Advanced visual network and cerebellar hyperresponsiveness to trigeminal nociception in migraine with aura.
Adult
Cerebellum
/ diagnostic imaging
Female
Humans
Magnetic Resonance Imaging
/ methods
Male
Middle Aged
Migraine with Aura
/ diagnostic imaging
Nerve Net
/ diagnostic imaging
Neural Pathways
/ physiopathology
Nociception
/ physiology
Pain
/ diagnostic imaging
Pain Measurement
/ methods
Prospective Studies
Random Allocation
Thalamus
/ diagnostic imaging
Trigeminal Nuclei
/ diagnostic imaging
Visual Cortex
/ diagnostic imaging
Visual Pathways
/ diagnostic imaging
Young Adult
Aura
CHEPS
Cerebellum
Migraine
fMRI
Journal
The journal of headache and pain
ISSN: 1129-2377
Titre abrégé: J Headache Pain
Pays: England
ID NLM: 100940562
Informations de publication
Date de publication:
03 May 2019
03 May 2019
Historique:
received:
05
02
2019
accepted:
18
04
2019
entrez:
5
5
2019
pubmed:
6
5
2019
medline:
19
7
2019
Statut:
epublish
Résumé
Despite the growing body of advanced studies investigating the neuronal correlates of pain processing in patients with migraine without aura (MwoA), only few similar studies have been conducted in patients with migraine with aura (MwA). Therefore, we aimed to explore the functional brain response to trigeminal noxious heat stimulation in patients with MwA. Seventeen patients with MwA and 15 age- and sex-matched healthy controls (HC) underwent whole-brain blood oxygen level-dependent (BOLD) fMRI during trigeminal noxious heat stimulation. To examine the specificity of any observed differences between patients with MwA and HC, the functional response of neural pathways to trigeminal noxious heat stimulation in patients with MwA was compared with 18 patients with MwoA. Secondary analyses investigated the correlations between BOLD signal changes and clinical parameters of migraine severity. We observed a robust cortical and subcortical pattern of BOLD response to trigeminal noxious heat stimulation across all participants. Patients with MwA showed a significantly increased activity in higher cortical areas known to be part of a distributed network involved in advanced visual processing, including lingual gyrus, inferior parietal lobule, inferior frontal gyrus and medial frontal gyrus. Moreover, a significantly greater cerebellar activation was observed in patients with MwA when compared with both patients with MwA and HC. Interestingly, no correlations were found between migraine severity parameters and magnitude of BOLD response in patients with MwA. Our findings, characterized by abnormal visual pathway response to trigeminal noxious heat stimulation, support the role of a functional integration between visual and trigeminal pain networks in the pathophysiological mechanisms underlying migraine with aura. Moreover, they expand the concept of "neurolimbic-pain network" as a model of MwoA including both limbic dysfunction and cortical dys-excitability. Indeed, we suggest a model of "neurolimbic-visual-pain network" in MwA patients, characterized by dysfunctional correlations between pain-modulating circuits not only with the cortical limbic areas but with advanced visual areas as well. Furthermore, the abnormal cerebellar response to trigeminal noxious heat stimulation may suggest a dysfunctional cerebellar inhibitory control on thalamic sensory gating, impinging on the advanced visual processing cortical areas in patients with MwA.
Sections du résumé
BACKGROUND
BACKGROUND
Despite the growing body of advanced studies investigating the neuronal correlates of pain processing in patients with migraine without aura (MwoA), only few similar studies have been conducted in patients with migraine with aura (MwA). Therefore, we aimed to explore the functional brain response to trigeminal noxious heat stimulation in patients with MwA.
METHODS
METHODS
Seventeen patients with MwA and 15 age- and sex-matched healthy controls (HC) underwent whole-brain blood oxygen level-dependent (BOLD) fMRI during trigeminal noxious heat stimulation. To examine the specificity of any observed differences between patients with MwA and HC, the functional response of neural pathways to trigeminal noxious heat stimulation in patients with MwA was compared with 18 patients with MwoA. Secondary analyses investigated the correlations between BOLD signal changes and clinical parameters of migraine severity.
RESULTS
RESULTS
We observed a robust cortical and subcortical pattern of BOLD response to trigeminal noxious heat stimulation across all participants. Patients with MwA showed a significantly increased activity in higher cortical areas known to be part of a distributed network involved in advanced visual processing, including lingual gyrus, inferior parietal lobule, inferior frontal gyrus and medial frontal gyrus. Moreover, a significantly greater cerebellar activation was observed in patients with MwA when compared with both patients with MwA and HC. Interestingly, no correlations were found between migraine severity parameters and magnitude of BOLD response in patients with MwA.
CONCLUSION
CONCLUSIONS
Our findings, characterized by abnormal visual pathway response to trigeminal noxious heat stimulation, support the role of a functional integration between visual and trigeminal pain networks in the pathophysiological mechanisms underlying migraine with aura. Moreover, they expand the concept of "neurolimbic-pain network" as a model of MwoA including both limbic dysfunction and cortical dys-excitability. Indeed, we suggest a model of "neurolimbic-visual-pain network" in MwA patients, characterized by dysfunctional correlations between pain-modulating circuits not only with the cortical limbic areas but with advanced visual areas as well. Furthermore, the abnormal cerebellar response to trigeminal noxious heat stimulation may suggest a dysfunctional cerebellar inhibitory control on thalamic sensory gating, impinging on the advanced visual processing cortical areas in patients with MwA.
Identifiants
pubmed: 31053057
doi: 10.1186/s10194-019-1002-3
pii: 10.1186/s10194-019-1002-3
pmc: PMC6734311
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
46Références
J Neurophysiol. 1999 Jul;82(1):463-71
pubmed: 10400972
Exp Brain Res. 2003 Nov;153(2):146-57
pubmed: 14610633
Neurosci Lett. 2004 May 6;361(1-3):237-40
pubmed: 15135937
J Neurol Neurosurg Psychiatry. 2005 Aug;76(8):1158-60
pubmed: 16024898
Cephalalgia. 2008 Jun;28(6):598-604
pubmed: 18422725
Cerebellum. 2009 Sep;8(3):260-6
pubmed: 19156474
Brain Res Rev. 2010 Oct 5;65(1):14-27
pubmed: 20553761
J Neurol Neurosurg Psychiatry. 2010 Sep;81(9):978-84
pubmed: 20595138
Mol Cell Neurosci. 2011 Jan;46(1):333-9
pubmed: 21040789
Neurology. 2011 Jan 25;76(4):361-5
pubmed: 21263137
Cephalalgia. 2012 Mar;32(4):279-88
pubmed: 22290556
J Neurol. 2012 Sep;259(9):1903-12
pubmed: 22349864
Headache. 2012 Nov-Dec;52(10):1553-65
pubmed: 22757613
Cephalalgia. 2013 Apr;33(6):365-74
pubmed: 23359872
Cephalalgia. 2013 Jun;33(8):526-39
pubmed: 23671250
Cephalalgia. 2013 Jul;33(9):629-808
pubmed: 23771276
Pain. 2013 Dec;154 Suppl 1:S44-53
pubmed: 23891892
Hum Brain Mapp. 2014 Jun;35(6):2714-23
pubmed: 24038870
Pain. 2014 Jul;155(7):1303-12
pubmed: 24721690
Eur J Neurosci. 2015 Jan;41(1):120-8
pubmed: 25327971
Lancet Neurol. 2015 Jan;14(1):81-91
pubmed: 25496899
Cephalalgia. 2015 Oct;35(11):1025-30
pubmed: 25631169
Cephalalgia. 2016 Feb;36(2):139-47
pubmed: 25926619
Headache. 2016 Oct;56(9):1418-1438
pubmed: 26350583
Cephalalgia. 2017 Apr;37(4):305-314
pubmed: 27084886
Neuroimage. 2017 Apr 15;150:112-118
pubmed: 28192274
Hum Brain Mapp. 2017 May;38(5):2635-2642
pubmed: 28240389
Brain. 2017 Jun 1;140(6):1633-1642
pubmed: 28430860
J Cereb Blood Flow Metab. 2019 Apr;39(4):730-739
pubmed: 28737061
Pain Med. 2018 Aug 1;19(8):1657-1666
pubmed: 29016952
Cephalalgia. 2018 Oct;38(11):1782-1791
pubmed: 29357683
Ann Neurol. 1995 Apr;37(4):538-45
pubmed: 7717691
Neuron. 1994 Jul;13(1):1-10
pubmed: 8043270
J Neurosci. 1993 Mar;13(3):1167-77
pubmed: 8382735
Neuroimage. 1995 Mar;2(1):45-53
pubmed: 9343589
Neuropsychologia. 1998 Nov;36(11):1141-59
pubmed: 9842760