scholarly journals Cerebral oxygenation during locomotion is modulated by respiration

2019 ◽  
Vol 10 (1) ◽  
Author(s):  
Qingguang Zhang ◽  
Morgane Roche ◽  
Kyle W. Gheres ◽  
Emmanuelle Chaigneau ◽  
Ravi T. Kedarasetti ◽  
...  

AbstractIn the brain, increased neural activity is correlated with increases of cerebral blood flow and tissue oxygenation. However, how cerebral oxygen dynamics are controlled in the behaving animal remains unclear. We investigated to what extent cerebral oxygenation varies during locomotion. We measured oxygen levels in the cortex of awake, head-fixed mice during locomotion using polarography, spectroscopy, and two-photon phosphorescence lifetime measurements of oxygen sensors. We find that locomotion significantly and globally increases cerebral oxygenation, specifically in areas involved in locomotion, as well as in the frontal cortex and the olfactory bulb. The oxygenation increase persists when neural activity and functional hyperemia are blocked, occurred both in the tissue and in arteries feeding the brain, and is tightly correlated with respiration rate and the phase of respiration cycle. Thus, breathing rate is a key modulator of cerebral oxygenation and should be monitored during hemodynamic imaging, such as in BOLD fMRI.

2019 ◽  
Author(s):  
Qingguang Zhang ◽  
Morgane Roche ◽  
Kyle W. Gheres ◽  
Emmanuelle Chaigneau ◽  
William D. Haselden ◽  
...  

AbstractIn the brain, increased neural activity is correlated with an increase of cerebral blood flow and increased tissue oxygenation. However, how cerebral oxygen dynamics are controlled in the behaving animals remains unclear. Here, we investigated to what extent the cerebral oxygenation varies during natural behaviors that change the whole-body homeostasis, specifically exercise. We measured oxygen levels in the cortex of awake, head-fixed mice during locomotion using polarography, spectroscopy, and two-photon phosphorescence lifetime measurements of oxygen sensors. We found that locomotion significantly and globally increases cerebral oxygenation, specifically in areas involved in locomotion, as well as in the frontal cortex and the olfactory bulb. The oxygenation increase persisted when neural activity and functional hyperemia were blocked, occurred both in the tissue and in arteries feeding the brain, and was tightly correlated with respiration rate and the phase of respiration cycle. Thus, respiration provides a dynamic pathway for modulating cerebral oxygenation.


2020 ◽  
Author(s):  
Qingguang Zhang ◽  
Kyle W. Gheres ◽  
Patrick J. Drew

AbstractThe concentration of oxygen in the brain spontaneously fluctuates, and the power distribution in these fluctuations has 1/f-like dynamics. Though these oscillations have been interpreted as being driven by neural activity, the origins of these 1/f-like oscillations is not well understood. Here, to gain insight of the origin of the 1/f-like oxygen fluctuations, we investigated the dynamics of tissue oxygenation and neural activity in awake behaving mice. We found that oxygen signal recorded from the cortex of mice had 1/f-like spectra. However, band-limited power in the local field potential, did not show corresponding 1/f-like fluctuations. When local neural activity was suppressed, the 1/f-like fluctuations in oxygen concentration persisted. Two-photon measurements of erythrocyte spacing fluctuations (‘stalls’) and mathematical modelling show that stochastic fluctuations in erythrocyte flow and stalling could underlie 1/f-like dynamics in oxygenation. These results show discrete nature of erythrocytes and their irregular flow, rather than neural activity, could drive 1/f-like fluctuations in tissue oxygenation.


PLoS Biology ◽  
2021 ◽  
Vol 19 (7) ◽  
pp. e3001298
Author(s):  
Qingguang Zhang ◽  
Kyle W. Gheres ◽  
Patrick J. Drew

The concentration of oxygen in the brain spontaneously fluctuates, and the distribution of power in these fluctuations has a 1/f-like spectra, where the power present at low frequencies of the power spectrum is orders of magnitude higher than at higher frequencies. Though these oscillations have been interpreted as being driven by neural activity, the origin of these 1/f-like oscillations is not well understood. Here, to gain insight of the origin of the 1/f-like oxygen fluctuations, we investigated the dynamics of tissue oxygenation and neural activity in awake behaving mice. We found that oxygen signal recorded from the cortex of mice had 1/f-like spectra. However, band-limited power in the local field potential did not show corresponding 1/f-like fluctuations. When local neural activity was suppressed, the 1/f-like fluctuations in oxygen concentration persisted. Two-photon measurements of erythrocyte spacing fluctuations and mathematical modeling show that stochastic fluctuations in erythrocyte flow could underlie 1/f-like dynamics in oxygenation. These results suggest that the discrete nature of erythrocytes and their irregular flow, rather than fluctuations in neural activity, could drive 1/f-like fluctuations in tissue oxygenation.


2005 ◽  
Vol 25 (7) ◽  
pp. 911-918 ◽  
Author(s):  
Hernan Gonzalez ◽  
Christian J Hunter ◽  
Laura Bennet ◽  
Gordon G Power ◽  
Alistair J Gunn

After exposure to asphyxia, infants may develop both prolonged, clinically evident seizures and shorter, clinically silent seizures; however, their effect on cerebral tissue oxygenation is unclear. We therefore examined the hypothesis that the increase in oxygen delivery during postasphyxial seizures might be insufficient to meet the needs of increased metabolism, thus causing a fall in tissue oxygenation, in unanesthetized near-term fetal sheep in utero (gestational age 125 ± 1 days). Fetuses were administered an infusion of the specific adenosine A1 receptor antagonist 8-cyclopentyl-1,3-dipropylxanthine, followed by 10 mins of asphyxia induced by complete umbilical cord occlusion. The fetuses then recovered for 3 days. Sixty-one episodes of electrophysiologically defined seizures were identified in five fetuses. Tissue PO2 (tPO2) did not change significantly during short seizures (<3.5 mins), 5.2 ± 0.2 versus baseline 5.6 ± 0.1 mm Hg (NS), but fell to 2.2 ± 0.2 mm Hg during seizures lasting more than 3.5 mins ( P<0.001). During prolonged seizures, cortical blood flow did not begin to increase until tPO2 had begun to fall, and then rose more slowly than the increase in metabolism, with a widening of the brain to blood temperature gradient. In conclusion, in the immature brain, during prolonged, but not short seizures, there is a transient mismatch between cerebral blood flow and metabolism leading to significant cerebral deoxygenation.


2019 ◽  
Author(s):  
Jianglai Wu ◽  
Yajie Liang ◽  
Shuo Chen ◽  
Ching-Lung Hsu ◽  
Mariya Chavarha ◽  
...  

Understanding information processing in the brain requires us to monitor neural activity in vivo at high spatiotemporal resolution. Using an ultrafast two-photon fluorescence microscope (2PFM) empowered by all-optical laser scanning, we imaged neural activity in vivo at up to 3,000 frames per second and submicron spatial resolution. This ultrafast imaging method enabled monitoring of both supra- and sub-threshold electrical activity down to 345 μm below the brain surface in head fixed awake mice.


2004 ◽  
Vol 97 (5) ◽  
pp. 1962-1969 ◽  
Author(s):  
Egbert G. Mik ◽  
Ton G. van Leeuwen ◽  
Nicolaas J. Raat ◽  
Can Ince

This study describes the use of two-photon excitation phosphorescence lifetime measurements for quantitative oxygen determination in vivo. Doubling the excitation wavelength of Pd-porphyrin from visible light to the infrared allows for deeper tissue penetration and a more precise and confined selection of the excitation volume due to the nonlinear two-photon effect. By using a focused laser beam from a 1,064-nm Q-switched laser, providing 10-ns pulses of 10 mJ, albumin-bound Pd-porphyrin was effectively excited and oxygen-dependent decay of phosphorescence was observed. In vitro calibration of phosphorescence lifetime vs. oxygen tension was performed. The obtained calibration constants were kq = 356 Torr−1·s−1 (quenching constant) and τ0 = 550 μs (lifetime at zero-oxygen conditions) at 37°C. The phosphorescence intensity showed a squared dependency to the excitation intensity, typical for two-photon excitation. In vivo demonstration of two-photon excitation phosphorescence lifetime measurements is shown by step-wise Po2 measurements through the cortex of rat kidney. It is concluded that quantitative oxygen measurements can be made, both in vitro and in vivo , using two-photon excitation oxygen-dependent quenching of phosphorescence. The use of two-photon excitation has the potential to lead to new applications of the phosphorescence lifetime technique, e.g., noninvasive oxygen scanning in tissue at high spatial resolution. To our knowledge, this is the first report in which two-photon excitation is used in the setting of oxygen-dependent quenching of phosphorescence lifetime measurements.


2009 ◽  
Vol 297 (3) ◽  
pp. R867-R876 ◽  
Author(s):  
T. Seifert ◽  
P. Rasmussen ◽  
P. Brassard ◽  
P. H. Homann ◽  
M. Wissenberg ◽  
...  

Endurance training improves muscular and cardiovascular fitness, but the effect on cerebral oxygenation and metabolism remains unknown. We hypothesized that 3 mo of endurance training would reduce cerebral carbohydrate uptake with maintained cerebral oxygenation during submaximal exercise. Healthy overweight males were included in a randomized, controlled study (training: n = 10; control: n = 7). Arterial and internal jugular venous catheterization was used to determine concentration differences for oxygen, glucose, and lactate across the brain and the oxygen-carbohydrate index [molar uptake of oxygen/(glucose + ½ lactate); OCI], changes in mitochondrial oxygen tension (ΔPMitoO2) and the cerebral metabolic rate of oxygen (CMRO2) were calculated. For all subjects, resting OCI was higher at the 3-mo follow-up (6.3 ± 1.3 compared with 4.7 ± 0.9 at baseline, mean ± SD; P < 0.05) and coincided with a lower plasma epinephrine concentration ( P < 0.05). Cerebral adaptations to endurance training manifested when exercising at 70% of maximal oxygen uptake (∼211 W). Before training, both OCI (3.9 ± 0.9) and ΔPMitoO2 (−22 mmHg) decreased ( P < 0.05), whereas CMRO2 increased by 79 ± 53 micromol·100·g−1 min−1 ( P < 0.05). At the 3-mo follow-up, OCI (4.9 ± 1.0) and ΔPMitoO2 (−7 ± 13 mmHg) did not decrease significantly from rest and when compared with values before training ( P < 0.05), CMRO2 did not increase. This study demonstrates that endurance training attenuates the cerebral metabolic response to submaximal exercise, as reflected in a lower carbohydrate uptake and maintaind cerebral oxygenation.


2017 ◽  
Vol 24 (3) ◽  
pp. 277-293 ◽  
Author(s):  
Selen Atasoy ◽  
Gustavo Deco ◽  
Morten L. Kringelbach ◽  
Joel Pearson

A fundamental characteristic of spontaneous brain activity is coherent oscillations covering a wide range of frequencies. Interestingly, these temporal oscillations are highly correlated among spatially distributed cortical areas forming structured correlation patterns known as the resting state networks, although the brain is never truly at “rest.” Here, we introduce the concept of harmonic brain modes—fundamental building blocks of complex spatiotemporal patterns of neural activity. We define these elementary harmonic brain modes as harmonic modes of structural connectivity; that is, connectome harmonics, yielding fully synchronous neural activity patterns with different frequency oscillations emerging on and constrained by the particular structure of the brain. Hence, this particular definition implicitly links the hitherto poorly understood dimensions of space and time in brain dynamics and its underlying anatomy. Further we show how harmonic brain modes can explain the relationship between neurophysiological, temporal, and network-level changes in the brain across different mental states ( wakefulness, sleep, anesthesia, psychedelic). Notably, when decoded as activation of connectome harmonics, spatial and temporal characteristics of neural activity naturally emerge from the interplay between excitation and inhibition and this critical relation fits the spatial, temporal, and neurophysiological changes associated with different mental states. Thus, the introduced framework of harmonic brain modes not only establishes a relation between the spatial structure of correlation patterns and temporal oscillations (linking space and time in brain dynamics), but also enables a new dimension of tools for understanding fundamental principles underlying brain dynamics in different states of consciousness.


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