Spatial and temporal patterns of nitric oxide diffusion and degradation drive emergent cerebrovascular dynamics.
Nitric oxide (NO) is a gaseous signaling molecule that plays an important role in neurovascular coupling. NO produced by neurons diffuses into the smooth muscle surrounding cerebral arterioles, driving vasodilation. However, the rate of NO degradation in hemoglobin is orders of magnitude higher than...
| Main Authors: | , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2020-07-01
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| Series: | PLoS Computational Biology |
| Online Access: | https://doi.org/10.1371/journal.pcbi.1008069 |
| _version_ | 1818578146005352448 |
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| author | William Davis Haselden Ravi Teja Kedarasetti Patrick J Drew |
| author_facet | William Davis Haselden Ravi Teja Kedarasetti Patrick J Drew |
| author_sort | William Davis Haselden |
| collection | DOAJ |
| description | Nitric oxide (NO) is a gaseous signaling molecule that plays an important role in neurovascular coupling. NO produced by neurons diffuses into the smooth muscle surrounding cerebral arterioles, driving vasodilation. However, the rate of NO degradation in hemoglobin is orders of magnitude higher than in brain tissue, though how this might impact NO signaling dynamics is not completely understood. We used simulations to investigate how the spatial and temporal patterns of NO generation and degradation impacted dilation of a penetrating arteriole in cortex. We found that the spatial location of NO production and the size of the vessel both played an important role in determining its responsiveness to NO. The much higher rate of NO degradation and scavenging of NO in the blood relative to the tissue drove emergent vascular dynamics. Large vasodilation events could be followed by post-stimulus constrictions driven by the increased degradation of NO by the blood, and vasomotion-like 0.1-0.3 Hz oscillations could also be generated. We found that these dynamics could be enhanced by elevation of free hemoglobin in the plasma, which occurs in diseases such as malaria and sickle cell anemia, or following blood transfusions. Finally, we show that changes in blood flow during hypoxia or hyperoxia could be explained by altered NO degradation in the parenchyma. Our simulations suggest that many common vascular dynamics may be emergent phenomena generated by NO degradation by the blood or parenchyma. |
| first_indexed | 2024-12-16T06:41:10Z |
| format | Article |
| id | doaj.art-4bfada81bf9a41fd8be82a787f0b28d3 |
| institution | Directory Open Access Journal |
| issn | 1553-734X 1553-7358 |
| language | English |
| last_indexed | 2024-12-16T06:41:10Z |
| publishDate | 2020-07-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Computational Biology |
| spelling | doaj.art-4bfada81bf9a41fd8be82a787f0b28d32022-12-21T22:40:41ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582020-07-01167e100806910.1371/journal.pcbi.1008069Spatial and temporal patterns of nitric oxide diffusion and degradation drive emergent cerebrovascular dynamics.William Davis HaseldenRavi Teja KedarasettiPatrick J DrewNitric oxide (NO) is a gaseous signaling molecule that plays an important role in neurovascular coupling. NO produced by neurons diffuses into the smooth muscle surrounding cerebral arterioles, driving vasodilation. However, the rate of NO degradation in hemoglobin is orders of magnitude higher than in brain tissue, though how this might impact NO signaling dynamics is not completely understood. We used simulations to investigate how the spatial and temporal patterns of NO generation and degradation impacted dilation of a penetrating arteriole in cortex. We found that the spatial location of NO production and the size of the vessel both played an important role in determining its responsiveness to NO. The much higher rate of NO degradation and scavenging of NO in the blood relative to the tissue drove emergent vascular dynamics. Large vasodilation events could be followed by post-stimulus constrictions driven by the increased degradation of NO by the blood, and vasomotion-like 0.1-0.3 Hz oscillations could also be generated. We found that these dynamics could be enhanced by elevation of free hemoglobin in the plasma, which occurs in diseases such as malaria and sickle cell anemia, or following blood transfusions. Finally, we show that changes in blood flow during hypoxia or hyperoxia could be explained by altered NO degradation in the parenchyma. Our simulations suggest that many common vascular dynamics may be emergent phenomena generated by NO degradation by the blood or parenchyma.https://doi.org/10.1371/journal.pcbi.1008069 |
| spellingShingle | William Davis Haselden Ravi Teja Kedarasetti Patrick J Drew Spatial and temporal patterns of nitric oxide diffusion and degradation drive emergent cerebrovascular dynamics. PLoS Computational Biology |
| title | Spatial and temporal patterns of nitric oxide diffusion and degradation drive emergent cerebrovascular dynamics. |
| title_full | Spatial and temporal patterns of nitric oxide diffusion and degradation drive emergent cerebrovascular dynamics. |
| title_fullStr | Spatial and temporal patterns of nitric oxide diffusion and degradation drive emergent cerebrovascular dynamics. |
| title_full_unstemmed | Spatial and temporal patterns of nitric oxide diffusion and degradation drive emergent cerebrovascular dynamics. |
| title_short | Spatial and temporal patterns of nitric oxide diffusion and degradation drive emergent cerebrovascular dynamics. |
| title_sort | spatial and temporal patterns of nitric oxide diffusion and degradation drive emergent cerebrovascular dynamics |
| url | https://doi.org/10.1371/journal.pcbi.1008069 |
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