Human cerebral autoregulation before, during and after spaceflight

Exposure to microgravity alters the distribution of body fluids and the degree of distension of cranial blood vessels, and these changes in turn may provoke structural remodelling and altered cerebral autoregulation. Impaired cerebral autoregulation has been documented following weightlessness simulated by head‐down bed rest in humans, and is proposed as a mechanism responsible for postspaceflight orthostatic intolerance. In this study, we tested the hypothesis that spaceflight impairs cerebral autoregulation. We studied six astronauts ∼72 and 23 days before, after 1 and 2 weeks in space (n= 4), on landing day, and 1 day after the 16 day Neurolab space shuttle mission. Beat‐by‐beat changes of photoplethysmographic mean arterial pressure and transcranial Doppler middle cerebral artery blood flow velocity were measured during 5 min of spontaneous breathing, 30 mmHg lower body suction to simulate standing in space, and 10 min of 60 deg passive upright tilt on Earth. Dynamic cerebral autoregulation was quantified by analysis of the transfer function between spontaneous changes of mean arterial pressure and cerebral artery blood flow velocity, in the very low‐ (0.02–0.07 Hz), low‐ (0.07–0.20 Hz) and high‐frequency (0.20–0.35 Hz) ranges. Resting middle cerebral artery blood flow velocity did not change significantly from preflight values during or after spaceflight. Reductions of cerebral blood flow velocity during lower body suction were significant before spaceflight (P < 0.05, repeated measures ANOVA), but not during or after spaceflight. Absolute and percentage reductions of mean (±s.e.m.) cerebral blood flow velocity after 10 min upright tilt were smaller after than before spaceflight (absolute, −4 ± 3 cm s−1 after versus−14 ± 3 cm s−1 before, P= 0.001; and percentage, −8.0 ± 4.8% after versus−24.8 ± 4.4% before, P < 0.05), consistent with improved rather than impaired cerebral blood flow regulation. Low‐frequency gain decreased significantly (P < 0.05) by 26, 23 and 27% after 1 and 2 weeks in space and on landing day, respectively, compared with preflight values, which is also consistent with improved autoregulation. We conclude that human cerebral autoregulation is preserved, and possibly even improved, by short‐duration spaceflight.

[1]  J. Shoemaker,et al.  Cerebral vasoconstriction precedes orthostatic intolerance after parabolic flight , 2000, Brain Research Bulletin.

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

[3]  C. Ray,et al.  Sympathetic and vascular responses to head-down neck flexion in humans. , 1997, The American journal of physiology.

[4]  M. Delp,et al.  Effects of hindlimb unloading on rat cerebral, splenic, and mesenteric resistance artery morphology. , 1999, Journal of applied physiology.

[5]  M. L. Riedesel,et al.  Simultaneous cerebrovascular and cardiovascular responses during presyncope. , 1995, Stroke.

[6]  Rune Aaslid,et al.  Comparison of Flow and Velocity During Dynamic Autoregulation Testing in Humans , 1994, Stroke.

[7]  G. W. Hoffler,et al.  Apollo space crew cardiovascular evaluations. , 1974, Aerospace medicine.

[8]  C. G. Blomqvist,et al.  Regulation of muscle sympathetic nerve activity after bed rest deconditioning. , 2001, American journal of physiology. Heart and circulatory physiology.

[9]  B. Levine,et al.  Spontaneous fluctuations in cerebral blood flow: insights from extended-duration recordings in humans. , 2000, American Journal of Physiology. Heart and Circulatory Physiology.

[10]  R. Panerai,et al.  Linear and nonlinear analysis of human dynamic cerebral autoregulation. , 1999, American journal of physiology. Heart and circulatory physiology.

[11]  B. Levine,et al.  Effects of head-down-tilt bed rest on cerebral hemodynamics during orthostatic stress. , 1997, Journal of applied physiology.

[12]  Irina Alferova,et al.  Adaptation of the left heart, cerebral and femoral arteries, and jugular and femoral veins during short- and long-term head-down tilt and spaceflights , 2001, European Journal of Applied Physiology.

[13]  Cole A. Giller,et al.  Cerebral Versus Systemic Hemodynamics During Graded Orthostatic Stress in Humans , 1994, Circulation.

[14]  L R Young,et al.  Tactile influences on astronaut visual spatial orientation: human neurovestibular studies on SLS-2. , 1996, Journal of applied physiology.

[15]  R. Furlan,et al.  Effects of standing on cerebrovascular resistance in patients with idiopathic orthostatic intolerance. , 1999, The American journal of medicine.

[16]  J. Handa,et al.  Effect of contrast material, hypercapnia, hyperventilation, hypertonic glucose and papaverine on the diameter of the cerebral arteries. Angiographic determination in man. , 1967, Investigative radiology.

[17]  T. E. Brown,et al.  Subnormal norepinephrine release relates to presyncope in astronauts after spaceflight. , 1996, Journal of applied physiology.

[18]  S. Ogawa,et al.  The Effect of Sevoflurane on Dynamic Cerebral Blood Flow Autoregulation Assessed by Spectral and Transfer Function Analysis , 2006, Anesthesia and analgesia.

[19]  T. Wein,et al.  Cerebrovascular and cardiovascular measurements during neurally mediated syncope induced by head-up tilt. , 1997, Stroke.

[20]  C. G. Blomqvist,et al.  Noninvasive determination of cardiac output by a modified acetylene rebreathing procedure utilizing mass spectrometer measurements. , 1977, Aviation, space, and environmental medicine.

[21]  B. Levine,et al.  Autonomic Neural Control of Dynamic Cerebral Autoregulation in Humans , 2002, Circulation.

[22]  C. Giller,et al.  Cerebral arterial diameters during changes in blood pressure and carbon dioxide during craniotomy. , 1993, Neurosurgery.

[23]  A P Blaber,et al.  Transfer function analysis of cerebral autoregulation dynamics in autonomic failure patients. , 1997, Stroke.

[24]  I. Alferova,et al.  Cardiac, arterial and venous adaptation to weightlessness during 6-month MIR spaceflights with and without thigh cuffs (bracelets) , 2000, European Journal of Applied Physiology.

[25]  A. Maillet,et al.  Changes in kinetics of cerebral auto‐regulation with head‐down bed rest , 2002, Clinical physiology and functional imaging.

[26]  B. Levine,et al.  Deterioration of cerebral autoregulation during orthostatic stress: insights from the frequency domain. , 1998, Journal of applied physiology.

[27]  J B Charles,et al.  Spaceflight alters autonomic regulation of arterial pressure in humans. , 1994, Journal of applied physiology.

[28]  Jay C Buckey,et al.  Human muscle sympathetic nerve activity and plasma noradrenaline kinetics in space , 2002, The Journal of physiology.

[29]  Yoshiki Sugiyama,et al.  Influence of microgravity on astronauts' sympathetic and vagal responses to Valsalva's manoeuvre , 2002, The Journal of physiology.

[30]  O B Paulson,et al.  Cerebral autoregulation. , 1984, Stroke.

[31]  D. Michikami,et al.  Increased vasomotor sympathetic nerve activity and decreased plasma nitric oxide release after head-down bed rest in humans: disappearance of correlation between vasoconstrictor and vasodilator , 2000, Neuroscience Letters.

[32]  B K Rutt,et al.  MRI measures of middle cerebral artery diameter in conscious humans during simulated orthostasis. , 2000, Stroke.

[33]  Arthur S Slutsky,et al.  Normocapnia improves cerebral oxygen delivery during conventional oxygen therapy in carbon monoxide-exposed research subjects. , 2002, Annals of emergency medicine.

[34]  C. Gharib,et al.  Effects of 28-day head-down tilt with and without countermeasures on lower body negative pressure responses. , 1995, Aviation Space and Environmental Medicine.

[35]  T. Driscoll,et al.  Control of red blood cell mass in spaceflight. , 1996, Journal of applied physiology.

[36]  B D Levine,et al.  Effect of head-down-tilt bed rest and hypovolemia on dynamic regulation of heart rate and blood pressure. , 2000, American journal of physiology. Regulatory, integrative and comparative physiology.

[37]  J P Bagian,et al.  Cerebral Blood Flow: Comparison of Ground‐Based and Spaceflight Data and Correlation with Space Adaptation Syndrome , 1991, Journal of clinical pharmacology.

[38]  J B Charles,et al.  Cardiovascular deconditioning during space flight and the use of saline as a countermeasure to orthostatic intolerance. , 1985, Aviation, space, and environmental medicine.

[39]  C A Giller The frequency-dependent behavior of cerebral autoregulation. , 1990, Neurosurgery.

[40]  E. Länsimies,et al.  Regional cerebral perfusion in cardiovascular reflex syncope , 1997, European Journal of Nuclear Medicine.

[41]  P. Novak,et al.  Autoregulation of cerebral blood flow in orthostatic hypotension. , 1998, Stroke.

[42]  C. G. Blomqvist,et al.  Orthostatic intolerance after spaceflight. , 1996, Journal of applied physiology.

[43]  L. Lipsitz,et al.  Dynamic regulation of middle cerebral artery blood flow velocity in aging and hypertension. , 2000, Stroke.

[44]  R. Aaslid,et al.  Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. , 1982, Journal of neurosurgery.

[45]  C. G. Blomqvist,et al.  Repeated plasma volume determination with the Evans Blue dye dilution technique: the method and a computer program. , 1991, Computers in biology and medicine.

[46]  C. Giller,et al.  A New Method for Fixation of Probes for Transcranial Doppler Ultrasound , 1997, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[47]  Rong Zhang,et al.  Human muscle sympathetic neural and haemodynamic responses to tilt following spaceflight , 2002, The Journal of physiology.

[48]  John F. Potter,et al.  Cerebral Autoregulatory Responses to Head-Up Tilt in Normal Subjects and Patients With Recurrent Vasovagal Syncope , 2001, Circulation.

[49]  B. Levine,et al.  Transfer function analysis of dynamic cerebral autoregulation in humans. , 1998, American journal of physiology. Heart and circulatory physiology.

[50]  Rong Zhang,et al.  Cardiovascular and sympathetic neural responses to handgrip and cold pressor stimuli in humans before, during and after spaceflight , 2002, The Journal of physiology.

[51]  O B Paulson,et al.  Transcranial Doppler Is Valid for Determination of the Lower Limit of Cerebral Blood Flow Autoregulation , 1994, Stroke.

[52]  B D Levine,et al.  Cardiac atrophy after bed-rest deconditioning: a nonneural mechanism for orthostatic intolerance. , 1997, Circulation.

[53]  B. Levine,et al.  Reduced baroreflex control of heart period after bed rest is normalized by acute plasma volume restoration. , 2004, American journal of physiology. Regulatory, integrative and comparative physiology.