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Alterations of thalamic nuclei volumes in patients with cluster headache

  • Functional Neuroradiology
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Abstract

Purpose

This study aimed to compare the alterations of thalamic nuclei volumes and the intrinsic thalamic network in patients with cluster headache and healthy controls.

Methods

We retrospectively enrolled 24 patients with episodic cluster headache and 24 healthy controls. We calculated the thalamic nuclei volumes in the patients with cluster headache and healthy controls based on three-dimensional T1-weighted imaging with automated segmentation using the FreeSurfer program. We also investigated the intrinsic thalamic network using structural co-variance analysis based on the thalamic nuclei volumes and graph theory under the BRAPH program. We compared the thalamic nuclei volumes and intrinsic thalamic networks in patients with cluster headaches and healthy controls.

Results

The right and left whole thalamic volumes did not differ in the patients with cluster headaches and healthy controls (0.4199 vs. 0.4069%, p = 0.2008; 0.4386 vs. 0.4273%, p = 0.3437; respectively). However, there were significant alterations of right and left medial geniculate nuclei volumes in the patients with cluster headaches and the healthy controls. The right and left medial geniculate nuclei volumes of the patients with cluster headaches were greater than those of the healthy controls (0.0088 vs. 0.0075%, p < 0.0001; 0.0086 vs. 0.0072%, p < 0.0001; respectively). The intrinsic thalamic networks of the groups were not different.

Conclusion

This study demonstrates significant alterations in the bilateral medial geniculate nuclei volumes in patients with cluster headache compared to healthy controls. These alterations may be related to the pathophysiology of cluster headache. However, there are no changes in the intrinsic thalamic network in patients with cluster headache.

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Availability of data and material

The data in this study are available from the corresponding author upon reasonable request.

References

  1. May A, Schwedt TJ, Magis D, Pozo-Rosich P, Evers S, Wang S-J (2018) Cluster headache. Nat Rev Dis Prim 4(1):1–17

    Google Scholar 

  2. Chung PW, Kim BS, Park JW, Sohn JH, Lee MJ, Kim BK, Chu MK, Ahn JY, Choi YJ, Song TJ, Bae DW, Kim D, Kim JM, Kim SK, Park KY, Chung JM, Moon HS, Oh K, Chung CS, Cho SJ (2021) Smoking history and clinical features of cluster headache: results from the Korean Cluster Headache Registry. J Clin Neurol 17(2):229–235. https://doi.org/10.3988/jcn.2021.17.2.229

    Article  PubMed  PubMed Central  Google Scholar 

  3. Arnold M (2018) Headache classification committee of the international headache society (IHS) the international classification of headache disorders. Cephalalgia 38(1):1–211

    Article  Google Scholar 

  4. Hoffmann J, May A (2018) Diagnosis, pathophysiology, and management of cluster headache. The Lancet Neurol 17(1):75–83

    Article  Google Scholar 

  5. May A, Bahra A, Büchel C, Frackowiak RS, Goadsby PJ (1998) Hypothalamic activation in cluster headache attacks. The Lancet 352(9124):275–278

    Article  CAS  Google Scholar 

  6. Chou K-H, Yang F-C, Fuh J-L, Kuo C-Y, Wang Y-H, Lirng J-F, Lin Y-Y, Wang S-J, Lin C-P (2017) Bout-associated intrinsic functional network changes in cluster headache: a longitudinal resting-state functional MRI study. Cephalalgia 37(12):1152–1163

    Article  Google Scholar 

  7. Pringsheim T (2002) Cluster headache: evidence for a disorder of circadian rhythm and hypothalamic function. Can J Neurol Sci 29(1):33–40

    Article  Google Scholar 

  8. Leone M, Bussone G (1993) A review of hormonal findings in cluster headache. Evidence for hypothalamic involvement Cephalalgia 13(5):309–317

    Article  CAS  Google Scholar 

  9. Schulte LH, May A (2016) The migraine generator revisited: continuous scanning of the migraine cycle over 30 days and three spontaneous attacks. Brain 139(7):1987–1993

    Article  Google Scholar 

  10. Lund N, Barloese M, Petersen A, Haddock B, Jensen R (2017) Chronobiology differs between men and women with cluster headache, clinical phenotype does not. Neurol 88(11):1069–1076

    Article  Google Scholar 

  11. Yang F-C, Chou K-H, Kuo C-Y, Lin Y-Y, Lin C-P, Wang S-J (2018) The pathophysiology of episodic cluster headache: insights from recent neuroimaging research. Cephalalgia 38(5):970–983

    Article  Google Scholar 

  12. Yang F-C, Chou K-H, Fuh J-L, Lee P-L, Lirng J-F, Lin Y-Y, Lin C-P, Wang S-J (2015) Altered hypothalamic functional connectivity in cluster headache: a longitudinal resting-state functional MRI study. J Neurol Neurosurg Psychiatry 86(4):437–445

    Article  Google Scholar 

  13. Absinta M, Rocca MA, Colombo B, Falini A, Comi G, Filippi M (2012) Selective decreased grey matter volume of the pain-matrix network in cluster headache. Cephalalgia 32(2):109–115

    Article  Google Scholar 

  14. Szabó N, Kincses ZT, Párdutz Á, Tóth E, Szok D, Csete G, Vécsei L (2013) White matter disintegration in cluster headache. J Headache Pain 14(1):1–6

    Article  Google Scholar 

  15. Qiu E, Wang Y, Ma L, Tian L, Liu R, Dong Z, Xu X, Zou Z, Yu S (2013) Abnormal brain functional connectivity of the hypothalamus in cluster headaches. PLoS One 8(2):e57896

    Article  CAS  Google Scholar 

  16. Teepker M, Menzler K, Belke M, Heverhagen JT, Voelker M, Mylius V, Oertel WH, Rosenow F, Knake S (2012) Diffusion tensor imaging in episodic cluster headache. Headache: The Journal of Head and Face Pain. 52(2):274–282

    Article  Google Scholar 

  17. Sprenger T, Ruether K, Boecker H, Valet M, Berthele A, Pfaffenrath V, Wöller A, Tölle T (2007) Altered metabolism in frontal brain circuits in cluster headache. Cephalalgia 27(9):1033–1042

    Article  CAS  Google Scholar 

  18. Ferraro S, Nigri A, Demichelis G, Pinardi C, Chiapparini L, Giani L, Proietti Cecchini A, Leone M (2020) Understanding cluster headache using magnetic resonance imaging. Front Neurol 11:535

    Article  Google Scholar 

  19. Kuner R, Kuner T (2021) Cellular circuits in the brain and their modulation in acute and chronic pain. Physiol Rev 101(1):213–258

    Article  CAS  Google Scholar 

  20. Apkarian AV, Bushnell MC, Treede R-D, Zubieta J-K (2005) Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 9(4):463–484

    Article  Google Scholar 

  21. Ab Aziz CB, Ahmad AH (2006) The role of the thalamus in modulating pain. The Malaysian journal of medical sciences: MJMS 13(2):11

    PubMed  PubMed Central  Google Scholar 

  22. Shin KJ, Lee HJ, Park KM (2019) Alterations of individual thalamic nuclei volumes in patients with migraine. J Headache Pain 20(1):112. https://doi.org/10.1186/s10194-019-1063-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Shin KJ, Lee H-J, Park KM (2019) Alterations of individual thalamic nuclei volumes in patients with migraine. J Headache Pain 20(1):1–8

    Article  Google Scholar 

  24. Mijalkov M, Kakaei E, Pereira JB, Westman E, Volpe G, Alzheimer’s Disease Neuroimaging I (2017) BRAPH: a graph theory software for the analysis of brain connectivity. PLoS ONE 12(8):e0178798. https://doi.org/10.1371/journal.pone.0178798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Farahani FV, Karwowski W, Lighthall NR (2019) Application of graph theory for identifying connectivity patterns in human brain networks: a systematic review. Front Neurosci 13:585. https://doi.org/10.3389/fnins.2019.00585

    Article  PubMed  PubMed Central  Google Scholar 

  26. Park KM, Lee BI, Shin KJ, Ha SY, Park J, Kim SE, Kim SE (2019) Pivotal role of subcortical structures as a network hub in focal epilepsy: evidence from graph theoretical analysis based on diffusion-tensor imaging. J Clin Neurol 15(1):68–76. https://doi.org/10.3988/jcn.2019.15.1.68

    Article  PubMed  Google Scholar 

  27. Holland PR, Goadsby PJ (2009) Cluster headache, hypothalamus, and orexin. Curr Pain Headache Rep 13(2):147–154

    Article  Google Scholar 

  28. Rocca MA, Valsasina P, Absinta M, Colombo B, Barcella V, Falini A, Comi G, Filippi M (2010) Central nervous system dysregulation extends beyond the pain-matrix network in cluster headache. Cephalalgia 30(11):1383–1391

    Article  Google Scholar 

  29. Yang F-C, Chou K-H, Fuh J-L, Huang C-C, Lirng J-F, Lin Y-Y, Lin C-P, Wang S-J (2013) Altered gray matter volume in the frontal pain modulation network in patients with cluster headache. PAIN® 154(6):801–807

    Article  Google Scholar 

  30. Kiraly A, Szabo N, Pardutz A, Toth E, Tajti J, Csete G, Farago P, Bodnar P, Szok D, Tuka B, Palinkas E, Ertsey C, Vecsei L, Kincses ZT (2018) Macro- and microstructural alterations of the subcortical structures in episodic cluster headache. Cephalalgia 38(4):662–673. https://doi.org/10.1177/0333102417703762

    Article  PubMed  Google Scholar 

  31. Sherman SM (2016) Thalamus plays a central role in ongoing cortical functioning. Nat Neurosci 19(4):533–541

    Article  CAS  Google Scholar 

  32. Sherman SM, Guillery R (2011) Distinct functions for direct and transthalamic corticocortical connections. J Neurophysiol 106(3):1068–1077

    Article  Google Scholar 

  33. Moisset X, Bouhassira D (2007) Brain imaging of neuropathic pain. Neuroimage 37:S80–S88

    Article  Google Scholar 

  34. Gustin SM, Peck CC, Wilcox SL, Nash PG, Murray GM, Henderson LA (2011) Different pain, different brain: thalamic anatomy in neuropathic and non-neuropathic chronic pain syndromes. J Neurosci 31(16):5956–5964

    Article  CAS  Google Scholar 

  35. Sandrini G, Antonaci F, Lanfranchi S, Milanov I, Danilov A, Nappi G (2000) Asymmetrical reduction of the nociceptive flexion reflex threshold in cluster headache. Cephalalgia 20(7):647–652

    Article  CAS  Google Scholar 

  36. May A, Bahra A, Büchel C, Frackowiak R, Goadsby P (2000) PET and MRA findings in cluster headache and MRA in experimental pain. Neurology 55(9):1328–1335

    Article  CAS  Google Scholar 

  37. Lee CC (2013) Thalamic and cortical pathways supporting auditory processing. Brain Lang 126(1):22–28

    Article  Google Scholar 

  38. Weinberger NM (2011) The medial geniculate, not the amygdala, as the root of auditory fear conditioning. Hear Res 274(1–2):61–74

    Article  Google Scholar 

  39. Aizenberg M, Rolón-Martínez S, Pham T, Rao W, Haas JS, Geffen MN (2019) Projection from the amygdala to the thalamic reticular nucleus amplifies cortical sound responses. Cell reports 28(3):605-615. e604

    Article  CAS  Google Scholar 

  40. Donishi T, Kimura A, Imbe H, Yokoi I, Kaneoke Y (2011) Sub-threshold cross-modal sensory interaction in the thalamus: lemniscal auditory response in the medial geniculate nucleus is modulated by somatosensory stimulation. Neuroscience 174:200–215. https://doi.org/10.1016/j.neuroscience.2010.11.041

    Article  CAS  PubMed  Google Scholar 

  41. Farahani FV, Karwowski W, Lighthall NR (2019) Application of graph theory for identifying connectivity patterns in human brain networks: a systematic review. Frontiers in Neuroscience 13:585

    Article  Google Scholar 

  42. Ha SY, Park KM (2019) Alterations of structural connectivity in episodic cluster headache: a graph theoretical analysis. J Clin Neurosci 62:60–65. https://doi.org/10.1016/j.jocn.2019.01.007

    Article  PubMed  Google Scholar 

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Acknowledgement

This work was supported by the 2021 Inje University research grant.

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Authors and Affiliations

  1. Departments of Neurology, Haeundae Paik Hospital, Inje University College of Medicine, Haeundae-ro 875, Haeundae-gu, Busan, 48108, Korea

    Dong Ah Lee & Kang Min Park

  2. Departments of Radiology, Haeundae Paik Hospital, Inje University College of Medicine, Busan, Korea

    Ho-Joon Lee

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  1. Dong Ah Lee
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Correspondence to Kang Min Park.

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All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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DAL and H-JL contributed equally to this study

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Lee, D.A., Lee, HJ. & Park, K.M. Alterations of thalamic nuclei volumes in patients with cluster headache. Neuroradiology 64, 1839–1846 (2022). https://doi.org/10.1007/s00234-022-02951-8

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