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

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.

CBF oscillations induced by trigeminal nerve stimulation protect the pericontusional penumbra in traumatic brain injury complicated by hemorrhagic shock

“…These studies suggest that such oscillations may represent an “on–off” feedback mechanism and provide a pump-like effect leading to improved tissue perfusion via temporary increases in the pressure gradient down the vascular tree. This hypothesis has been further supported by computational simulation, wherein low-frequency CBF oscillations supply higher amplitudes of localized oxygen delivery relative to oscillations at a higher frequency 16 . Furthermore, pulsatile blood flow can increase shear stress on the vessel endothelium which stimulates the release of nitric oxide and inhibits endothelin production, thus increasing oxygen delivery to brain tissue 18 , 21 .…”

“…Specifically, pulsatile blood flow can increase shear stress on the vessel endothelium which stimulates the release of nitric oxide and inhibits endothelin production, thus increasing oxygen delivery to brain tissue 21 . Furthermore, these oscillatory patterns represent an “on–off” feedback mechanism that serves to maintain tissue perfusion in the setting of oxygen deprivation with computational models suggesting that low frequency oscillatory flow is beneficial to tissue oxygenation 15 , 16 . It might be that brief, rhythmic increases in CBF during the oscillatory stimulus (Fig.…”

“…Several studies, from clinical findings to computational models, indicate significant effect of low-frequency oscillatory patterns of CBF to maintain tissue perfusion in the setting of oxygen deprivation 15 , 16 . While the precise mechanism of these oscillatory patterns is not well understood, it might be linked to multiple protective mechanisms for compromised cerebrovascular regulation and cerebral oxygenation.…”

Behavior and Regional Cortical BOLD Signal Fluctuations Are Altered in Adult Rabbits After Neonatal Volatile Anesthetic Exposure

“…On the other hand, ALFF also can be related to non-neuronal vasomotion. The dominant frequency of brain tissue oxygen oscillations (BTOO), which are attributed to vasomotion at the level of arterioles (Hudetz et al, 1998;Aalkjaer et al, 2011;Mateo et al, 2017), has been shown to change during development (Doubovikov and Aksenov, 2020). The dominant frequency of BTOO is around 1-2 cycles/min (0.0167-0.0333 Hz) in neonates (Aksenov et al, 2018) and approximately 10 cycles/min (0.167 Hz) in adults (Linsenmeier et al, 2016).…”

Normal Development of Local Neurovascular Interactions and the Diagnostic Value of Resting State Functional MRI in Neurovascular Deficiency Based on the Example of Neonatal Anesthesia Exposure

“…In adults, it is characterized by a 10 cycles per minute (cpm) dominant power frequency ( 35 , 36 ), whereas underdeveloped vasomotion has a dominant frequency below 3 cpm ( 37 ). This shift in frequency of vasomotion and corresponding brain tissue oxygen oscillations represents a normal development and is needed to prevent localized hypoxia depending on the oxygen demand by developing neurons and neuronal networks ( 36 ). If neonatal anesthesia affects the development of the glutamatergic system, GABAergic system, or normal formation of astrocytes, the development of vasomotion can be affected as well.…”