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Oscillations and concentration dynamics of brain tissue oxygen in neonates and adults

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Abstract

The brain is a metabolically demanding organ and its health directly depends on brain oxygen dynamics to prevent hypoxia and ischemia. Localized brain tissue oxygen is characterized by a baseline level combined with spontaneous oscillations. These oscillations are attributed to spontaneous changes of vascular tone at the level of arterioles and their frequencies depend on age. Specifically, lower frequencies are more typical for neonates than for adults. We have built a mathematical model which analyses the diffusion abilities of oxygen based on the frequency of source brain oxygen oscillations and neuronal demand. We have found that a lower frequency of spontaneous oscillations of localized brain tissue oxygen can support higher amplitudes of oxygen concentration at areas distant from a source relative to oscillations at higher frequencies. Since hypoxia and ischemia are very common events during early development and the neurovascular unit is underdeveloped in neonates, our results indicate that lower frequency oxygen oscillations can represent an effective passive method of neonatal brain protection against hypoxia. These results can have a potential impact on future studies aiming to find new treatment strategies for brain ischemia.

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References

  • Aalkjaer, C., Boedtkjer, D., Matchkov, V. (2011). Vasomotion - what is currently thought? Acta Physiologica (Oxf), 202(3), 253–269.

    Article  CAS  Google Scholar 

  • Aksenov, D.P., Dmitriev, A.V., Miller, M.J., Wyrwicz, A.M., Linsenmeier, R.A. (2018). Brain tissue oxygen regulation in awake and anesthetized neonates. Neuropharmacology, 135, 368–375.

    Article  CAS  Google Scholar 

  • Andreone, B.J., Lacoste, B., Gu, C. (2015). Neuronal and vascular interactions. Annual Review Neuroscience, 38, 25–46.

    Article  CAS  Google Scholar 

  • Attwell, D., Buchan, A.M., Charpak, S., Lauritzen, M., Macvicar, B.A., Newman, E.A. (2010). Glial and neuronal control of brain blood flow. Nature, 468(7321), 232–243.

    Article  CAS  Google Scholar 

  • Charriaut-Marlangue, C., & Baud, O. (2018). A model of perinatal ischemic stroke in the rat: 20 years already and what lessons? Frontiers in Neurology, 9, 650.

    Article  Google Scholar 

  • Choy, M., Ganesan, V., Thomas, D.L., Thornton, J.S., Proctor, E., King, M.D., et al. (2006). The chronic vascular and haemodynamic response after permanent bilateral common carotid occlusion in newborn and adult rats. Journal of Cerebral Blood Flow and Metabolism, 26(8), 1066–1075.

    Article  Google Scholar 

  • Collaborators, GBDCoD. (2018). Global, regional, and national age-sex-specific mortality for 282 causes of death in 195 countries and territories, 1980-2017: a systematic analysis for the global burden of disease study 2017. Lancet, 392(10159), 1736–1788.

    Article  Google Scholar 

  • Dagal, A., & Lam, A.M. (2009). Cerebral autoregulation and anesthesia. Current Opinion in Anaesthesiology, 22(5), 547–552.

    Article  Google Scholar 

  • Dienel, G.A. (2019). Brain glucose metabolism: integration of energetics with function. Physiology Review, 99 (1), 949–1045.

    Article  CAS  Google Scholar 

  • Goldman, D., & Popel, A.S. (2001). A computational study of the effect of vasomotion on oxygen transport from capillary networks. Journal of Theoretical Biology, 209(2), 189–199.

    Article  CAS  Google Scholar 

  • Hudetz, A.G., Biswal, B.B., Shen, H., Lauer, K.K., Kampine, J.P. (1998). Spontaneous fluctuations in cerebral oxygen supply. an introduction. Advances in Experimental Medicine and Biology, 454, 551–559.

    Article  CAS  Google Scholar 

  • Kozberg, M., & Hillman, E. (2016). Neurovascular coupling and energy metabolism in the developing brain. Progress in Brain Research, 225, 213–242.

    Article  CAS  Google Scholar 

  • Larson, J., Drew, K.L., Folkow, L.P., Milton, S.L., Park, T.J. (2014). No oxygen? no problem! intrinsic brain tolerance to hypoxia in vertebrates. Journal of Experimental Biology, 217(Pt 7), 1024–1039.

    Article  CAS  Google Scholar 

  • Linsenmeier, R.A., Aksenov, D.P., Faber, H.M., Makar, P., Wyrwicz, A.M. (2016). Spontaneous fluctuations of po2 in the rabbit somatosensory cortex. Advances in Experimental Medicine and Biology, 876, 311–317.

    Article  CAS  Google Scholar 

  • Manil, J., Bourgain, R.H., Van Waeyenberge, M., Colin, F., Blockeel, E., De Mey, B., et al. (1984). Properties of the spontaneous fluctuations in cortical oxygen pressure. Advances in Experimental Medicine and Biology, 169, 231–239.

    Article  CAS  Google Scholar 

  • Masamoto, K., & Tanishita, K. (2009). Oxygen transport in brain tissue. Journal of Biomechanical Engineering, 131(7), 074002.

    Article  Google Scholar 

  • Mateo, C., Knutsen, P.M., Tsai, P.S., Shih, A.Y., Kleinfeld, D. (2017). Entrainment of arteriole vasomotor fluctuations by neural activity is a basis of blood-oxygenation-level-dependent r̈esting-statec̈onnectivity. Neuron, 96(4), 936–948 e933.

    Article  CAS  Google Scholar 

  • Millar, L.J., Shi, L., Hoerder-Suabedissen, A., Molnar, Z. (2017). Neonatal hypoxia ischaemia: mechanisms, models, and therapeutic challenges. Frontiers in Cellular Neuroscience, 11, 78.

    Article  Google Scholar 

  • Munnich, A., & Kuchenmeister, U. (2014). Causes, diagnosis and therapy of common diseases in neonatal puppies in the first days of life: cornerstones of practical approach. Reproduction in Domestic Animals, 49 Supply, 2, 64–74.

    Article  Google Scholar 

  • Muoio, V., Persson, P.B., Sendeski, M.M. (2014). The neurovascular unit - concept review. Acta Physiologica (Oxf), 210(4), 790– 798.

    Article  CAS  Google Scholar 

  • Ndubuizu, O., & LaManna, J.C. (2007). Brain tissue oxygen concentration measurements. Antioxidants and Redox Signaling, 9(8), 1207–1219.

    Article  CAS  Google Scholar 

  • Pantoni, L., Fierini, F., Poggesi, A. (2014). Thrombolysis in acute stroke patients with cerebral small vessel disease. Thrombolysis in Acute Stroke Patients with Cerebral Small Vessel Disease, 37(1), 5–13.

    CAS  Google Scholar 

  • Popel, A.S. (1989). Theory of oxygen transport to tissue. Critical Reviews in Biomedical Engineering, 17(3), 257–321.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma, R., Llinas, R.H., Urrutia, V., Marsh, E.B. (2018). Collaterals predict outcome regardless of time last known normal. Journal of Stroke and Cerebrovascular Diseases, 27(4), 971–977.

    Article  Google Scholar 

  • Singer, D. (1999). Neonatal tolerance to hypoxia: a comparative-physiological approach. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 123(3), 221– 234.

    Article  CAS  Google Scholar 

  • Suwa, K. (1992). Analysis of oxygen transport to the brain when two or more parameters are affected simultaneously. Journal of Anesthesia, 6(3), 297–304.

    Article  CAS  Google Scholar 

  • Tsai, A.G., & Intaglietta, M. (1993). Evidence of flowmotion induced changes in local tissue oxygenation. International Journal of Microcirculation: Clinical and Experimental, 12(1), 75–88.

    CAS  Google Scholar 

  • Willie, C.K., Tzeng, Y.C., Fisher, J.A., Ainslie, P.N. (2014). Integrative regulation of human brain blood flow. The Journal of Physiology, 592(5), 841–859.

    Article  CAS  Google Scholar 

  • Zeiger, S.L., McKenzie, J.R., Stankowski, J.N., Martin, J.A., Cliffel, D.E., McLaughlin, B. (2010). Neuron specific metabolic adaptations following multi-day exposures to oxygen glucose deprivation. Biochimica et Biophysica Acta, 1802(11), 1095–1104.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Engineering Sciences and Applied Mathematics, Northwestern University, Evanston, IL, 60208, USA

    Evan D. Doubovikov

  2. Department of Radiology, NorthShore University HealthSystem, 1033 University Place, Suite 100, Evanston, IL, 60201, USA

    Daniil P. Aksenov

Authors
  1. Evan D. Doubovikov
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  2. Daniil P. Aksenov
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Correspondence to Daniil P. Aksenov.

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Action Editor: Barry Richmond

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This work was supported by National Institute of General Medical Sciences (R01 GM112715) and National Institute of Neurological Disorders and Stroke (R01 NS107383).

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Doubovikov, E.D., Aksenov, D.P. Oscillations and concentration dynamics of brain tissue oxygen in neonates and adults. J Comput Neurosci 48, 21–26 (2020). https://doi.org/10.1007/s10827-019-00736-2

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  • DOI: https://doi.org/10.1007/s10827-019-00736-2

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