Gamma-aminobutyric acid and glutamate/glutamine levels in the dentate nucleus and periaqueductal gray in new daily persistent headache: a magnetic resonance spectroscopy study.
Dentate nucleus
Gamma-aminobutyric acid
Glutamate/glutamine
Magnetic resonance spectroscopy
New daily persistent headache
Periaqueductal gray
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:
29 Aug 2024
29 Aug 2024
Historique:
received:
06
07
2024
accepted:
17
08
2024
medline:
31
8
2024
pubmed:
31
8
2024
entrez:
29
8
2024
Statut:
epublish
Résumé
Magnetic resonance spectroscopy (MRS) studies have indicated that the imbalance between gamma-aminobutyric acid (GABA) and glutamate/glutamine (Glx) levels was the potential cause of migraine development. However, the changes in the GABA and Glx levels in patients with New daily persistent headache (NDPH) remain unclear. This study aimed to investigate the changes in GABA and Glx levels in the periaqueductal gray (PAG) and dentate nucleus (DN) in patients with NDPH using the MEGA-PRESS sequence. Twenty-one NDPH patients and 22 age- and sex-matched healthy controls (HCs) were included and underwent a 3.0T MRI examination, using the MEGA-PRESS sequence to analyze GABA and Glx levels of PAG and DN. The correlations between these neurotransmitter levels and clinical characteristics were also analyzed. There were no significant differences in the GABA+/Water, GABA+/Cr, Glx/Water, and Glx/Cr levels in both PAG and DN between the two groups (all p > 0.05). Moderate-severe NDPH patients had lower levels of Glx/Water (p = 0.034) and Glx/Cr (p = 0.012) in DN than minimal-mild NDPH patients. In patients with NDPH, higher Glx/Water levels in the PAG (r=-0.471, p = 0.031, n = 21) and DN (r=-0.501, p = 0.021, n = 21) and higher Glx/Cr levels in DN (r=-0.483, p = 0.026, n = 21) were found to be correlated with lower Visual Analogue Scale scores. Additionally, a positive correlation was observed between the GABA+/Cr levels in the DN and the Generalized Anxiety Disorder-7 scores (r = 0.519, p = 0.039, n = 16). The results of this study indicated that the GABA and Glx levels in the PAG and DN may not be the primary contributor to the development of NDPH. The correlations between certain clinical scales and the neurotransmitter levels may be derived from the NDPH related symptoms.
Sections du résumé
BACKGROUND
BACKGROUND
Magnetic resonance spectroscopy (MRS) studies have indicated that the imbalance between gamma-aminobutyric acid (GABA) and glutamate/glutamine (Glx) levels was the potential cause of migraine development. However, the changes in the GABA and Glx levels in patients with New daily persistent headache (NDPH) remain unclear. This study aimed to investigate the changes in GABA and Glx levels in the periaqueductal gray (PAG) and dentate nucleus (DN) in patients with NDPH using the MEGA-PRESS sequence.
METHODS
METHODS
Twenty-one NDPH patients and 22 age- and sex-matched healthy controls (HCs) were included and underwent a 3.0T MRI examination, using the MEGA-PRESS sequence to analyze GABA and Glx levels of PAG and DN. The correlations between these neurotransmitter levels and clinical characteristics were also analyzed.
RESULTS
RESULTS
There were no significant differences in the GABA+/Water, GABA+/Cr, Glx/Water, and Glx/Cr levels in both PAG and DN between the two groups (all p > 0.05). Moderate-severe NDPH patients had lower levels of Glx/Water (p = 0.034) and Glx/Cr (p = 0.012) in DN than minimal-mild NDPH patients. In patients with NDPH, higher Glx/Water levels in the PAG (r=-0.471, p = 0.031, n = 21) and DN (r=-0.501, p = 0.021, n = 21) and higher Glx/Cr levels in DN (r=-0.483, p = 0.026, n = 21) were found to be correlated with lower Visual Analogue Scale scores. Additionally, a positive correlation was observed between the GABA+/Cr levels in the DN and the Generalized Anxiety Disorder-7 scores (r = 0.519, p = 0.039, n = 16).
CONCLUSIONS
CONCLUSIONS
The results of this study indicated that the GABA and Glx levels in the PAG and DN may not be the primary contributor to the development of NDPH. The correlations between certain clinical scales and the neurotransmitter levels may be derived from the NDPH related symptoms.
Identifiants
pubmed: 39210271
doi: 10.1186/s10194-024-01845-9
pii: 10.1186/s10194-024-01845-9
doi:
Substances chimiques
Glutamic Acid
3KX376GY7L
Glutamine
0RH81L854J
gamma-Aminobutyric Acid
56-12-2
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
142Subventions
Organisme : National Natural Science Foundation of China
ID : 32170752
Organisme : National Natural Science Foundation of China
ID : 62271061
Organisme : National Natural Science Foundation of Beijing
ID : Z200024
Organisme : Beijing Municipal Natural Science Foundation
ID : L232130
Informations de copyright
© 2024. The Author(s).
Références
Yamani N, Olesen J (2019) New daily persistent headache: a systematic review on an enigmatic disorder. J Headache Pain 20:80. https://doi.org/10.1186/s10194-019-1022-z
doi: 10.1186/s10194-019-1022-z
pubmed: 31307396
pmcid: 6734284
(2018) Headache Classification Committee of the International Headache Society (IHS) The International Classification of Headache Disorders, 3rd edition. Cephalalgia 38:1–211. https://doi.org/10.1177/0333102417738202
Gelfand AA, Robbins MS, Szperka CL (2022) New Daily Persistent Headache—A Start with an Uncertain End. JAMA Neurol 79:733. https://doi.org/10.1001/jamaneurol.2022.1727
doi: 10.1001/jamaneurol.2022.1727
pubmed: 35788252
pmcid: 10084815
Cheema S, Mehta D, Ray JC et al (2023) New daily persistent headache: a systematic review and meta-analysis. Cephalalgia 43:033310242311680. https://doi.org/10.1177/03331024231168089
doi: 10.1177/03331024231168089
Peek AL, Leaver AM, Foster S et al (2021) Increased GABA + in people with migraine, Headache, and Pain Conditions- A potential marker of Pain. J Pain 22:1631–1645. https://doi.org/10.1016/j.jpain.2021.06.005
doi: 10.1016/j.jpain.2021.06.005
pubmed: 34182103
pmcid: 8935361
Wang W, Zhang X, Bai X et al (2022) Gamma-aminobutyric acid and glutamate/glutamine levels in the dentate nucleus and periaqueductal gray with episodic and chronic migraine: a proton magnetic resonance spectroscopy study. J Headache Pain 23:83. https://doi.org/10.1186/s10194-022-01452-6
doi: 10.1186/s10194-022-01452-6
pubmed: 35840907
pmcid: 9287958
Zhang X, Wang W, Bai X et al (2023) Changes in gamma-aminobutyric acid and glutamate/glutamine levels in the right thalamus of patients with episodic and chronic migraine: a proton magnetic resonance spectroscopy study. Headache 63:104–113. https://doi.org/10.1111/head.14449
doi: 10.1111/head.14449
pubmed: 36651572
Bathel A, Schweizer L, Stude P et al (2018) Increased thalamic glutamate/glutamine levels in migraineurs. J Headache Pain 19:55. https://doi.org/10.1186/s10194-018-0885-8
doi: 10.1186/s10194-018-0885-8
pubmed: 30019230
pmcid: 6049847
Mullins PG, McGonigle DJ, O’Gorman RL et al (2014) Current practice in the use of MEGA-PRESS spectroscopy for the detection of GABA. NeuroImage 86:43–52. https://doi.org/10.1016/j.neuroimage.2012.12.004
doi: 10.1016/j.neuroimage.2012.12.004
pubmed: 23246994
Grewal M, Dabas A, Saharan S et al (2016) GABA quantitation using MEGA-PRESS: Regional and hemispheric differences: Regional and Hemispheric GABA levels. J Magn Reson Imaging 44:1619–1623. https://doi.org/10.1002/jmri.25324
doi: 10.1002/jmri.25324
pubmed: 27264205
pmcid: 5512099
Bai X, Edden RAE, Gao F et al (2015) Decreased γ-aminobutyric acid levels in the parietal region of patients with Alzheimer’s disease: in vivo GABA levels measurement in AD. J Magn Reson Imaging 41:1326–1331. https://doi.org/10.1002/jmri.24665
doi: 10.1002/jmri.24665
pubmed: 24863149
Gong T, Xiang Y, Saleh MG et al (2018) Inhibitory motor dysfunction in parkinson’s disease subtypes. Magn Reson Imaging 47:1610–1615. https://doi.org/10.1002/jmri.25865
doi: 10.1002/jmri.25865
Zhang H, Zhu Z, Ma W-X et al (2024) The contribution of periaqueductal gray in the regulation of physiological and pathological behaviors. Front NeuroSci 18:1380171. https://doi.org/10.3389/fnins.2024.1380171
doi: 10.3389/fnins.2024.1380171
pubmed: 38650618
pmcid: 11034386
Sillery E, Bittar RG, Robson MD et al (2005) Connectivity of the human periventricular-periaqueductal gray region. J Neurosurg 103:1030–1034. https://doi.org/10.3171/jns.2005.103.6.1030
doi: 10.3171/jns.2005.103.6.1030
pubmed: 16381189
Cao J, Zhang Y, Li H et al (2021) Different modulation effects of 1 hz and 20 hz transcutaneous auricular vagus nerve stimulation on the functional connectivity of the periaqueductal gray in patients with migraine. J Transl Med 19:354. https://doi.org/10.1186/s12967-021-03024-9
doi: 10.1186/s12967-021-03024-9
pubmed: 34404427
pmcid: 8371886
Bagley EE, Ingram SL (2020) Endogenous opioid peptides in the descending pain modulatory circuit. Neuropharmacology 173:108131. https://doi.org/10.1016/j.neuropharm.2020.108131
doi: 10.1016/j.neuropharm.2020.108131
pubmed: 32422213
pmcid: 7313723
Kros L, Angueyra Aristizábal CA, Khodakhah K (2018) Cerebellar involvement in migraine. Cephalalgia 38:1782–1791. https://doi.org/10.1177/0333102417752120
doi: 10.1177/0333102417752120
pubmed: 29357683
Domínguez C, López A, Ramos-Cabrer P et al (2019) Iron deposition in periaqueductal gray matter as a potential biomarker for chronic migraine. Neurology 92. https://doi.org/10.1212/WNL.0000000000007047
Wang W, Qiu D, Mei Y et al (2024) Altered functional connectivity of brainstem nuclei in new daily persistent headache: evidence from resting-state functional magnetic resonance imaging. CNS Neurosci Ther 30:e14686. https://doi.org/10.1111/cns.14686
doi: 10.1111/cns.14686
pubmed: 38516817
pmcid: 10958407
Szabo E, Chang YC, Shulman J et al (2022) Alterations in the structure and function of the brain in adolescents with new daily persistent headache: a pilot MRI study. Headache 62:858–869. https://doi.org/10.1111/head.14360
doi: 10.1111/head.14360
pubmed: 35861130
Kosinski M, Bayliss MS, Bjorner JB et al A six-item short-form survey for measuring headache impact: The HIT-6ä
Buysse DJ, Reynolds CF, Monk TH et al (1989) The Pittsburgh sleep quality index: a new instrument for psychiatric practice and research. Psychiatry Res 28:193–213. https://doi.org/10.1016/0165-1781(89)90047-4
doi: 10.1016/0165-1781(89)90047-4
pubmed: 2748771
Spitzer RL, Kroenke K, Williams JBW, Löwe B (2006) A brief measure for assessing generalized anxiety disorder: the GAD-7. Arch Intern Med 166:1092. https://doi.org/10.1001/archinte.166.10.1092
doi: 10.1001/archinte.166.10.1092
pubmed: 16717171
Kroenke K, Spitzer RL, Williams JBW (2001) The PHQ-9: validity of a brief depression severity measure. J Gen Intern Med 16:606–613. https://doi.org/10.1046/j.1525-1497.2001.016009606.x
doi: 10.1046/j.1525-1497.2001.016009606.x
pubmed: 11556941
pmcid: 1495268
Sirucek L, Zoelch N, Schweinhardt P (2024) Improving magnetic resonance spectroscopy in the brainstem periaqueductal gray using spectral registration. Magn Reson Med 91:28–38. https://doi.org/10.1002/mrm.29832
doi: 10.1002/mrm.29832
pubmed: 37800387
Edden RAE, Puts NAJ, Harris AD et al (2014) Gannet: a batch-processing tool for the quantitative analysis of gamma‐aminobutyric acid–edited MR spectroscopy spectra. Magn Reson Imaging 40:1445–1452. https://doi.org/10.1002/jmri.24478
doi: 10.1002/jmri.24478
Fu T, Liu L, Huang X et al (2022) Cerebral blood flow alterations in migraine patients with and without aura: an arterial spin labeling study. J Headache Pain 23:131. https://doi.org/10.1186/s10194-022-01501-0
doi: 10.1186/s10194-022-01501-0
pubmed: 36195842
pmcid: 9531478
Affatato O, Rukh G, Schiöth HB, Mwinyi J (2023) Volumetric differences in Cerebellum and Brainstem in patients with migraine: a UK Biobank Study. Biomedicines 11:2528. https://doi.org/10.3390/biomedicines11092528
doi: 10.3390/biomedicines11092528
pubmed: 37760969
pmcid: 10526353
Mehnert J, May A (2019) Functional and structural alterations in the migraine cerebellum. J Cereb Blood Flow Metab 39:730–739. https://doi.org/10.1177/0271678X17722109
doi: 10.1177/0271678X17722109
pubmed: 28737061
Chen Z, Chen X, Liu M et al (2017) Disrupted functional connectivity of periaqueductal gray subregions in episodic migraine. J Headache Pain 18:36. https://doi.org/10.1186/s10194-017-0747-9
doi: 10.1186/s10194-017-0747-9
pubmed: 28321594
pmcid: 5359195
Messina R, Sudre CH, Wei DY et al (2023) Biomarkers of Migraine and Cluster Headache: differences and similarities. Ann Neurol 93:729–742. https://doi.org/10.1002/ana.26583
doi: 10.1002/ana.26583
pubmed: 36565271
Bagnall MW, Zingg B, Sakatos A et al (2009) Glycinergic projection neurons of the Cerebellum. J Neurosci 29:10104–10110. https://doi.org/10.1523/JNEUROSCI.2087-09.2009
doi: 10.1523/JNEUROSCI.2087-09.2009
pubmed: 19675244
pmcid: 3196611
Xie L, Wu H, Chen Q et al (2023) Divergent modulation of pain and anxiety by GABAergic neurons in the ventrolateral periaqueductal gray and dorsal raphe. Neuropsychopharmacol 48:1509–1519. https://doi.org/10.1038/s41386-022-01520-0
doi: 10.1038/s41386-022-01520-0
Ma W, Li L, Kong L et al (2023) Whole-brain monosynaptic inputs to lateral periaqueductal gray glutamatergic neurons in mice. CNS Neurosci Ther cns 14338. https://doi.org/10.1111/cns.14338
Diaz-Mitoma F, Vanast WJ, Tyrrell DLJ (1987) Increased frequency of epstein-barr virus excretion in patients with new daily persistent headaches. Lancet 329:411–415. https://doi.org/10.1016/S0140-6736(87)90119-X
doi: 10.1016/S0140-6736(87)90119-X
Santoni JR, Santoni-Williams CJ (1993) Headache and painful lymphadenopathy in Extracranial or systemic infection: etiology of New Daily Persistant headaches. Intern Med 32:530–532. https://doi.org/10.2169/internalmedicine.32.530
doi: 10.2169/internalmedicine.32.530
pubmed: 8286828
Rozen T, Roth J, Denenberg N (2006) Cervical spine joint hypermobility: a possible predisposing factor for New Daily Persistent Headache. Cephalalgia 26:1182–1185. https://doi.org/10.1111/j.1468-2982.2006.01187.x
doi: 10.1111/j.1468-2982.2006.01187.x
pubmed: 16961783
Rozen TD (2016) New daily persistent headache: a lack of an association with white matter abnormalities on neuroimaging. Cephalalgia 36:987–992. https://doi.org/10.1177/0333102415612766
doi: 10.1177/0333102415612766
pubmed: 26498346
Naegel S, Zeller J, Hougaard A et al (2022) No structural brain alterations in new daily persistent headache – a cross sectional VBM/SBM study. Cephalalgia 42:335–344. https://doi.org/10.1177/03331024211045653
doi: 10.1177/03331024211045653
pubmed: 34601946
Zhang X, Wang W, Zhang X et al (2023) Normal glymphatic system function in patients with new daily persistent headache using diffusion tensor image analysis along the perivascular space. Headache 63:663–671. https://doi.org/10.1111/head.14514
doi: 10.1111/head.14514
pubmed: 37140029
Mei Y, Wang W, Qiu D et al (2023) Micro-structural white matter abnormalities in new daily persistent headache: a DTI study using TBSS analysis. J Headache Pain 24:80. https://doi.org/10.1186/s10194-023-01620-2
doi: 10.1186/s10194-023-01620-2
pubmed: 37394419
pmcid: 10315051
Zhang X, Wang W, Bai X et al (2023) Alterations in regional homogeneity and multiple frequency amplitudes of low-frequency fluctuation in patients with new daily persistent headache: a resting-state functional magnetic resonance imaging study. J Headache Pain 24:14. https://doi.org/10.1186/s10194-023-01543-y
doi: 10.1186/s10194-023-01543-y
pubmed: 36814220
pmcid: 9946707
Qiu D, Wang W, Mei Y et al (2023) Brain structure and cortical activity changes of new daily persistent headache: multimodal evidence from MEG/sMRI. J Headache Pain 24:45. https://doi.org/10.1186/s10194-023-01581-6
doi: 10.1186/s10194-023-01581-6
pubmed: 37098498
pmcid: 10129440
Wang W, Yuan Z, Zhang X et al (2023) Mapping the aberrant brain functional connectivity in new daily persistent headache: a resting-state functional magnetic resonance imaging study. J Headache Pain 24:46. https://doi.org/10.1186/s10194-023-01577-2
doi: 10.1186/s10194-023-01577-2
pubmed: 37098469
pmcid: 10131335
Bai X, Wang W, Zhang X et al (2022) Cerebral perfusion variance in new daily persistent headache and chronic migraine: an arterial spin-labeled MR imaging study. J Headache Pain 23:156. https://doi.org/10.1186/s10194-022-01532-7
doi: 10.1186/s10194-022-01532-7
pubmed: 36482334
pmcid: 9733035
De La González J, Ramos A, Mato-Abad V et al (2013) Higher glutamate to glutamine ratios in Occipital regions in Women with Migraine during the Interictal State. Headache 53:365–375. https://doi.org/10.1111/head.12030
doi: 10.1111/head.12030
Siniatchkin M, Sendacki M, Moeller F et al (2012) Abnormal changes of synaptic excitability in migraine with aura. Cereb Cortex 22:2207–2216. https://doi.org/10.1093/cercor/bhr248
doi: 10.1093/cercor/bhr248
pubmed: 22079926
Zielman R, Wijnen JP, Webb A et al (2017) Cortical glutamate in migraine. Brain 140:1859–1871. https://doi.org/10.1093/brain/awx130
doi: 10.1093/brain/awx130
pubmed: 28633367
Bigal ME, Hetherington H, Pan J et al (2008) Occipital levels of GABA are related to severe headaches in migraine. Neurology 70:2078–2080. https://doi.org/10.1212/01.wnl.0000313376.07248.28
doi: 10.1212/01.wnl.0000313376.07248.28
pubmed: 18505983
Stærmose TG, Knudsen MK, Kasch H, Blicher JU (2019) Cortical GABA in migraine with aura -an ultrashort echo magnetic resonance spectroscopy study. J Headache Pain 20:110. https://doi.org/10.1186/s10194-019-1059-z
doi: 10.1186/s10194-019-1059-z
pubmed: 31795972
pmcid: 6889606
Hamel E, Currents H (2007) Serotonin and migraine: Biology and Clinical implications. Cephalalgia 27:1293–1300. https://doi.org/10.1111/j.1468-2982.2007.01476.x
doi: 10.1111/j.1468-2982.2007.01476.x
pubmed: 17970989
Razeghi Jahromi S, Togha M, Ghorbani Z et al (2019) The association between dietary tryptophan intake and migraine. Neurol Sci 40:2349–2355. https://doi.org/10.1007/s10072-019-03984-3
doi: 10.1007/s10072-019-03984-3
pubmed: 31254181
Sanacora G, Mason GF, Rothman DL, Krystal JH (2002) Increased occipital cortex GABA concentrations in depressed patients after Therapy with selective serotonin reuptake inhibitors. AJP 159:663–665. https://doi.org/10.1176/appi.ajp.159.4.663
doi: 10.1176/appi.ajp.159.4.663
Bhagwagar Z, Wylezinska M, Taylor M et al (2004) Increased brain GABA concentrations following Acute Administration of a selective serotonin reuptake inhibitor. AJP 161:368–370. https://doi.org/10.1176/appi.ajp.161.2.368
doi: 10.1176/appi.ajp.161.2.368
Jacobs GE, Der Grond JV, Teeuwisse WM et al (2010) Hypothalamic glutamate levels following serotonergic stimulation: a pilot study using 7-Tesla magnetic resonance spectroscopy in healthy volunteers. Prog Neuropsychopharmacol Biol Psychiatry 34:486–491. https://doi.org/10.1016/j.pnpbp.2010.01.019
doi: 10.1016/j.pnpbp.2010.01.019
pubmed: 20138102
Jeong H-J, Chenu D, Johnson EE et al (2008) Sumatriptan inhibits synaptic transmission in the Rat Midbrain Periaqueductal Grey. Mol Pain 4. https://doi.org/10.1186/1744-8069-4-54 . 1744-8069-4–54
Taylor NE, Pei J, Zhang J et al (2019) The role of glutamatergic and dopaminergic neurons in the Periaqueductal Gray/Dorsal raphe: separating analgesia and anxiety. https://doi.org/10.1523/ENEURO.0018-18.2019 . eNeuro 6:ENEURO.0018-18.2019
Zhang Y, Huang X, Xin W-J et al (2023) Somatostatin neurons from Periaqueductal Gray to Medulla Facilitate Neuropathic Pain in male mice. J Pain 24:1020–1029. https://doi.org/10.1016/j.jpain.2023.01.002
doi: 10.1016/j.jpain.2023.01.002
pubmed: 36641028
Uniyal R, Paliwal VK, Tripathi A (2017) Psychiatric comorbidity in new daily persistent headache: a cross-sectional study. Eur J Pain 21:1031–1038. https://doi.org/10.1002/ejp.1000
doi: 10.1002/ejp.1000
pubmed: 28146324
Peek AL, Leaver AM, Foster S et al (2021) Increase in ACC GABA + levels correlate with decrease in migraine frequency, intensity and disability over time. J Headache Pain 22:150. https://doi.org/10.1186/s10194-021-01352-1
doi: 10.1186/s10194-021-01352-1
pubmed: 34903165
pmcid: 8903525