Top

Published in:

01-09-2012 | Original Communication

Pain processing in patients with migraine: an event-related fMRI study during trigeminal nociceptive stimulation

Authors: Antonio Russo, Alessandro Tessitore, Fabrizio Esposito, Laura Marcuccio, Alfonso Giordano, Renata Conforti, Andrea Truini, Antonella Paccone, Florindo d’Onofrio, Gioacchino Tedeschi

Published in: Journal of Neurology | Issue 9/2012

Abstract

We explored the functional pattern of the pain-processing network in patients with migraine, in the interictal periods, during trigeminal noxious stimulation. Contact heat evoked potential stimulation induced thermal pain and functional magnetic resonance imaging were used to measure whole-brain activation in 16 patients with episodic migraine without aura and 16 age- and gender-matched healthy controls in response to a severe (53°C) noxious, a moderate (51°C) noxious, and a control (41°C) stimulus applied to the maxillary skin. When comparing the fMRI activation over the entire brain, patients with migraine, with respect to healthy controls, showed a significantly greater activation in the perigenual part of anterior cingulate cortex at 51°C and less activation in the bilateral secondary somatosensory cortex at 53°C. A group-by-stimulus interaction analysis revealed a region in the pons showing a divergent response in patients and healthy controls. Correlation analyses demonstrated that the pons activation correlated with higher headache-related disability in patients. Our findings demonstrate increased antinociceptive activity in patients with migraine, which may represent a compensatory reorganization to modulate pain perception at the same intensity of healthy controls.

Kim JH, Kim S, Suh SI et al (2010) Interictal metabolic changes in episodic migraine: a voxel-based FDG-PET study. Cephalalgia 30(1):53–61PubMed

Messlinger K (2009) Migraine: where and how does the pain originate? Exp Brain Res 196(1):179–193PubMedCrossRef

Coppola G, Pierelli F, Schoenen J (2007) Is the cerebral cortex hyperexcitable or hyperresponsive in migraine? Cephalalgia 27(12):1427–1439PubMedCrossRef

Aderjan D, Stankewitz A, May A (2010) Neuronal mechanisms during repetitive trigemino-nociceptive stimulation in migraine patients. Pain 151(1):97–103PubMedCrossRef

Welch KM, Nagesh V, Aurora SK et al (2001) Periaqueductal gray matter dysfunction in migraine: cause or the burden of illness? Headache 41(7):629–637PubMedCrossRef

Aurora SK, Barrodale PM, Tipton RL et al (2007) Brainstem dysfunction in chronic migraine as evidenced by neurophysiological and positron emission tomography studies. Headache 47(7):996–1003 (discussion 1004–1007)PubMedCrossRef

Moulton EA, Burstein R, Tully S et al (2008) Interictal dysfunction of a brainstem descending modulatory center in migraine patients. PLoS One 3(11):e3799PubMedCrossRef

May A, Goadsby PJ (1999) The trigeminovascular system in humans: pathophysiologic implications for primary headache syndromes of the neural influences on the cerebral circulation. J Cereb Blood Flow Metab 19(2):115–127PubMedCrossRef

Borsook D, Burstein R, Becerra L (2004) Functional imaging of the human trigeminal system: opportunities for new insights into pain processing in health and disease. J Neurobiol 61(1):107–125PubMedCrossRef

10.

Kovelowski CJ, Ossipov MH, Sun H et al (2000) Supraspinal cholecystokinin may drive tonic descending facilitation mechanisms to maintain neuropathic pain in the rat. Pain 87(3):265–273PubMedCrossRef

11.

Kim JH, Suh SI, Seol HY et al (2008) Regional grey matter changes in patients with migraine: a voxel-based morphometry study. Cephalalgia 28(6):598–604PubMedCrossRef

12.

Bahra A, Matharu MS, Buchel C et al (2001) Brainstem activation specific to migraine headache. Lancet 357(9261):1016–1017PubMedCrossRef

13.

Weiller C, May A, Limmroth V et al (1995) Brain stem activation in spontaneous human migraine attacks. Nat Med 1(7):658–660PubMedCrossRef

14.

Afridi SK, Giffin NJ, Kaube H et al (2005) A positron emission tomographic study in spontaneous migraine. Arch Neurol 62(8):1270–1275PubMedCrossRef

15.

Afridi SK, Matharu MS, Lee L et al (2005) A PET study exploring the laterality of brainstem activation in migraine using glyceryl trinitrate. Brain 128(Pt 4):932–939PubMedCrossRef

16.

Stankewitz A, Aderjan D, Eippert F et al (2011) Trigeminal nociceptive transmission in migraineurs predicts migraine attacks. J Neurosci 31(6):1937–1943PubMedCrossRef

17.

Roberts K, Papadaki A, Goncalves C et al (2008) Contact heat evoked potentials using simultaneous EEG and fMRI and their correlation with evoked pain. BMC Anesthesiol 8:8PubMedCrossRef

18.

Truini A, Galeotti F, Pennisi E et al (2007) Trigeminal small-fibre function assessed with contact heat evoked potentials in humans. Pain 132(1–2):102–107PubMedCrossRef

19.

Headache Classification Committee of the International Headache Society (2004) The international classification of headache disorders: 2nd edition. Cephalalgia 24(Suppl 1):9–160

20.

Sauro KM, Rose MS, Becker WJ et al (2010) HIT-6 and MIDAS as measures of headache disability in a headache referral population. Headache 50(3):383–395PubMedCrossRef

21.

Bayliss MS, Dewey JE, Dunlap I et al (2003) A study of the feasibility of Internet administration of a computerized health survey: the headache impact test (HIT). Qual Life Res 12(8):953–961PubMedCrossRef

22.

Stankewitz A, Voit HL, Bingel U et al (2010) A new trigemino-nociceptive stimulation model for event-related fMRI. Cephalalgia 30(4):475–485PubMed

23.

Olesen J, Burstein R, Ashina M, Tfelt-Hansen P (2009) Origin of pain in migraine: evidence for peripheral sensitisation. Lancet Neurol 8(7):679–690PubMedCrossRef

24.

Friston KJ, Frith CD, Frackowiak RS et al (1995) Characterizing dynamic brain responses with fMRI: a multivariate approach. Neuroimage 2(2):166–172PubMedCrossRef

25.

Friston KJ, Holmes AP, Poline JB et al (1995) Analysis of fMRI time-series revisited. Neuroimage 2(1):45–53PubMedCrossRef

26.

Forman SD, Cohen JD, Fitzgerald M, Eddy WF et al (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 33(5):636–647PubMedCrossRef

27.

Peyron R, Laurent B, Garcia-Larrea L (2000) Functional imaging of brain responses to pain. A review and meta-analysis. Neurophysiol Clin 30(5):263–288PubMedCrossRef

28.

Brooks J, Tracey I (2005) From nociception to pain perception: imaging the spinal and supraspinal pathways. J Anat 207(1):19–33PubMedCrossRef

29.

Tracey I, Dunckley P (2004) Importance of anti- and pro-nociceptive mechanisms in human disease. Gut 53(11):1553–1555PubMedCrossRef

30.

May A (2006) A review of diagnostic and functional imaging in headache. J Headache Pain 7(4):174–184PubMedCrossRef

31.

Valfre W, Rainero I, Bergui M et al (2008) Voxel-based morphometry reveals gray matter abnormalities in migraine. Headache 48(1):109–117PubMedCrossRef

32.

Seifert F, Maihofner C (2009) Central mechanisms of experimental and chronic neuropathic pain: findings from functional imaging studies. Cell Mol Life Sci 66(3):375–390PubMedCrossRef

33.

Tessitore A, Russo A, Esposito F et al (2011) Interictal cortical reorganization in episodic migraine without aura: an event-related fMRI study during parametric trigeminal nociceptive stimulation. Neurol Sci 32(Suppl 1):S165–S167PubMedCrossRef

34.

Ferraro S, Grazzi L, Mandelli ML et al (2011) Pain processing in medication overuse headache: a functional magnetic resonance imaging (fMRI) study. Pain Med [Epub ahead of print]

35.

Rocca MA, Ceccarelli A, Falini A et al (2006) Brain gray matter changes in migraine patients with T2-visible lesions: a 3-T MRI study. Stroke 37:1765–1770PubMedCrossRef

Title: Pain processing in patients with migraine: an event-related fMRI study during trigeminal nociceptive stimulation
Authors: Antonio Russo
Alessandro Tessitore
Fabrizio Esposito
Laura Marcuccio
Alfonso Giordano
Renata Conforti
Andrea Truini
Antonella Paccone
Florindo d’Onofrio
Gioacchino Tedeschi
Publication date: 01-09-2012
Publisher: Springer-Verlag
Published in: Journal of Neurology / Issue 9/2012
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-012-6438-1

At a glance: The STEP trials

Springer Medicine

Pain processing in patients with migraine: an event-related fMRI study during trigeminal nociceptive stimulation

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 9/2012

Analysis of myelinated fibers in human skin biopsies of patients with neuropathies

Inflammatory demyelinating CNS disorder in a case of X-linked Charcot–Marie–Tooth disease: positive response to natalizumab

Migraine with aura in patients over 50 years of age: the Marseille’s registry

Assessment of dual tasking has no clinical value for fall prediction in Parkinson’s disease

Neuroimaging

Susceptibility to pattern glare following stroke