Sympathetic control of the brain circulation: Appreciating the complexities to better understand the controversy

Autonomic Neuroscience: Basic and Clinical

Volumn 207, Issue , 2017, Pages 37-47

  Brassard, Patrice ^a,b   Tymko, Michael M ^c   Ainslie, Philip N ^c  

^a UNIVERSITÉ LAVAL   (Canada)

^b LAVAL UNIVERSITY   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Brain circulation; Cerebral blood flow regulation; Neural control; Sympathetic nerve activity

Indexed keywords

ADRENERGIC SYSTEM; BRAIN BLOOD FLOW; BRAIN BLOOD VOLUME; BRAIN CIRCULATION; HEMODYNAMICS; OXYGENATION; PRIORITY JOURNAL; REVIEW; THERMAL DIFFUSION; ANIMAL; BLOOD PRESSURE; BRAIN; HUMAN; PATHOPHYSIOLOGY; PHYSIOLOGY; SLEEP; VASCULARIZATION;

ANIMALS; BLOOD PRESSURE; BRAIN; CEREBROVASCULAR CIRCULATION; HUMANS; SLEEP; SYMPATHETIC NERVOUS SYSTEM;

EID: 85019110408     PISSN: 15660702     EISSN: 18727484     Source Type: Journal    
DOI: 10.1016/j.autneu.2017.05.003     Document Type: Review

References (109)

1. Aaslid, R., Blaha, M., Sviri, G., Douville, C.M., Newell, D.W., Asymmetric dynamic cerebral autoregulatory response to cyclic stimuli. Stroke 38 (2007), 1465–1469.
2. Ainslie, P.N., Have a safe night: intimate protection against cerebral hyperperfusion during REM sleep. J. Appl. Physiol. (1985) 106 (2009), 1031–1033.
3. Ainslie, P.N., Brassard, P., Why is the neural control of cerebral autoregulation so controversial?. F1000Prime Rep., 6, 2014, 14.
4. Ainslie, P.N., Duffin, J., Integration of cerebrovascular CO2 reactivity and chemoreflex control of breathing: mechanisms of regulation, measurement, and interpretation. Am. J. Phys. Regul. Integr. Comp. Phys. 296 (2009), R1473–R1495.
5. Ainslie, P.N., Hoiland, R.L., Transcranial Doppler ultrasound: valid, invalid, or both?. J. Appl. Physiol. (1985) 117 (2014), 1081–1083.
6. Ainslie, P.N., Lucas, S.J., Fan, J.L., Thomas, K.N., Cotter, J.D., Tzeng, Y.C., Burgess, K.R., Influence of sympathoexcitation at high altitude on cerebrovascular function and ventilatory control in humans. J. Appl. Physiol.(1985) 113 (2012), 1058–1067.
7. Ainslie, P.N., Shaw, A.D., Smith, K.J., Willie, C.K., Ikeda, K., Graham, J., Macleod, D.B., Stability of cerebral metabolism and substrate availability in humans during hypoxia and hyperoxia. Clin. Sci. (Lond.), 2013.
8. Bleys, R.L., Cowen, T., Innervation of cerebral blood vessels: morphology, plasticity, age-related, and Alzheimer's disease-related neurodegeneration. Microsc. Res. Tech. 53 (2001), 106–118.
9. Brassard, P., Seifert, T., Wissenberg, M., Jensen, P.M., Hansen, C.K., Secher, N.H., Phenylephrine decreases frontal lobe oxygenation at rest but not during moderately intense exercise. J. Appl. Physiol. 108 (2010), 1472–1478.
10. Brassard, P., Ferland-Dutil, H., Smirl, J.D., Paquette, M., Le Blanc, O., Malenfant, S., Ainslie, P.N., Evidence for hysteresis in the cerebral pressure-flow relationship in healthy men. Am. J. Physiol. Heart Circ. Physiol. 312 (2017), H701–H704.
11. Brown, C.M., Dutsch, M., Hecht, M.J., Neundorfer, B., Hilz, M.J., Assessment of cerebrovascular and cardiovascular responses to lower body negative pressure as a test of cerebral autoregulation. J. Neurol. Sci. 208 (2003), 71–78.
12. Busija, D.W., Leffler, C.W., Eicosanoid synthesis elicited by norepinephrine in piglet parietal cortex. Brain Res. 403 (1987), 243–248.
13. Cassaglia, P.A., Griffiths, R.I., Walker, A.M., Sympathetic nerve activity in the superior cervical ganglia increases in response to imposed increases in arterial pressure. Am. J. Phys. Regul. Integr. Comp. Phys. 294 (2008), R1255–R1261.
14. Cassaglia, P.A., Griffiths, R.I., Walker, A.M., Cerebral sympathetic nerve activity has a major regulatory role in the cerebral circulation in REM sleep. J. Appl. Physiol. (1985) 106 (2009), 1050–1056.
15. Charkoudian, N., Wallin, B.G., Sympathetic neural activity to the cardiovascular system: integrator of systemic physiology and interindividual characteristics. Compr. Physiol. 4 (2014), 825–850.
16. Coverdale, N.S., Gati, J.S., Opalevych, O., Perrotta, A., Shoemaker, J.K., Cerebral blood flow velocity underestimates cerebral blood flow during modest hypercapnia and hypocapnia. J. Appl. Physiol. 117:1985 (2014), 1090–1096.
17. Dacey, R.G. Jr., Duling, B.R., Effect of norepinephrine on penetrating arterioles of rat cerebral cortex. Am. J. Phys. 246 (1984), H380–H385.
18. Deegan, B.M., Cooke, J.P., Lyons, D., Olaighin, G., Serrador, J.M., Cerebral autoregulation in the vertebral and middle cerebral arteries during combine head upright tilt and lower body negative pressure in healthy humans. Conference Proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Eng. Med. Biol. Soc., 2010, 2505–2508 (Conference 2010).
19. Donnelly, J., Budohoski, K.P., Smielewski, P., Czosnyka, M., Regulation of the cerebral circulation: bedside assessment and clinical implications. Crit. Care, 20, 2016, 129.
20. Edvinsson, L., Neurogenic mechanisms in the cerebrovascular bed. Autonomic nerves, amine receptors and their effects on cerebral blood flow. Acta Physiol. Scand. Suppl. 427 (1975), 1–35.
21. Edvinsson, L., Owman, C., Sjoberg, N.O., Autonomic nerves, mast cells, and amine receptors in human brain vessels. A histochemical and pharmacological study. Brain Res. 115 (1976), 377–393.
22. Edvinsson, L., MacKenzie, E.T., McCulloch, J., Cerebral Blood Flow and Metabolism. 1993, Raven Press, New York.
23. Fernandes, I.A., Mattos, J.D., Campos, M.O., Machado, A.C., Rocha, M.P., Rocha, N.G., Vianna, L.C., Nobrega, A.C., Selective alpha1-adrenergic blockade disturbs the regional distribution of cerebral blood flow during static handgrip exercise. Am. J. Physiol. Heart Circ. Physiol. 310 (2016), H1541–H1548.
24. Fog, M., Cerebral circulation II. Reaction of pial arteries to increase in blood pressure. Arch. Neurol. Psychiatr., 41, 1939, 9.
25. Fog, M., Cerebral circulation. the reaction of pial arteries to a fall in blood pressure. Arch. Neurol. Psychiatr., 37, 1939, 14.
26. Giovannitti, J.A. Jr., Thoms, S.M., Crawford, J.J., Alpha-2 adrenergic receptor agonists: a review of current clinical applications. Anesth. Prog. 62 (2015), 31–39.
27. Goadsby, P.J., Autonomic nervous system control of the cerebral circulation. Handb. Clin. Neurol. 117 (2013), 193–201.
28. Gross, P.M., Marcus, M.L., Heistad, D.D., Regional distribution of cerebral blood flow during exercise in dogs. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 48 (1980), 213–217.
29. Gross, P.M., Harper, A.M., Teasdale, G.M., Interaction of histamine with noradrenergic constrictory mechanisms in cat cerebral arteries and veins. Can. J. Physiol. Pharmacol. 61 (1983), 756–763.
30. Guo, H., Tierney, N., Schaller, F., Raven, P.B., Smith, S.A., Shi, X., Cerebral autoregulation is preserved during orthostatic stress superimposed with systemic hypotension. J. Appl. Physiol. (1985) 100 (2006), 1785–1792.
31. Hamner, J.W., Tan, C.O., Relative contributions of sympathetic, cholinergic, and myogenic mechanisms to cerebral autoregulation. Stroke 45 (2014), 1771–1777.
32. Hamner, J.W., Tan, C.O., Lee, K., Cohen, M.A., Taylor, J.A., Sympathetic control of the cerebral vasculature in humans. Stroke 41 (2010), 102–109.
33. Hansen, J., Sander, M., Sympathetic neural overactivity in healthy humans after prolonged exposure to hypobaric hypoxia. J. Physiol. 546 (2003), 921–929.
34. Harmel, M.H., Hafkenschiel, J.H. et al., The effect of bilateral stellate ganglion block on the cerebral circulation in normotensive and hypertensive patients. J. Clin. Invest. 28 (1949), 415–418.
35. Haubrich, C., Wendt, A., Diehl, R.R., Klotzsch, C., Dynamic autoregulation testing in the posterior cerebral artery. Stroke 35 (2004), 848–852.
36. Heistad, D.D., Marcus, M.L., Gross, P.M., Effects of sympathetic nerves on cerebral vessels in dog, cat, and monkey. Am. J. Phys. 235 (1978), H544–H552.
37. Hoiland, R.L., Ainslie, P.N., CrossTalk proposal: the middle cerebral artery diameter does change during alterations in arterial blood gases and blood pressure. J. Physiol. 594 (2016), 4073–4075.
38. Hoiland, R.L., Ainslie, P.N., Wildfong, K.W., Smith, K.J., Bain, A.R., Willie, C.K., Foster, G., Monteleone, B., Day, T.A., Indomethacin-induced impairment of regional cerebrovascular reactivity: implications for respiratory control. J. Physiol. 593 (2015), 1291–1306.
39. Ide, K., Boushel, R., Sorensen, H.M., Fernandes, A., Cai, Y., Pott, F., Secher, N.H., Middle cerebral artery blood velocity during exercise with beta-1 adrenergic and unilateral stellate ganglion blockade in humans. Acta Physiol. Scand. 170 (2000), 33–38.
40. Jordan, J., Shannon, J.R., Diedrich, A., Black, B., Costa, F., Robertson, D., Biaggioni, I., Interaction of carbon dioxide and sympathetic nervous system activity in the regulation of cerebral perfusion in humans. Hypertension 36 (2000), 383–388.
41. Kang, C.K., Oh, S.T., Chung, R.K., Lee, H., Park, C.A., Kim, Y.B., Yoo, J.H., Kim, D.Y., Cho, Z.H., Effect of stellate ganglion block on the cerebrovascular system: magnetic resonance angiography study. Anesthesiology 113 (2010), 936–944.
42. Kay, V.L., Rickards, C.A., The role of cerebral oxygenation and regional cerebral blood flow on tolerance to central hypovolemia. Am. J. Phys. Regul. Integr. Comp. Phys. 310 (2016), R375–R383.
43. Kellawan, M.J., Harrell, J.W., Roldan-Alzate, A., Wieben, O., Schrage, W.G., Regional hypoxic cerebral vasodilation facilitated by diameter changes primarily in anterior versus posterior circulation. J. Cereb. Blood Flow Metab., 2016.
44. Kim, Y.S., Seifert, T., Brassard, P., Rasmussen, P., Vaag, A., Nielsen, H.B., Secher, N.H., van Lieshout, J.J., Impaired cerebral blood flow and oxygenation during exercise in type 2 diabetic patients. Phys. Rep., 3, 2015.
45. Kimmerly, D.S., Tutungi, E., Wilson, T.D., Serrador, J.M., Gelb, A.W., Hughson, R.L., Shoemaker, J.K., Circulating norepinephrine and cerebrovascular control in conscious humans. Clin. Physiol. Funct. Imaging 23 (2003), 314–319.
46. Kiowski, W., Hulthen, U.L., Ritz, R., Buhler, F.R., Alpha 2 adrenoceptor-mediated vasoconstriction of arteries. Clin. Pharmacol. Ther. 34 (1983), 565–569.
47. Kobayashi, S., Tsukahara, S., Sugita, K., Nagata, T., Adrenergic and cholinergic innervation of rat cerebral arteries. Consecutive demonstration on whole mount preparations. Histochemistry 70 (1981), 129–138.
48. ter Laan, M., van Dijk, J.M.C., Elting, J.W.J., Staal, M.J., Absalom, A.R., Sympathetic regulation of cerebral blood flow in humans: a review. Br. J. Anaesth. 111 (2013), 361–367.
49. Lee, H.W., Caldwell, J.E., Dodson, B., Talke, P., Howley, J., The effect of clonidine on cerebral blood flow velocity, carbon dioxide cerebral vasoreactivity, and response to increased arterial pressure in human volunteers. Anesthesiology 87 (1997), 553–558.
50. Levine, B.D., Giller, C.A., Lane, L.D., Buckey, J.C., Blomqvist, C.G., Cerebral versus systemic hemodynamics during graded orthostatic stress in humans. Circulation 90 (1994), 298–306.
51. Lewis, N.C., Ainslie, P.N., Atkinson, G., Jones, H., Grant, E.J., Lucas, S.J., Initial orthostatic hypotension and cerebral blood flow regulation: effect of alpha1-adrenoreceptor activity. Am. J. Phys. Regul. Integr. Comp. Phys. 304 (2013), R147–R154.
52. Lewis, N.C., Bain, A.R., MacLeod, D.B., Wildfong, K.W., Smith, K.J., Willie, C.K., Sanders, M.L., Numan, T., Morrison, S.A., Foster, G.E., Stewart, J.M., Ainslie, P.N., Impact of hypocapnia and cerebral perfusion on orthostatic tolerance. J. Physiol. 592 (2014), 5203–5219.
53. Lewis, N.C., Messinger, L., Monteleone, B., Ainslie, P.N., Effect of acute hypoxia on regional cerebral blood flow: effect of sympathetic nerve activity. J. Appl. Physiol. (1985) 116 (2014), 1189–1196.
54. Lewis, N.C., Smith, K.J., Bain, A.R., Wildfong, K.W., Numan, T., Ainslie, P.N., Impact of transient hypotension on regional cerebral blood flow in humans. Clin. Sci. (Lond.) 129 (2015), 169–178.
55. van Lieshout, J.J., Secher, N.H., Point:Counterpoint: sympathetic activity does/does not influence cerebral blood flow. Point: sympathetic activity does influence cerebral blood flow. J. Appl. Physiol. 105 (2008), 1364–1366.
56. van Lieshout, J.J., Pott, F., Madsen, P.L., van Goudoever, J., Secher, N.H., Muscle tensing during standing: effects on cerebral tissue oxygenation and cerebral artery blood velocity. Stroke 32 (2001), 1546–1551.
57. Liu, J., Tseng, B.Y., Khan, M.A., Tarumi, T., Hill, C., Mirshams, N., Hodics, T.M., Hynan, L.S., Zhang, R., Individual variability of cerebral autoregulation, posterior cerebral circulation and white matter hyperintensity. J. Physiol. 594 (2016), 3141–3155.
58. Maekawa, T., Cho, S., Fukusaki, M., Shibata, O., Sumikawa, K., Effects of clonidine on human middle cerebral artery flow velocity and cerebrovascular CO2 response during sevoflurane anesthesia. J. Neurosurg. Anesthesiol. 11 (1999), 173–177.
59. Mayhan, W.G., Responses of cerebral arterioles to activation of beta-adrenergic receptors during diabetes mellitus. Stroke 25 (1994), 141–146.
60. Meng, L., Hou, W., Chui, J., Han, R., Gelb, A.W., Cardiac output and cerebral blood flow: the integrated regulation of brain perfusion in adult humans. Anesthesiology 123 (2015), 1198–1208.
61. Mitchell, D.A., Lambert, G., Secher, N.H., Raven, P.B., van Lieshout, J., Esler, M.D., Jugular venous overflow of noradrenaline from the brain: a neurochemical indicator of cerebrovascular sympathetic nerve activity in humans. J. Physiol. 587 (2009), 2589–2597.
62. Muller, M.J., Bosy-Westphal, A., Kutzner, D., Heller, M., Metabolically active components of fat-free mass and resting energy expenditure in humans: recent lessons from imaging technologies. Obes. Rev. 3 (2002), 113–122.
63. Novak, V., Spies, J.M., Novak, P., McPhee, B.R., Rummans, T.A., Low, P.A., Hypocapnia and cerebral hypoperfusion in orthostatic intolerance. Stroke 29 (1998), 1876–1881.
64. Numan, T., Bain, A.R., Hoiland, R.L., Smirl, J.D., Lewis, N.C., Ainslie, P.N., Static autoregulation in humans: a review and reanalysis. Med. Eng. Phys. 6 (2014), 1487–1495.
65. Ogawa, Y., Iwasaki, K., Aoki, K., Shibata, S., Kato, J., Ogawa, S., Central hypervolemia with hemodilution impairs dynamic cerebral autoregulation. Anesth. Analg. 105 (2007), 1389–1396 (table of contents).
66. Ogawa, Y., Iwasaki, K., Aoki, K., Kojima, W., Kato, J., Ogawa, S., Dexmedetomidine weakens dynamic cerebral autoregulation as assessed by transfer function analysis and the thigh cuff method. Anesthesiology 109 (2008), 642–650.
67. Ogoh, S., Brothers, R.M., Barnes, Q., Eubank, W.L., Hawkins, M.N., Purkayastha, S., A, O.Y., Raven, P.B., The effect of changes in cardiac output on middle cerebral artery mean blood velocity at rest and during exercise. J. Physiol. 569 (2005), 697–704.
68. Ogoh, S., Dalsgaard, M.K., Secher, N.H., Raven, P.B., Dynamic blood pressure control and middle cerebral artery mean blood velocity variability at rest and during exercise in humans. Acta Physiol (Oxford) 191 (2007), 3–14.
69. Ogoh, S., Brothers, R.M., Eubank, W.L., Raven, P.B., Autonomic neural control of the cerebral vasculature: acute hypotension. Stroke 39 (2008), 1979–1987.
70. Ogoh, S., Sato, K., Okazaki, K., Miyamoto, T., Hirasawa, A., Sadamoto, T., Shibasaki, M., Blood flow in internal carotid and vertebral arteries during graded lower body negative pressure in humans. Exp. Physiol. 100 (2015), 259–266.
71. Ohta, S., Hadeishi, H., Suzuki, M., Effect of stellate ganglion block on cerebral blood flow in normoxemic and hyperoxemic states. J. Neurosurg. Anesthesiol. 2 (1990), 272–279.
72. Peebles, K.C., Richards, A.M., Celi, L., McGrattan, K., Murrell, C.J., Ainslie, P.N., Human cerebral arteriovenous vasoactive exchange during alterations in arterial blood gases. J. Appl. Physiol.(1985) 105 (2008), 1060–1068.
73. Peebles, K.C., Ball, O.G., MacRae, B.A., Horsman, H.M., Tzeng, Y.C., Sympathetic regulation of the human cerebrovascular response to carbon dioxide. J. Appl. Physiol.(1985) 113 (2012), 700–706.
74. Purkayastha, S., Saxena, A., Eubank, W.L., Hoxha, B., Raven, P.B., Alpha1-adrenergic receptor control of the cerebral vasculature in humans at rest and during exercise. Exp. Physiol. 98 (2013), 451–461.
75. Rajan, V., Varghese, B., van Leeuwen, T.G., Steenbergen, W., Review of methodological developments in laser Doppler flowmetry. Lasers Med. Sci. 24 (2009), 269–283.
76. Remensnyder, J.P., Mitchell, J.H., Sarnoff, S.J., Functional sympatholysis during muscular activity. Observations on influence of carotid sinus on oxygen uptake. Circ. Res. 11 (1962), 370–380.
77. Rohlwink, U.K., Figaji, A.A., Methods of monitoring brain oxygenation. Childs Nerv. Syst. 26 (2010), 453–464.
78. Rosendorff, C., Mitchell, G., Mitchell, D., Adrenergic innervation affecting local cerebral blood flow. Owman, C., Edvinsson, L., (eds.) Neurogenic Control of Brain Circulation: Werner-Gren Center International Symposium Series, vol. 30, 1977, Pergamon, Oxford, 455–464.
79. Sandor, P., Nervous control of the cerebrovascular system: doubts and facts. Neurochem. Int. 35 (1999), 237–259.
80. Sato, K., Fisher, J.P., Seifert, T., Overgaard, M., Secher, N.H., Ogoh, S., Blood flow in internal carotid and vertebral arteries during orthostatic stress. Exp. Physiol. 97 (2012), 1272–1280.
81. Scheinberg, P., Cerebral blood flow in vascular disease of the brain; with observations on the effects of stellate ganglion block. Am. J. Med. 8 (1950), 139–147.
82. Schmidt, B., Klingelhofer, J., Perkes, I., Czosnyka, M., Cerebral autoregulatory response depends on the direction of change in perfusion pressure. J. Neurotrauma 26 (2009), 651–656.
83. Seifert, T., Rasmussen, P., Secher, N.H., Nielsen, H.B., Cerebral oxygenation decreases during exercise in humans with beta-adrenergic blockade. Acta Physiol (Oxford) 196 (2009), 295–302.
84. Sercombe, R., Lacombe, P., Aubineau, P., Mamo, H., Pinard, E., Reynier-Rebuffel, A.M., Seylaz, J., Is there an active mechanism limiting the influence of the sympathetic system on the cerebral vascular bed? Evidence for vasomotor escape from sympathetic stimulation in the rabbit. Brain Res. 164 (1979), 81–102.
85. Sercombe, R., Hardebo, J.E., Kahrstrom, J., Seylaz, J., Amine-induced responses of pial and penetrating cerebral arteries: evidence for heterogeneous responses. J. Cereb. Blood Flow Metab. 10 (1990), 808–818.
86. Serrador, J.M., Picot, P.A., Rutt, B.K., Shoemaker, J.K., Bondar, R.L., MRI measures of middle cerebral artery diameter in conscious humans during simulated orthostasis. Stroke 31 (2000), 1672–1678.
87. Serrador, J.M., Hughson, R.L., Kowalchuk, J.M., Bondar, R.L., Gelb, A.W., Cerebral blood flow during orthostasis: role of arterial CO2. Am. J. Phys. Regul. Integr. Comp. Phys. 290 (2006), R1087–R1093.
88. Shenkin, H.A., Cervical sympathectomy on patients with occlusive cerebrovascular disease. Arch. Surg. 98 (1969), 317–320.
89. Shenkin, H.A., Cabieses, F., Van Den Noordt, G., The effect of bilateral stellectomy upon the cerebral circulation of man. J. Clin. Invest. 30 (1951), 90–93.
90. Smith, K.J., MacLeod, D., Willie, C.K., Lewis, N.C., Hoiland, R.L., Ikeda, K., Tymko, M.M., Donnelly, J., Day, T.A., MacLeod, N., Lucas, S.J., Ainslie, P.N., Influence of high altitude on cerebral blood flow and fuel utilization during exercise and recovery. J. Physiol. 592 (2014), 5507–5527.
91. Strandgaard, S., Sigurdsson, S.T., Point:Counterpoint: Sympathetic activity does/does not influence cerebral blood flow. Counterpoint: Sympathetic nerve activity does not influence cerebral blood flow. J. Appl. Physiol. 105 (2008), 1366–1367 (discussion 1367–1368).
92. Suzuki, J., Iwabuchi, T., Hori, S., Cervical sympathectomy for cerebral vasospasm after aneurysm rupture. Neurol. Med. Chir. (Tokyo) 15:Pt 1 (1975), 41–50.
93. Tsukahara, T., Taniguchi, T., Shimohama, S., Fujiwara, M., Handa, H., Characterization of beta adrenergic receptors in human cerebral arteries and alteration of the receptors after subarachnoid hemorrhage. Stroke 17 (1986), 202–207.
94. Tymko, M.M., Rickards, C.A., Skow, R.J., Ingram-Cotton, N.C., Howatt, M.K., Day, T.A., The effects of superimposed tilt and lower body negative pressure on anterior and posterior cerebral circulations. Phys. Rep., 2016, 4.
95. Tzeng, Y.C., Willie, C.K., Atkinson, G., Lucas, S.J., Wong, A., Ainslie, P.N., Cerebrovascular regulation during transient hypotension and hypertension in humans. Hypertension 56 (2010), 268–273.
96. Vajkoczy, P., Roth, H., Horn, P., Lucke, T., Thome, C., Hubner, U., Martin, G.T., Zappletal, C., Klar, E., Schilling, L., Schmiedek, P., Continuous monitoring of regional cerebral blood flow: experimental and clinical validation of a novel thermal diffusion microprobe. J. Neurosurg. 93 (2000), 265–274.
97. Valdueza, J.M., Draganski, B., Hoffmann, O., Dirnagl, U., Einhaupl, K.M., Analysis of CO2 vasomotor reactivity and vessel diameter changes by simultaneous venous and arterial Doppler recordings. Stroke 30 (1999), 81–86.
98. Van Lieshout, J.J., Wieling, W., Karemaker, J.M., Secher, N.H., Syncope, cerebral perfusion, and oxygenation. J. Appl. Physiol. (1985) 94 (2003), 833–848.
99. Verbree, J., Bronzwaer, A.S., Ghariq, E., Versluis, M.J., Daemen, M.J., van Buchem, M.A., Dahan, A., van Lieshout, J.J., van Osch, M.J., Assessment of middle cerebral artery diameter during hypocapnia and hypercapnia in humans using ultra-high-field MRI. J. Appl. Physiol. (1985) 117 (2014), 1084–1089.
100. Verbree, J., Bronzwaer, A., van Buchem, M.A., Daemen, M., van Lieshout, J.J., van Osch, M., Middle cerebral artery diameter changes during rhythmic handgrip exercise in humans. J. Cereb. Blood Flow Metab., 2016.
101. Wagerle, L.C., Kumar, S.P., Delivoria-Papadopoulos, M., Effect of sympathetic nerve stimulation on cerebral blood flow in newborn piglets. Pediatr. Res. 20 (1986), 131–135.
102. Wagerle, L.C., Kurth, C.D., Roth, R.A., Sympathetic reactivity of cerebral arteries in developing fetal lamb and adult sheep. Am. J. Phys. 258 (1990), H1432–H1438.
103. Willie, C.K., Colino, F.L., Bailey, D.M., Tzeng, Y.C., Binsted, G., Jones, L.W., Haykowsky, M.J., Bellapart, J., Ogoh, S., Smith, K.J., Smirl, J.D., Day, T.A., Lucas, S.J., Eller, L.K., Ainslie, P.N., Utility of transcranial Doppler ultrasound for the integrative assessment of cerebrovascular function. J. Neurosci. Methods 196 (2011), 221–237.
104. Willie, C.K., Tzeng, Y.C., Fisher, J.A., Ainslie, P.N., Integrative regulation of human brain blood flow. J. Physiol. 592 (2014), 841–859.
105. Wintermark, M., Sesay, M., Barbier, E., Borbely, K., Dillon, W.P., Eastwood, J.D., Glenn, T.C., Grandin, C.B., Pedraza, S., Soustiel, J.F., Nariai, T., Zaharchuk, G., Caille, J.M., Dousset, V., Yonas, H., Comparative overview of brain perfusion imaging techniques. Stroke 36 (2005), e83–e99.
106. Zhang, R., Levine, B.D., Autonomic ganglionic blockade does not prevent reduction in cerebral blood flow velocity during orthostasis in humans. Stroke 38 (2007), 1238–1244.
107. Zhang, R., Zuckerman, J.H., Iwasaki, K., Wilson, T.E., Crandall, C.G., Levine, B.D., Autonomic neural control of dynamic cerebral autoregulation in humans. Circulation 106 (2002), 1814–1820.
108. Zhang, R., Crandall, C.G., Levine, B.D., Cerebral hemodynamics during the Valsalva maneuver: insights from ganglionic blockade. Stroke 35 (2004), 843–847.
109. Zornow, M.H., Maze, M., Dyck, J.B., Shafer, S.L., Dexmedetomidine decreases cerebral blood flow velocity in humans. J. Cereb. Blood Flow Metab. 13 (1993), 350–353.