Neuronal nitric oxide synthase regulates regional brain perfusion in healthy humans
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Aims: Neuronal nitric oxide synthase (nNOS) is highly expressed within the cardiovascular and nervous systems. Studies in genetically modified mice suggest roles in brain blood flow regulation while dysfunctional nNOS signalling is implicated in cerebrovascular ischaemia and migraine. Previous human studies have investigated the effects of non-selective NOS inhibition but there has been no direct investigation of the role of nNOS in human cerebrovascular regulation. We hypothesized that inhibition of the tonic effects of nNOS would result in global or localized changes in cerebral blood flow (CBF), as well as changes in functional brain connectivity. Methods and results: We investigated the acute effects of a selective nNOS inhibitor, S-methyl-L-thiocitrulline (SMTC), on CBF and brain functional connectivity in healthy human volunteers (n = 19). We performed a randomized, placebo-controlled, crossover study with either intravenous SMTC or placebo, using magnetic resonance imaging protocols with arterial spin labelling and functional resting state neuroimaging. SMTC infusion induced an ∼4% decrease in resting global CBF [−2.3 (−0.3, −4.2) mL/100g/min, mean (95% confidence interval, CI), P = 0.02]. In a whole-brain voxel-wise factorial-design comparison of CBF maps, we identified a localized decrease in regional blood flow in the right hippocampus and parahippocampal gyrus following SMTC vs. placebo (2921 voxels; T = 7.0; x = 36; y = −32; z = −12; P < 0.001). This was accompanied by a decrease in functional connectivity to the left superior parietal lobule vs. placebo (484 voxels; T = 5.02; x = −14; y = −56; z = 74; P = 0.009). These analyses adjusted for the modest changes in mean arterial blood pressure induced by SMTC as compared to placebo [+8.7 mmHg (+1.8, +15.6), mean (95% CI), P = 0.009]. Conclusions: These data suggest a fundamental physiological role of nNOS in regulating regional CBF and functional connectivity in the human hippocampus. Our findings have relevance to the role of nNOS in the regulation of cerebral perfusion in health and disease.
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NO plays a pivotal role in neurovascular coupling, whereby neuronal activity triggers local vasodilation, thereby increasing cerebral blood flow.
“NO plays a pivotal role in neurovascular coupling, whereby neuronal activity triggers local vasodilation, thereby increasing cerebral blood flow [166,167].”
From Dietary Nitrate-Rich Vegetables as Natural Modulators of Health: Mechanisms and Benefits in Ageing Populations (2026) · cites this paper as [167]
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- Authors
- O’Gallagher, K., Puledda, F., O’Daly, O., Ryan, M., Dancy, L., Chowienczyk, P. J., Zelaya, F., Goadsby, P. J., & Shah, A. M.
- Affiliations
- King's College London (GB)
- Department of Neuroimaging, Centre for Neuroimaging Sciences, Institute of Psychiatry, Psychology & Neuroscience, London, UK
- Department of Clinical Pharmacology, King’s College London British Heart Foundation Centre of Research Excellence, School of Cardiovascular Medicine & Sciences, London, UK
- Corresponding author
- Goadsby, Peter J
- Shah, Ajay M
- ORCID
- Venue
- Cardiovascular Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2021-04-30
- Volume
- 118
- Issue
- 5
- Pages
- 1321-1329
- ISSN
- 0008-6363 (ISSN-L)
- 1755-3245
- PMC
- PMC8953449
- OpenAlex
- W3171548369
- Cited by
- 39
- References
- 54
- Citations by year
- 2026: 4 · 2025: 13 · 2024: 11 · 2023: 5 · 2022: 3 · 2021: 3
- FWCI
- 2.91
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cardiovascular Research (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research Portal (King's College London) (submittedVersion, other-oa)
- Funders
- National Institute for Health Research Biomedical Research Centre
- Guy’s & St Thomas’ NHS Foundation Trust and King’s College London (IS-BRC-1215-20006)
- NIHR SLaM Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King’s College London (IS-BRC-1215-20018)
- King’s College Hospital NHS Foundation Trust. We also acknowledge support from the British Heart Foundation (CH/1999001/11735, RE/18/2/34213)
- UK Medical Research Council Clinical Research Training Fellowship (MR/R017751/1)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Keywords
- neuronal nitric oxide synthase, cerebral blood flow, S-methyl-L-thiocitrulline, nNOS inhibition, brain functional connectivity, hippocampus, parahippocampal gyrus, superior parietal lobule, cerebrovascular regulation, arterial spin labeling, resting-state functional connectivity
- MeSH terms
- Animals, Brain, Enzyme Inhibitors, Humans, Nitric Oxide, Perfusion, Regional Blood Flow, Cross-Over Studies, Mice, Nitric Oxide Synthase Type I
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