Comprehensive Assessment of the Functional State of the Cerebral Cortex Microcirculatory Bed at Different Stages of Aging

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Abstract

Using Doppler flowmetry and tissue optical oximetry, a comprehensive spectral analysis of the oscillatory components of the myogenic, neurogenic and endothelial components of microvascular tone and an assessment of the oxygen transport dynamics in the cerebral cortex of rats at the age of 4, 18 and 23 months were performed. Regional differences of age-dependent changes in the regulatory mechanisms of microcirculation and the efficiency of tissue oxygen extraction were revealed. It was found that at the age of 18 months, microcirculatory changes are observed in the frontal and parietal cortical areas and are manifested as a decrease in sympathetic regulation of microcirculation, a decrease in precapillary myogenic resistance, vasodilation and an increase in the contribution of the capillary unit to microcirculation. In the parietal cortical area, these changes contribute to the activation of tissue oxidative metabolism and to an increase in oxygen consumption. With further aging, microvascular endothelial dysfunction develops and the contribution of the endothelial component to the total perfusion level of all cortical areas decreases. These disorders in 23-month-old rats are accompanied by an increase in the contribution of sympathetic regulation of microcirculation in the frontal cortex, a decrease in the contribution of the capillary unit to the microcirculation in the occipital area, and the development of stagnant processes in the venous area of the microcirculatory bed of the parietal cortex, reducing the efficiency of tissue oxygen extraction from the blood.

About the authors

O. P Gorshkova

Pavlov Institute of Physiology, Russian Academy of Sciences

Email: o_gorshkova@inbox.ru
St. Petersburg, Russia

I. B Sokolova

Pavlov Institute of Physiology, Russian Academy of Sciences

St. Petersburg, Russia

References

  1. Mandalà M. and Cipolla M. J. Aging-related structural and functional changes in cerebral arteries: caloric restriction (CR) intervention. J. Vasc. Med. Surg., 9 (7), 1000002 (2021).
  2. Bennett H. C., Zhang Q., Wu Y. T., Chon U., Pi H. J., Drew P. J., and Kim Y. Aging drives cerebrovascular network remodeling and functional changes in the mouse brain. Nat Commun., 15, 6398 (2024). doi: 10.1038/s41467-024-50559-8
  3. Sakamuri S. S., Sure V. N., Kolli L., Evans W. R., Sperling J. A., Bix G. J., Wang X., Atochin D. N., Murfee W. L., Mostany R., and Katakam P. V. Aging related impairment of brain microvascular bioenergetics involves oxidative phosphorylation and glycolytic pathways. J. Cereb. Blood Flow Metab., 42 (8), 1410 (2022). doi: 10.1177/0271678X211069266
  4. Li Y., Choi W. J., Wei W. Song S., Zhang Q., Liu J., and Wang R. K. Aging-associated changes in cerebral vasculature and blood flow as determined by quantitative optical coherence tomography angiography. Neurobiol. Aging, 70, 148 (2018). doi: 10.1016/j.neurobiolaging.2018.06.017
  5. Alisch J. S. R., Khattar N., Kim R. W., Cortina L. E., Rejimon A. C., Qian W., Ferrucci L., Resnick S. M., Spencer R. G., and Bouhrara M. Sex and age-related differences in cerebral blood flow investigated using pseudo-continuous arterial spin labeling magnetic resonance imaging. Aging (Albany NY), 13 (4), 4911 (2021). doi: 10.18632/aging.202673
  6. Claassen J. A. H. R., Thijssen D. H. J., Panerai R. B., and Faraci F. M. Regulation, of cerebral blood flow in humans: physiology and clinical implications of autoregulation. Physiol. Rev., 101 (4), 1487 (2021). doi: 10.1152/physrev.00022.2020
  7. Gorshkova O. P. Changes in rat cerebral blood flow velocities at different stages of aging. J. Evol. Biochem. Phys., 59, 569-576 (2023). doi: 10.1134/S0022093023020229
  8. Peng S. L., Chen X., Li Y., Rodrigue K. M., Park D. C., and Lu H. Age-related changes in cerebrovascular reactivity and their relationship to cognition: a four-year longitudinal study. Neuroimage, 174, 257-262 (2018). doi: 10.1016/j.neuroimage.2018.03.033
  9. Bogorad M. I., DeStefano J. G., Linville R. M., Wong A. D., and Searson P. C. Cerebrovascular plasticity: processes that lead to changes in the architecture of brain microvessels. J. Cereb. Blood Flow Metab., 39 (8), 1413 (2019). doi: 10.1177/0271678X19855875
  10. Bailey T. G., Klein T., Meneses, A. L., Stefanidis K. B., Ruediger S., Green D. J., Stuckenschneider T., Schneider S., and Askew C. D. Cerebrovascular function and its association with systemic artery function and stiffness in older adults with and without mild cognitive impairment. Eur J Appl Physiol., 122, 1843-1856 (2022). doi: 10.1007/s00421-022-04956-w
  11. Pahlavian S. H., Wang X., Ma S., Zheng H., Casey M., D’Orazio L. M., Shao X., Ringman J. M., Chui H., Wang D. J., and Yan L. Cerebroarterial pulsatility and resistivity indices are associated with cognitive impairment and white matter hyperintensity in elderly subjects: A phase-contrast MRI study. J. Cereb. Blood Flow Metab., 41 (3), 670 (2021). doi: 10.1177/0271678X20927101
  12. Houben A. J. H. M., Martens R. J. H., and Stehouwer C. D. A. Assessing microvascular function in humans from a chronic disease perspective. J. Am. Soc. Nephrol., 28 (12), 3461 (2017). doi: 10.1681/ASN.2017020157
  13. Lecrux C. and Hamel E. Neuronal networks and mediators of cortical neurovascular coupling responses in normal and altered brain states. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 371 (1705), 20150350 (2016). doi: 10.1098/rstb.2015.0350
  14. Hamel E. Perivascular nerves and the regulation of cerebrovascular tone. J. Appl. Physiol. (1985), 100 (3), 1059 (2006). doi: 10.1152/japplphysiol.00954.2005
  15. Brown L. S., Foster C. G., Courtney J.-M., King N. E., Howells D. W., and Sutherland B. A. Pericytes and neurovascular function in the healthy and diseased brain. Front. Cell. Neurosci., 13, 282 (2019). doi: 10.3389/fncel.2019.00282
  16. Grubb S., Cai C., Hald B. O., Khennouf L., Murmu R. P., Jensen A. G. K., Fordsmann J., Zambach S., and Lauritzen M. Precapillary sphincters maintain perfusion in the cerebral cortex. Nat. Commun., 11, 395 (2020). doi: 10.1038/s41467-020-14330-z
  17. Erdener S. E. and Dalkara T. Small vessels are a big problem in neurodegeneration and neuroprotection. Front. Neurol., 10, 889 (2019). doi: 10.3389/fneur.2019.00889
  18. Østergaard L., Jespersen S. N., Engedahl T., Gutiérrez Jiménez E., Ashkanian M., Hansen M. B., Eskildsen S., and Mouridsen K. Capillary dysfunction: its detection and causative role in dementias and stroke. Curr. Neurol. Neurosci. , 15 (6), 37 (2015). doi: 10.1007/s11910-015-0557-x
  19. Berthiaume A. A., Schmid F. Stamenkovic S. Coelho-Santos V, Nielson C., Weber B., Majesky M., and Shih A. Pericyte remodeling is deficient in the aged brain and contributes to impaired capillary fow and structure. Nat. Commun. , 13, 5912 (2022). doi: 10.1038/s41467-022-33464-w
  20. Gorshkova O. P. Age-related changes in the functional activity of ATP-sensitive potassium channels in rat pial arteries. J. Evol. Biochem. Phys., 58, 345-352 (2022). doi: 10.1134/S0022093022020041
  21. Крупаткин А. И. и Сидоров В. В. Лазерная допплеровская флоуметрия микроциркуляции крови (Медицина, М., 2005).
  22. Александрин В. В., Иванов А. В. и Кубатиев А. А. Вейвлет-анализ мозгового кровотока у крыс в терминальном состоянии. Патогенез, 20 (1), 69 (2022). doi: 10.25557/2310-0435.2022.01.69-73
  23. Федорович А. А., Горшков А. Ю., Королев А. И., Омельяненко К. В., Дадаева В. А., Михайлова М. А., Чащин М. Г. и Драпкина О. М. Гендерные различия структурно-функционального состояния микроциркуляторного русла кожи у лиц с впервые выявленной артериальной гипертензией. Кардиоваскулярная терапия и профилактика, 22 (8), 3696 (2023). doi: 10.15829/1728-8800-2023-3696
  24. Sargent S. M., Bonney S. K., Li Y., Stamenkovic S., Takeno M. M., Coelho-Santos V., and Shih A. Y. Endothelial structure contributes to heterogeneity in brain capillary diameter. Vasc. Biol., 5 (1), e230010 (2023). doi: 10.1530/VB-23-0010
  25. Sonntag W. E., Eckman D. M., Ingraham J., and Riddle D. R. Regulation of cerebrovascular aging. In Brain Aging: Models, Methods, and Mechanisms, Ed. by D.R. Riddle (CRC Press/Taylor & Francis, Boca Raton (FL), 2007), chapt. 12.
  26. Крупаткин А. И. Колебания кровотока - новый диагностический язык в исследовании микроциркуляции. Регионарное кровообращение и микроциркуляция, 13 (1), 83-99 (2014). doi: 10.24884/1682-6655-2014-13-1-83-99
  27. Zimmerman B., Rypma B., Gratton G., and Fabiani M. Age-related changes in cerebrovascular health and their effects on neural function and cognition: A comprehensive review. Psychophysiology, 58 (7), e13796 (2021). doi: 10.1111/psyp.13796
  28. Hennigs J. K., Matuszcak C., Trepel M., and Körbelin J. Vascular endothelial cells: heterogeneity and targeting approaches. Cells., 10 (10), 2712 (2021). doi: 10.3390/cells10102712
  29. Чуян Е. Н., Ананченко М. Н. и Трибрат Н. С. Индивидуально-типологические реакции микроциркуляторных процессов на электромагнитное излучение миллиметрового диапазона. Регионарное кровообращение и микроциркуляция, 9 (1), 68-74 (2010). doi: 10.24884/1682-6655-2010-9-1-68-74
  30. Фролов А. В., Локтионова Ю. И., Жарких Е. В., Сидоров В. В., Танканаг А. В. и Дунаев А. В. Реакция микроциркуляции крови в коже различных участков тела при выполнении дыхательных упражнений йоги. Регионарное кровообращение и микроциркуляция, 22 (1), 72-84 (2023). doi: 10.24884/1682-6655-2023-22-1-72-84
  31. Thorn C. E., Kyte H., Slaff D. W., and Shore A. C. An association between vasomotion and oxygen extraction. Am. J. Physiol. Heart. Circ. Physiol., 301 (2), H429-H442 (2011). doi: 10.1152/ajpheart.01316.2010
  32. Рогаткин Д. А. Физические основы оптической оксиметрии. Медицинская физика, 2, 97-114 (2012).

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