Morphological structures of the circumvetricular complex

Authors

DOI:

https://doi.org/10.29038/NCBio.24.1-2

Keywords:

circumventricular complex, cerebrospinal fluid, brain, blood-brain barrier.

Abstract

Brain homeostasis requires the maintenance of barriers between the brain and the periphery, which are provided by brain microvessels in the blood-brain barrier and epithelial cells in the choroid plexus. Circumventricular complex (CVC) – structures located around the third and fourth ventricles, lining the cavity of the third ventricle (neurohypophysis, vascular organ of the end plate, epiphysis, subvault and subcommissural organs) and the fourth ventricle (posterior region), different from other structures of the brain due to the maximum vascularization and the absence of a typical blood-brain barrier. The subcommissural organ and the area postrema are located at the confluence between the ventricles, while the neurohypophysis, the vascular organ of the terminal plate, and the pineal gland line the ventricular depressions. All structures of the central nervous system are divided into sensory and secretory. Vessels in the CVC branch into a network of fenestrated capillaries with loosely connected astrocytic ends, which allows them to be considered as gates» to the brain; substances are transported by blood and freely leave the capillary lumen. Neurons and glial cells of the CVC form a unique symbiosis of receptors and ion channels, receiving chemical signals from the bloodstream. CVCs are described as the «windows of the brain» that form the blood-CSF barrier on the ventricular wall, which is composed of tanycyte-like cells that line the ventricular ependyma. Astrocytes and tanycytes form a dense barrier in the distal part of the CVC, preventing the free diffusion of the molecules obtained. from the blood to the neighboring areas of the brain. The barrier in front of the fenestrated vessels of the CVC may limit molecules carried by the blood through these «windows of the brain» and prevent their diffusion into the cerebrospinal fluid. In the central nervous system, connections between the central nervous system and peripheral blood flow serve as an alternative route for peptides and hormones of nervous tissue into the bloodstream, primarily performing neuroimmune-endocrine functions, as well as the role of an «immune watchman».

Key words: circumventricular complex, cerebrospinal fluid, brain, blood-brain barrier.

References

Пикалюк, В. С.; Бессалова, Є. Ю.; Кісельов, В. В.; Роль і місце спинномозкової рідини в нейроендокринній регуляції діяльності репродуктивної системи живого організму. Кримський журнал експериментальної і клінічної медицини. 2012. 9(3-4(9-8)). С. 41–46.

Пикалюк, В. С.; Бессалова, Є. Ю.; Новосельцева, О. К. Лактотропний ефект ксеногенної цереброспінальної рідини. VI конгрес Українського товариства нейронаук. Київ, 4–8червня, 2014 р. Київ, 2014. С. 140.

Пикалюк, В. С.; Бессалова, Є. Ю.; Олейникова, О. К.; Корольов, В. А.; Волков, П. М. Роль цереброспінальної рідини в морфологічній і функціональній інтеграції регуляторних систем: фізіологія та медицина. Дослідження, високі технології, стартапи. Збірник статей VI міжнародної практичної конференції, 2014 С. 6–9.

Пикалюк, В. С.; Бессалова, Є. Ю.; Олейникова, О. К. Сучасний погляд на регуляторну роль цереброспінальної рідини в організмі ссавців та людини. Актуальні питання антропології, 2014. Вип. 9. С. 265–274.

Пикалюк, В. С.; Корольов, В. А.; Бессалова, Є. Ю.; Ткач, В. В.; Макалиш, Т. П. Роль цереброспінальної рідини в механізмах взаємодії нервової, ендокринної та імунної систем. Актуальні питання морфології. Збірник матеріалів міжнародної наукової конференції, присвяченої 100-річчю від дня народження проф. Б. В. Перліна. Кишинів. 2012. С. 312–317.

Пикалюк, В. С.; Корсунська, Л. Л.; Роменський, А. О.; Шаймарданова, Л. Р. Циркумвентрикулярна система як «ворота» у головний мозок. Таврійський медико-біологічний вісник, 2013. 16(1, ч. 1(61). С. 270–276.

Пикалюк, В. С.; Ткач, В. В.; Роменський, А. О.; Шаймарданова, Л. Р. Деякі аспекти циркумвентрикулярної системи. Кримський журнал експериментальної та клінічної медицини, 2016. 6( 3). С. 177–182.

Arendt, D.; Tosches, M. A.; Marlow, H. From nerve net to nerve ring, nerve cord and brain – evolution of the nervous system. Nat Rev Neurosci., 2016. 17 P. 61–72.

Bennett, L.; Yang, M.; Enikolopov, G.; Iacovitti, L. Circumventricular Organs: A Novel Site of Neural Stem Cells in the Adult Brain. Mol Cell Neurosci., 2009. 41(3). P. 337–347. DOI: 10.1016/j.mcn.2009.04.007.

Blaylock, R. L.; Excitotoxins, neurodegeneration, neurodevelopment, migraines, seizures. Medical Sentinel Magazine by the Association of American Physicians and Surgeons, 2000. 7(2) P. 12.

Bourque, C. W.; Oliet, S. H.; Richard, D. Osmoreceptors, osmoreception, and osmoregulation. Front Neuroendocrinol, 1994. 15(3). P. 231–74. DOI: 10.1006/frne.1994.1010.

Bourque, C. W. Central mechanisms of osmosensation and systemic osmoregulation. Nat Rev Neurosci., 2008. 9 P. 519–531.

Cancelliere, N. M.; Black, E. A.; Ferguson, A. V. Neurohumoral integration of cardiovascular function by the lamina terminalis. Curr Hypertens Rep., 2015. 17. P. 9.

Castaneyra‐Perdomo, A.; Meyer, G.; Heylings, D. J. Early development of the human area postrema and subfornical organ. Anat. Rec., 1992. 232. P. 612–619.

Ciura, S.; Liedtke, W.; Bourque, Ch. W. Hypertonicity Sensing in Organum Vasculosum Lamina Terminalis Neurons: A Mechanical Process Involving TRPV1 But Not TRPV4. The Journal of Neuroscience., 2011. 31(41). P. 14669–4676.

Clarke, I. J. Hypothalamus as an endocrine organ. Compr Physiol., 2015. 5. P. 217–253.

Davis, S. W.; Ellsworth, B. S.; Perez Millan MI, et al. Pituitary gland development and disease: from stem cell to hormone production. Curr Top Dev Biol., 2013. 106. P. 1–47.

Ferguson, A. V.; Bains, J. S.; Electrophysiology of the circumventricular organs. Frontiers in Neuroendocrinology, 1996. 17(4). P. 440–475.

Fry, M.; Hoyda, T. D.; Ferguson, A. V. Making sense of it: Roles of the sensory circumventricular organs in feeding and regulation of energy homeostasis. Exp. Biol. Med., 2007. 232. P. 14–26.

Furube, E.; Ishii, H.; Nambu, Y.; Kurganov, E.; Nagaoka, S.; Morita, M.; Miyata, S.; Neural stem cell phenotype of tanycyte-like ependymal cells in the circumventricular organs and central canal of adult mouse brain. Sci Rep., 2020. 10. P. 2826. DOI: 10.1038/s41598-020-59629-5.

Ganong, W. F. Circumventricular organs: Definition and role in the regulation of endocrine and autonomic function. Clin. Exp. Pharmacol. Physiol., 2000. 27. P. 422–427.

García-Lecea, M.; Gasanov, E.; Jedrychowska, J.; Kondrychyn, I.; Te, Ch.; May-Su, Y.; Korzh, V. Development of Circumventricular Organs in the Mirror of Zebrafish Enhancer-Trap Transgenics. Front Neuroanat., 2017. 11. P. 114. DOI: 10.3389/fnana.2017.00114.

Grondona, J. M.; Hoyo‐Becerra, C.; Visser, R. et al. The subcommissural organ and the development of the posterior commissure. Int Rev Cell Mol Biol., 2012. 296. P. 63–137.

Guerra, M. M.; Gonzalez, C.; Caprile, T., et al. Understanding how the subcommissural organ and other periventricular secretory structures contribute via the cerebrospinal fluid to neurogenesis. Front Cell Neurosci., 2015. 9. P. 480.

Hindmarch, C. C.; Ferguson, A. V. Physiological roles for the subfornical organ: a dynamic transcriptome shaped by autonomic state. J. Physiol., 2016. 594. P. 1581–1589.

Hirth F. On the origin and evolution of the tripartite brain. Brain Behav Evol., 2010. 76. P. 3–10.

Hofer, H. O. The terminal organ of the subcommissural complex of chordates: Definition and perspectives. Gegenbaurs Morphol. Jahrb., 1987. 133. P. 217–226.

Issa, A. T.; Miyata, K.; Heng, V.; Mitchell, K. D.; Derbenev, A. V. Increased neuronal activity in the OVLT of Cyp1a1 Ren2 transgenic rats with inducible Ang IIdependent malignant hypertension. Neurosci. Lett., 2012. 519. P. 26–30.

Kiecker, C.; Graham, A.; Logan, M. Differential cellular responses to hedgehog signalling in vertebrates‐what is the role of competence? J. Dev. Biol. 2016. 4. P. 36.

Kiecker, C.; Lumsden, A. The role of organizers in patterning the nervous system. Annu Rev. Neurosci., 2012. 35. P. 347–367.

Kiecker, C. The origins of the circumventricular organs. J. Anat., 2018. 32(4). P. 540–553. DOI: 10.1111/joa.12771.

Kwon, J. J.; Dow, S. A.; Young, C. N. Sensory Circumventricular Organs, Neuroendocrine Control, and Metabolic Regulation. Metabolites., 2021. 11(8). P. 494. DOI: 10.3390/metabo11080494.

Langlet, F.; Mullier, A.; Bouret, S. G.; Prevot, V.; Dehouck, B. Tanycyte-Like Cells Form a Blood–Cerebrospinal Fluid Barrier in the Circumventricular Organs of the Mouse Brain. J Comp. Neurol., 2013. 15. 521(15). P. 3389–3405. DOI: 10.1002/cne.23355.

Liebrich, L. S.; Schredl, M.; Findeisen, P.; Groden, C.; Bumb, J. M.; Nölte, I. S. Morphology and function: MR pineal volume and melatonin level in human saliva are correlated. J. Magn. Reson. Imaging., 2014. 40. P. 966–971. DOI: 10.1002/jmri.24449.

Matsuda, T.; Hiyama, T. Y.; Niimura, F., et al. Distinct neural mechanisms for the control of thirst and salt appetite in the subfornical organ. Nat. Neurosci., 2017. 20. P. 230–241.

McKinley, M. J.; Yao, S. T.; Uschakov, A., et al. The median preoptic nucleus: front and centre for the regulation of body fluid, sodium, temperature, sleep and cardiovascular homeostasis. Acta Physiol. (Oxf)., 2015. 214. P. 8–32.

Mimee, A.; Smith, P. M.; Ferguson, A. V. Circumventricular organs: Targets for integration of circulating fluid and energy balance signals? Physiol. Behav., 2013. 121. P. 96–102.

Miyata, S. New aspects in fenestrated capillary and tissue dynamics in the sensory circumventricular organs of adult brains. Front. Neurosci., 2015. 9. P. 390. DOI: 10.3389/fnins.2015.00390.

Morita, S.; Furube, E.; Mannari, T.; Okuda, H.; Tatsumi, K.; Wanaka, A.; Miyata, S. Heterogeneous vascular permeability and alternative diffusion barrier in sensory circumventricular organs of adult mouse brain. Cell Tissue Res., 2016. 363. P. 497–511. DOI: 10.1007/s00441-015-2207-7.

Price, C. J.; Hoyda, T. D.; Ferguson, A. V. The area postrema: a brain monitor and integrator of systemic autonomic state. Neuroscientist, 2008. 14. P. 182–194.

Roth, J.; Rummel, C.; Barth, S. W.; Gerstberger, R.; Hübschle, T. Molecular aspects of fever and hyperthermia. Immunol. Allergy Clin. North Am., 2009. 29. P. 229–245.

Schulz, M.; Engelhardt, B. The circumventricular organs participate in the immunopathogenesis of experimental autoimmune encephalomyelitis. Cerebrospinal Fluid Res., 2005. 2. P. 8. DOI: 10.1186/1743-8454-2-8.

Silva, S. C.; Cavadas, C. Hypothalamic Dysfunction in Obesity and Metabolic Disorders. Adv. Neurobiol., 2017. 19. P. 73–116. DOI: 10.1007/978-3-319-63260-5_4.

Sisó, S.; Jeffrey, M.; González, L. Sensory circumventricular organs in health and disease. Acta. Neuropathol., 2010. 120. P. 689–705.

Szarek, E.; Cheah, P. S.; Schwartz, J., et al. Molecular genetics of the developing neuroendocrine hypothalamus. Mol. Cell Endocrinol., 2010. 323 P. 115–123.

Timper, K.; Brüning, J. C. Hypothalamic circuits regulating appetite and energy homeostasis: Pathways to obesity. Dis. Model. Mech., 2017. 10. P. 679–689. DOI: 10.1242/dmm.026609.

Verheggen, I. C.; de Jong, J. J.; van Boxtel, M. P.; Postma, A. A.; Verhey, F. R.; Jansen, J. F., et al. Permeability of the windows of the brain: feasibility of dynamic contrast-enhanced MRI of the circumventricular organs. Fluids Barriers CNS., 2020. 17. P. 66. DOI: 10.1186/s12987-020-00228-x.

Wang, Y.; Sabbagh, M. F.; Gu, X.; Rattner, A.; Williams, J.; Nathans, J. Beta-catenin signaling regulates barrier-specific gene expression in circumventricular organ and ocular vasculatures. Elife., 2019. 1:8. P. 43257. DOI: 10.7554/eLife.43257.

Wuerfel, E.; Infante-Duarte, C.; Glumm, R.; Jens, T. Wuerfel. Gadofluorine M-enhanced MRI shows involvement of circumventricular organs in neuroinflammation. J. Neuroinflammation, 2010. 7. P. 70. DOI: 10.1186/1742-2094-7-70.

Published

2024-06-26

Issue

Section

Human and Animal Physiology

How to Cite

Morphological structures of the circumvetricular complex. (2024). Notes in Current Biology, 7(1). https://doi.org/10.29038/NCBio.24.1-2