Ashina S, Burstein R, Silberstein S, Reed ML, Serrano D, Stewart WF (2008): Cutaneous allodynia in the migraine population. Ann Neurol 63:148–158.
Lorenz J, Minoshima S, Casey KL (2003): Keeping pain out of mind: The role of the dorsolateral prefrontal cortex in pain modulation. Brain 126:1079–1091.
Lu H, Donahue MJ, van Zijl PC (2006): Detrimental effects of BOLD signal in arterial spin labeling fMRI at high field strength. Magn Reson Med 56:546–552.
Macefield VG, Gandevia SC, Henderson LA (2007): Discrete changes in cortical activation during experimentally induced referred muscle pain: A single-trial fMRI study. Cereb Cortex 17:2050–2059.
Maleki N, Becerra L, Brawn J, Bigal M, Burstein R, Borsook D (2012): Concurrent functional and structural cortical alterations in migraine. Cephalalgia 32:607–620.
Moulton EA, Keaser ML, Gullapalli RP, Greenspan JD (2005): Regional intensive and temporal patterns of functional MRI activation distinguishing noxious and innocuous contact heat. J Neurophysiol 93:2183–2193.
O'Reilly RC (2010): The What and How of prefrontal cortical organization. Trends Neurosci 33:355–361.
Prescot A, Becerra L, Pendse G, Tully S, Jensen E, Hargreaves R, Renshaw P, Burstein R, Borsook D (2009): Excitatory neurotransmitters in brain regions in interictal migraine patients. Mol Pain 5:34.
Rocca MA, Ceccarelli A, Falini A, Colombo B, Tortorella P, Bernasconi L, Comi G, Scotti G, Filippi M (2006): Brain gray matter changes in migraine patients with T2-visible lesions. A 3-T MRI study. Stroke 37:1765–1770.
Rocca MA, Messina R, Colombo B, Falini A, Comi G, Filippi M (2014): Structural brain MRI abnormalities in pediatric patients with migraine. J Neurol 261:350–357.
Sandrini G, Rossi P, Milanov I, Serrao M, Cecchini A, Nappi G (2006): Abnormal modulatory influence of diffuse noxious inhibitory controls in migraine and chronic tension-type headache patients. Cephalalgia 26:782–789.
Satterthwaite TD, Shinohara RT, Wolf DH, Hopson RD, Elliott MA, Vandekar SN, Ruparel K, Calkins ME, Roalf DR, Gennatas ED, Jackson C, Erus G, Prabhakaran K, Davatzikos C, Detre JA, Hakonarson H, Gur RC, Gur RE (2014): Impact of puberty on the evolution of cerebral perfusion during adolescence. Proc Natl Acad Sci USA 111:8643–8648.
Schmidt-Wilcke T, Ganssbauer S, Neuner T, Bogdahn U, May A (2008): Subtle grey matter changes between migraine patients and healthy controls. Cephalalgia 28:1–4.
Schwedt TJ, Chong CD, Chiang CC, Baxter L, Schlaggar BL, Dodick DW (2014): Enhanced pain-induced activity of pain-processing regions in a case-control study of episodic migraine. Cephalalgia 34:947–958.
Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004): Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23(Suppl 1):S208–S219.
Sonal Sekhar M, Sasidharan S, Joseph S, Kumar A (2012): Migraine management: How do the adult and paediatric migraines differ? Saudi Pharma J 20:1–7.
Soriani S, Feggi L, Battistella PA, Arnaldi C, De Carlo L, Stipa S (1997): Interictal and ictal phase study with Tc 99m HMPAO brain SPECT in juvenile migraine with aura. Headache 37:31–36.
Stankewitz A, Schulz E, May A (2013): Neuronal correlates of impaired habituation in response to repeated trigemino-nociceptive but not to olfactory input in migraineurs: An fMRI study. Cephalalgia 33:256–265.
Strassman AM, Raymond SA, Burstein R (1996): Sensitization of meningeal sensory neurons and the origin of headaches. Nature 384:560–564.
Thukral BB (2015): Problems and preferences in pediatric imaging. Indian J Radiol Imag 25:359–364.
Timmermann L, Ploner M, Haucke K, Schmitz F, Baltissen R, Schnitzler A (2001): Differential coding of pain intensity in the human primary and secondary somatosensory cortex. J Neurophysiol 86:1499–1503.
Torquati K, Pizzella V, Della Penna S, Franciotti R, Babiloni C, Rossini PM, Romani GL (2002): Comparison between SI and SII responses as a function of stimulus intensity. Neuroreport 13:813–819.
Valfre W, Rainero I, Bergui M, Pinessi L (2008): Voxel-based morphometry reveals gray matter abnormalities in migraine. Headache 48:109–117.
Várkuti B, Cavusoglu M, Kullik A, Schiffler B, Veit R, Yilmaz Ö, Rosenstiel W, Braun C, Uludag K, Birbaumer N, Sitaram R (2011): Quantifying the link between anatomical connectivity, gray matter volume and regional cerebral blood flow: An integrative MRI study. PLoS One 6:e14801.
Wang Z (2012): Improving cerebral blood flow quantification for arterial spin labeled perfusion MRI by removing residual motion artifacts and global signal fluctuations. Magn Reson Imag 30:1409–1415.
Wang Z, Aguirre GK, Rao H, Wang J, Fernandez-Seara MA, Childress AR, Detre JA (2008): Empirical optimization of ASL data analysis using an ASL data processing toolbox: ASLtbx. Magn Reson Imag 26:261–269.
Wu WC, Fernandez-Seara M, Detre JA, Wehrli FW, Wang J (2007): A theoretical and experimental investigation of the tagging efficiency of pseudocontinuous arterial spin labeling. Magn Reson Med 58:1020–1027.
Wu WC, Jain V, Li C, Giannetta M, Hurt H, Wehrli FW, Wang DJ (2010): In vivo venous blood T1 measurement using inversion recovery true-FISP in children and adults. Magn Reson Med 64:1140–1147.
Youssef AM, Macefield VG, Henderson LA (2016): Cortical influences on brainstem circuitry responsible for conditioned pain modulation in humans. Hum Brain Mapp 37:2630–2644.