Frontal cerebral cortex blood flow, oxygen delivery and oxygenation during normoxic and hypoxic exercise in athletes

Non‐technical summary  Exercise capacity is limited at high altitude where hypoxia (i.e. decreased amount of inspired oxygen resulting in decreased oxygen in the blood) is present, but it is unknown whether a reduction in the oxygen delivered to the brain constitutes the signal to the brain to prematurely terminate exercise. We show that during hypoxic exercise equivalent to exercise at ∼4000 m above sea‐level, the oxygen delivered to the brain during intense exercise is ∼60% less than that delivered to the brain at comparable exercise intensity at sea‐level. These results show that reduction in the oxygen delivered to the brain could constitute the signal to limit maximal exercise capacity in hypoxia, and help us understand better why exercise capacity is limited at high altitude. Moreover, a plausible mechanism of exercise limitation in patients who present decreased oxygen in the blood during exercise due to pulmonary and/or cardiac disease is revealed.

[1]  Marco Ferrari,et al.  Muscle oxygenation and pulmonary gas exchange kinetics during cycling exercise on-transitions in humans. , 2003, Journal of applied physiology.

[2]  N. Secher,et al.  Dynamic cerebral autoregulation during exhaustive exercise in humans. , 2005, American journal of physiology. Heart and circulatory physiology.

[3]  P. Raven,et al.  Dynamic blood pressure control and middle cerebral artery mean blood velocity variability at rest and during exercise in humans , 2007, Acta physiologica.

[4]  P. Ainslie,et al.  Alterations in cerebral dynamics at high altitude following partial acclimatization in humans: wakefulness and sleep. , 2007, Journal of applied physiology.

[5]  P. Rasmussen,et al.  Cerebral hypoperfusion during hypoxic exercise following two different hypoxic exposures: independence from changes in dynamic autoregulation and reactivity. , 2008, American journal of physiology. Regulatory, integrative and comparative physiology.

[6]  M Czosnyka,et al.  Thresholds for Hypoxic Cerebral Vasodilation in Volunteers , 1997, Anesthesia and analgesia.

[7]  M. Kjaer,et al.  Muscle Perfusion and Metabolic Heterogeneity: Insights from Noninvasive Imaging Techniques , 2006, Exercise and sport sciences reviews.

[8]  H B Nielsen,et al.  Cerebral desaturation during exercise reversed by O2 supplementation. , 1999, American journal of physiology. Heart and circulatory physiology.

[9]  Peter Niederer,et al.  Noninvasive measurement of regional cerebral blood flow and regional cerebral blood volume by near-infrared spectroscopy and indocyanine green dye dilution , 2003, NeuroImage.

[10]  B Chance,et al.  Recovery from exercise-induced desaturation in the quadriceps muscles of elite competitive rowers. , 1992, The American journal of physiology.

[11]  S. Ogoh,et al.  Interaction between the ventilatory and cerebrovascular responses to hypo‐ and hypercapnia at rest and during exercise , 2008, The Journal of physiology.

[12]  F. Yamazaki,et al.  Modulation of arterial baroreflex control of heart rate by skin cooling and heating in humans. , 2000, Journal of applied physiology.

[13]  Tomoko Sadamoto,et al.  Different blood flow responses to dynamic exercise between internal carotid and vertebral arteries in women. , 2010, Journal of applied physiology.

[14]  J. V. van Lieshout,et al.  Cerebral blood flow and metabolism during exercise: implications for fatigue. , 2008, Journal of applied physiology.

[15]  P. Raven,et al.  The effect of changes in cardiac output on middle cerebral artery mean blood velocity at rest and during exercise , 2005, The Journal of physiology.

[16]  Swapan Mookerjee,et al.  Cerebral oxygenation declines at exercise intensities above the respiratory compensation threshold , 2007, Respiratory Physiology & Neurobiology.

[17]  Robert Boushel,et al.  Cardiac output and leg and arm blood flow during incremental exercise to exhaustion on the cycle ergometer. , 2007, Journal of applied physiology.

[18]  Use of near infrared spectroscopy to estimate cerebral blood flow in conscious and anaesthetized adult subjects. , 1996 .

[19]  S. Zakynthinos,et al.  Contribution of respiratory muscle blood flow to exercise‐induced diaphragmatic fatigue in trained cyclists , 2008, The Journal of physiology.

[20]  Respiratory, cerebrovascular and pressor responses to acute hypoxia: dependency on PET(CO2). , 2004, Advances in experimental medicine and biology.

[21]  G. Hempelmann,et al.  [Cerebral oximetry by infrared spectroscopy in comparison with continuous measurement of oxygen saturation of the jugular vein bulb in interventions of the internal carotid artery]. , 1995, VASA. Zeitschrift fur Gefasskrankheiten.

[22]  D. Delpy,et al.  The effect of scalp ischaemia on measurement of cerebral blood volume by near-infrared spectroscopy , 1996, Physiological measurement.

[23]  Albert Gjedde,et al.  Capillary-Oxygenation-Level-Dependent Near-Infrared Spectrometry in Frontal Lobe of Humans , 2007, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[24]  Philip N. Ainslie,et al.  Cardiorespiratory and cerebrovascular responses to hyperoxic and hypoxic rebreathing: Effects of acclimatization to high altitude , 2008, Respiratory Physiology & Neurobiology.

[25]  Fumio Yamazaki,et al.  Different vascular responses in glabrous and nonglabrous skin with increasing core temperature during exercise , 2006, European Journal of Applied Physiology.

[26]  Sungho Tak,et al.  Quantitative Analysis of Hemodynamic and Metabolic Changes in Subcortical Vascular Dementia Using Simultaneous Near-infrared Spectroscopy and Fmri Measurements , 2022 .

[27]  N. Secher,et al.  Bicarbonate attenuates arterial desaturation during maximal exercise in humans. , 2002, Journal of applied physiology.

[28]  D. Paterson,et al.  Effects of prior heavy-intensity exercise on pulmonary O2 uptake and muscle deoxygenation kinetics in young and older adult humans. , 2004, Journal of applied physiology.

[29]  Akira Koike,et al.  Cerebral oxygenation during exercise in cardiac patients. , 2004, Chest.

[30]  W. Kuebler,et al.  Intercostal muscle blood flow limitation in athletes during maximal exercise , 2009, The Journal of physiology.

[31]  Egill Rostrup,et al.  Cerebral hemodynamics measured with simultaneous PET and near-infrared spectroscopy in humans , 2002, Brain Research.

[32]  A. Subudhi,et al.  Cerebrovascular responses to incremental exercise during hypobaric hypoxia: effect of oxygenation on maximal performance. , 2008, American journal of physiology. Heart and circulatory physiology.

[33]  D. Paterson,et al.  Adaptation of pulmonary O2 uptake kinetics and muscle deoxygenation at the onset of heavy-intensity exercise in young and older adults. , 2005, Journal of applied physiology.

[34]  S. Kety,et al.  THE NITROUS OXIDE METHOD FOR THE QUANTITATIVE DETERMINATION OF CEREBRAL BLOOD FLOW IN MAN: THEORY, PROCEDURE AND NORMAL VALUES. , 1948, The Journal of clinical investigation.

[35]  S. Arridge,et al.  Experimentally measured optical pathlengths for the adult head, calf and forearm and the head of the newborn infant as a function of inter optode spacing. , 1992, Advances in experimental medicine and biology.

[36]  Takuya Osada,et al.  Brain and central haemodynamics and oxygenation during maximal exercise in humans , 2004, The Journal of physiology.

[37]  L. Friberg,et al.  Cerebral effects of scalp cooling and extracerebral contribution to calculated blood flow values using the intravenous 133Xe technique. , 1986, Scandinavian journal of clinical and laboratory investigation.

[38]  J. Tobias,et al.  Cerebral oxygenation monitoring: near-infrared spectroscopy , 2006, Expert review of medical devices.

[39]  N. Secher,et al.  Middle cerebral artery flow velocity and blood flow during exercise and muscle ischemia in humans. , 1992, Journal of applied physiology.

[40]  K. Pattinson,et al.  Effect of exercise on cerebral perfusion in humans at high altitude. , 2005, Journal of applied physiology.

[41]  Ravi S. Menon,et al.  Transient hemodynamics during a breath hold challenge in a two part functional imaging study with simultaneous near-infrared spectroscopy in adult humans , 2003, NeuroImage.

[42]  L. Nybo,et al.  Enhanced cerebral CO2 reactivity during strenuous exercise in man , 2006, European Journal of Applied Physiology.

[43]  N. Secher,et al.  Maintained cerebral and skeletal muscle oxygenation during maximal exercise in patients with liver cirrhosis. , 2005, Journal of hepatology.

[44]  Nicolas Caesar Petersen,et al.  Reduced muscle activation during exercise related to brain oxygenation and metabolism in humans , 2010, The Journal of physiology.

[45]  A. Subudhi,et al.  Frontal and motor cortex oxygenation during maximal exercise in normoxia and hypoxia. , 2009, Journal of applied physiology.

[46]  K Ide,et al.  Cerebral metabolic response to submaximal exercise. , 1999, Journal of applied physiology.

[47]  Andrew C. Dimmen,et al.  Effects of acute hypoxia on cerebral and muscle oxygenation during incremental exercise. , 2007, Journal of applied physiology.

[48]  D. Poole,et al.  Effects of hyperoxia on maximal leg O2 supply and utilization in men. , 1993, Journal of applied physiology.

[49]  D. Delpy,et al.  Optical pathlength measurements on adult head, calf and forearm and the head of the newborn infant using phase resolved optical spectroscopy. , 1995, Physics in medicine and biology.

[50]  S. Carroll,et al.  Emergence of the verification phase procedure for confirming ‘true’V̇O2max , 2009, Scandinavian journal of medicine & science in sports.

[51]  N. Secher,et al.  Regional cerebral artery mean flow velocity and blood flow during dynamic exercise in humans. , 1992, Journal of applied physiology.

[52]  B. Saltin,et al.  Determinants of maximal oxygen uptake in severe acute hypoxia. , 2003, American journal of physiology. Regulatory, integrative and comparative physiology.

[53]  P. W. Mccormick,et al.  Intracerebral penetration of infrared light. Technical note. , 1992, Journal of neurosurgery.

[54]  N. Lassen,et al.  Middle cerebral artery blood velocity and cerebral blood flow and O2 uptake during dynamic exercise. , 1993, Journal of applied physiology.

[55]  P. Dow Estimations of cardiac output and central blood volume by dye dilution. , 1956, Physiological reviews.

[56]  D. Paterson,et al.  Relationship between Pulmonary O2 Uptake Kinetics and Muscle Deoxygenation during Moderate‐Intensity Exercise. , 2003, Journal of applied physiology.

[57]  W. Kuebler,et al.  Noninvasive Measurement of Regional Cerebral Blood Flow by Near-Infrared Spectroscopy and Indocyanine Green , 1998, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[58]  N. Secher,et al.  Near-infrared spectroscopy determined brain and muscle oxygenation during exercise with normal and resistive breathing. , 2001, Acta physiologica Scandinavica.

[59]  H. Langberg,et al.  Regional blood flow during exercise in humans measured by near-infrared spectroscopy and indocyanine green. , 2000, Journal of applied physiology.

[60]  Shigehiko Ogoh,et al.  Cerebral blood flow during exercise: mechanisms of regulation. , 2009, Journal of applied physiology.

[61]  Control of skin blood flow during exercise: thermal and nonthermal factors. , 1979, Journal of applied physiology: respiratory, environmental and exercise physiology.

[62]  S. Arridge,et al.  Estimation of optical pathlength through tissue from direct time of flight measurement , 1988 .

[63]  Shigehiko Ogoh,et al.  The distribution of blood flow in the carotid and vertebral arteries during dynamic exercise in humans , 2011, The Journal of physiology.

[64]  R. Naeije,et al.  Relationship of middle cerebral artery blood flow velocity to intensity during dynamic exercise in normal subjects , 2004, European Journal of Applied Physiology and Occupational Physiology.

[65]  N. Secher,et al.  Cerebral oxygenation during exercise in patients with terminal lung disease. , 2002, Chest.

[66]  M. Poulin,et al.  Assessments of flow by transcranial Doppler ultrasound in the middle cerebral artery during exercise in humans. , 1999, Journal of applied physiology.

[67]  J. Mitchell,et al.  Cerebral blood flow during submaximal and maximal dynamic exercise in humans. , 1989, Journal of applied physiology.

[68]  J A Stolwijk,et al.  Skin blood flow and sweating changes following exercise training and heat acclimation. , 1977, Journal of applied physiology: respiratory, environmental and exercise physiology.