The impact of age on cerebral perfusion, oxygenation and metabolism during exercise in humans

Journal of Physiology

Volumn 594, Issue 16, 2016, Pages 4471-4483

  Braz, Igor D ^a   Fisher, James P ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE;

ADRENERGIC ACTIVITY; AGING; ARTERIAL CARBON DIOXIDE TENSION; BLOOD PRESSURE; BRAIN BLOOD FLOW; BRAIN METABOLISM; BRAIN PERFUSION; EXERCISE; FITNESS; HEART OUTPUT; HUMAN; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; TISSUE OXYGENATION;

EID: 84982234839     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP271081     Document Type: Review

References (106)

1. Aaslid R, Markwalder TM & Nornes H (1982). Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg 57, 769–774.
2. Ainslie PN, Barach A, Murrell C, Hamlin M, Hellemans J & Ogoh S (2007). Alterations in cerebral autoregulation and cerebral blood flow velocity during acute hypoxia: rest and exercise. Am J Physiol Heart Circ Physiol 292, H976–983.
3. Ainslie PN, Cotter JD, George KP, Lucas S, Murrell C, Shave R, Thomas KN, Williams MJ & Atkinson G (2008). Elevation in cerebral blood flow velocity with aerobic fitness throughout healthy human ageing. J Physiol 586, 4005–4010.
4. 2 reactivity and chemoreflex control of breathing: mechanisms of regulation, measurement, and interpretation. Am J Physiol Regul Integr Comp Physiol 296, R1473–1495.
5. Ainslie PN & Hoiland RL (2014). Transcranial Doppler ultrasound: valid, invalid, or both? J Appl Physiol (1985) 117, 1081–1083.
6. Auer LM, Edvinsson L & Johansson BB (1983). Effect of sympathetic nerve stimulation and adrenoceptor blockade on pial arterial and venous calibre and on intracranial pressure in the cat. Acta Physiol Scand 119, 213–217.
7. Bain CA, Walters MR, Lees KR & Lumsden MA (2004). The effect of HRT on cerebral haemodynamics and cerebral vasomotor reactivity in post-menopausal women. Hum Reprod 19, 2411–2414.
8. Bill A & Linder J (1976). Sympathetic control of cerebral blood flow in acute arterial hypertension. Acta Physiol Scand 96, 114–121.
9. Blumenthal JA, Babyak MA, Moore KA, Craighead WE, Herman S, Khatri P, Waugh R, Napolitano MA, Forman LM, Appelbaum M, Doraiswamy PM & Krishnan KR (1999). Effects of exercise training on older patients with major depression. Arch Intern Med 159, 2349–2356.
10. Bolduc V, Thorin-Trescases N & Thorin E (2013). Endothelium-dependent control of cerebrovascular functions through age: exercise for healthy cerebrovascular aging. Am J Physiol Heart Circ Physiol 305, H620–633.
11. Braz ID, Scott C, Simpson LL, Springham EL, Tan BW, Balanos GM & Fisher JP (2014). Influence of muscle metaboreceptor stimulation on middle cerebral artery blood velocity in humans. Exp Physiol 99, 1478–1487.
12. Brys M, Brown CM, Marthol H, Franta R & Hilz MJ (2003). Dynamic cerebral autoregulation remains stable during physical challenge in healthy persons. Am J Physiol Heart Circ Physiol 285, H1048–1054.
13. Burgmans S, Gronenschild EH, Fandakova Y, Shing YL, van Boxtel MP, Vuurman EF, Uylings HB, Jolles J & Raz N (2011). Age differences in speed of processing are partially mediated by differences in axonal integrity. Neuroimage 55, 1287–1297.
14. Burns A & Tyrrell P (1992). Association of age with regional cerebral oxygen utilization: a positron emission tomography study. Age Ageing 21, 316–320.
15. Carter HH, Spence AL, Pugh CJ, Ainslie P, Naylor LH & Green DJ (2014). Cardiovascular responses to water immersion in humans: impact on cerebral perfusion. Am J Physiol Regul Integr Comp Physiol 306, R636–640.
16. Colcombe SJ, Erickson KI, Scalf PE, Kim JS, Prakash R, McAuley E, Elavsky S, Marquez DX, Hu L & Kramer AF (2006). Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci 61, 1166–1170.
17. Coverdale NS, Gati JS, Opalevych O, Perrotta A & Shoemaker JK (2014). Cerebral blood flow velocity underestimates cerebral blood flow during modest hypercapnia and hypocapnia. J Appl Physiol (1985) 117, 1090–1096.
18. 2/carbohydrate uptake ratio in humans. J Physiol 540, 681–689.
19. Dalsgaard MK, Nybo L, Cai Y & Secher NH (2003). Cerebral metabolism is influenced by muscle ischaemia during exercise in humans. Exp Physiol 88, 297–302.
20. Dalsgaard MK, Quistorff B, Danielsen ER, Selmer C, Vogelsang T & Secher NH (2004). A reduced cerebral metabolic ratio in exercise reflects metabolism and not accumulation of lactate within the human brain. J Physiol 554, 571–578.
21. Dinenno FA & Joyner MJ (2006). α-Adrenergic control of skeletal muscle circulation at rest and during exercise in aging humans. Microcirculation 13, 329–341.
22. Dinenno FA, Masuki S & Joyner MJ (2005). Impaired modulation of sympathetic α-adrenergic vasoconstriction in contracting forearm muscle of ageing men. J Physiol 567, 311–321.
23. Duckles SP & Krause DN (2007). Cerebrovascular effects of oestrogen: multiplicity of action. Clin Exp Pharmacol Physiol 34, 801–808.
24. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, Kim JS, Heo S, Alves H, White SM, Wojcicki TR, Mailey E, Vieira VJ, Martin SA, Pence BD, Woods JA, McAuley E & Kramer AF (2011). Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci USA 108, 3017–3022.
25. Fisher JP, Hartwich D, Seifert T, Olesen ND, McNulty CL, Nielsen HB, van Lieshout JJ & Secher NH (2013). Cerebral perfusion, oxygenation and metabolism during exercise in young and elderly individuals. J Physiol 591, 1859–1870.
26. Fisher JP, Ogoh S, Young CN, Raven PB & Fadel PJ (2008). Regulation of middle cerebral artery blood velocity during dynamic exercise in humans: influence of aging. J Appl Physiol (1985) 105, 266–273.
27. Fleg JL, O'Connor F, Gerstenblith G, Becker LC, Clulow J, Schulman SP & Lakatta EG (1995). Impact of age on the cardiovascular response to dynamic upright exercise in healthy men and women. J Appl Physiol (1985) 78, 890–900.
28. Floyd TF, Clark JM, Gelfand R, Detre JA, Ratcliffe S, Guvakov D, Lambertsen CJ & Eckenhoff RG (2003). Independent cerebral vasoconstrictive effects of hyperoxia and accompanying arterial hypocapnia at 1 ATA. J Appl Physiol (1985) 95, 2453–2461.
29. Flück D, Braz ID, Keiser S, Huppin F, Haider T, Hilty M, Fisher JP & Lundby C (2014). Age, aerobic fitness and cerebral perfusion during exercise: role of carbon dioxide. Am J Physiol Heart Circ Physiol 307, H515–523.
30. Fox PT & Raichle ME (1986). Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc Natl Acad Sci USA 83, 1140–1144.
31. Hagberg JM, Allen WK, Seals DR, Hurley BF, Ehsani AA & Holloszy JO (1985). A hemodynamic comparison of young and older endurance athletes during exercise. J Appl Physiol (1985) 58, 2041–2046.
32. Heckmann JG, Brown CM, Cheregi M, Hilz MJ & Neundorfer B (2003). Delayed cerebrovascular autoregulatory response to ergometer exercise in normotensive elderly humans. Cerebrovasc Dis 16, 423–429.
33. Hellstrom G, Fischer-Colbrie W, Wahlgren NG & Jogestrand T (1996). Carotid artery blood flow and middle cerebral artery blood flow velocity during physical exercise. J Appl Physiol (1985) 81, 413–418.
34. Hiura M, Nariai T, Ishii K, Sakata M, Oda K, Toyohara J & Ishiwata K (2014). Changes in cerebral blood flow during steady-state cycling exercise: a study using oxygen-15-labeled water with PET. J Cereb Blood Flow Metab 34, 389–396.
35. Hoedt-Rasmussen K (1965). Regional cerebral flow in man measured externally following intra-arterial administration of 85-Kr or 133-Xe dissolved in saline. Acta Neurol Scand Suppl 14, 65–68.
36. Ide K, Boushel R, Sorensen HM, Fernandes A, Cai Y, Pott F & Secher NH (2000a). Middle cerebral artery blood velocity during exercise with β-1 adrenergic and unilateral stellate ganglion blockade in humans. Acta Physiol Scand 170, 33–38.
37. Ide K, Gullov AL, Pott F, Van Lieshout JJ, Koefoed BG, Petersen P & Secher NH (1999). Middle cerebral artery blood velocity during exercise in patients with atrial fibrillation. Clin Physiol 19, 284–289.
38. 2 uptake in human brain during recovery from maximal exercise. J Physiol 522, 159–164.
39. Ido Y, Chang K, Woolsey TA & Williamson JR (2001). NADH: sensor of blood flow need in brain, muscle, and other tissues. FASEB J 15, 1419–1421.
40. Jagust W (2013). Vulnerable neural systems and the borderland of brain aging and neurodegeneration. Neuron 77, 219–234.
41. 2 in exercise. J Appl Physiol Respir Environ Exerc Physiol 47, 954–960.
42. Jorgensen LG, Perko G & Secher NH (1992). Regional cerebral artery mean flow velocity and blood flow during dynamic exercise in humans. J Appl Physiol (1985) 73, 1825–1830.
43. Kety SS (1956). Human cerebral blood flow and oxygen consumption as related to aging. J Chronic Dis 3, 478–486.
44. Kety SS & Schmidt CF (1946). The effects of active and passive hyperventilation on cerebral blood flow, cerebral oxygen consumption, cardiac output, and blood pressure of normal young men. J Clin Invest 25, 107–119.
45. Kety SS & Schmidt CF (1948a). The effects of altered arterial tensions of carbon dioxide and oxygen on cerebral blood flow and cerebral oxygen consumption of normal young men. J Clin Invest 27, 484–492.
46. Kety SS & Schmidt CF (1948b). The nitrous oxide method for the quantitative determination of cerebral blood flow in man: theory, procedure and normal values. J Clin Invest 27, 476–483.
47. Kleinerman J & Sancetta SM (1955). Effect of mild steady state exercise on cerebral and general haemodynamics of normal untrained subjects. J Clin Invest 34, 1.
48. Ko KR, Ngai AC & Winn HR (1990). Role of adenosine in regulation of regional cerebral blood flow in sensory cortex. Am J Physiol Heart Circ Physiol 259, H1703–1708.
49. 2 and bicarbonate on pial vessels. Stroke 8, 358–360.
50. 2 action of cat pial arterioles. Stroke 8, 226–229.
51. Kramer AF, Hahn S, Cohen NJ, Banich MT, McAuley E, Harrison CR, Chason J, Vakil E, Bardell L, Boileau RA & Colcombe A (1999). Ageing, fitness and neurocognitive function. Nature 400, 418–419.
52. Krause DN, Duckles SP & Pelligrino DA (2006). Influence of sex steroid hormones on cerebrovascular function. J Appl Physiol (1985) 101, 1252–1261.
53. 2. J Appl Physiol 14, 966–982.
54. Leenders KL, Perani D, Lammertsma AA, Heather JD, Buckingham P, Healy MJ, Gibbs JM, Wise RJ, Hatazawa J, Herold S, et al. (1990). Cerebral blood flow, blood volume and oxygen utilization. Normal values and effect of age. Brain 113, 27–47.
55. Lindsay J, Laurin D, Verreault R, Hebert R, Helliwell B, Hill GB & McDowell I (2002). Risk factors for Alzheimer's disease: a prospective analysis from the Canadian Study of Health and Aging. Am J Epidemiol 156, 445–453.
56. Linkis P, Jorgensen LG, Olesen HL, Madsen PL, Lassen NA & Secher NH (1995). Dynamic exercise enhances regional cerebral artery mean flow velocity. J Appl Physiol (1985) 78, 12–16.
57. Lowe RF & Gilboe DD (1971). Demonstration of alpha and beta adrenergic receptors in canine cerebral vasculature. Stroke 2, 193–200.
58. Lucas SJ, Cotter JD, Brassard P & Bailey DM (2015). High-intensity interval exercise and cerebrovascular health: curiosity, cause, and consequence. J Cereb Blood Flow Metab 35, 902–911.
59. Lyngeraa TS, Pedersen LM, Mantoni T, Belhage B, Rasmussen LS, van Lieshout JJ & Pott FC (2013). Middle cerebral artery blood velocity during running. Scand J Med Sci Sports 23, e32–37.
60. Ma J, Ayata C, Huang PL, Fishman MC & Moskowitz MA (1996). Regional cerebral blood flow response to vibrissal stimulation in mice lacking type I NOS gene expression. Am J Physiol Heart Circ Physiol 270, H1085–1090.
61. 2 uptake during dynamic exercise. J Appl Physiol (1985) 74, 245–250.
62. Markel TA, Daley JC 3rd, Hogeman CS, Herr MD, Khan MH, Gray KS, Kunselman AR & Sinoway LI (2003). Aging and the exercise pressor reflex in humans. Circulation 107, 675–678.
63. Marsden KR, Haykowsky MJ, Smirl JD, Jones H, Nelson MD, Altamirano-Diaz LA, Gelinas JC, Tzeng YC, Smith KJ, Willie CK, Bailey DM & Ainslie PN (2012). Aging blunts hyperventilation-induced hypocapnia and reduction in cerebral blood flow velocity during maximal exercise. Age (Dordr) 34, 725–735.
64. Martin AJ, Friston KJ, Colebatch JG & Frackowiak RS (1991). Decreases in regional cerebral blood flow with normal aging. J Cereb Blood Flow Metab 11, 684–689.
65. Mayhan WG, Arrick DM, Sharpe GM & Sun H (2008). Age-related alterations in reactivity of cerebral arterioles: role of oxidative stress. Microcirculation 15, 225–236.
66. Micieli G, Tassorelli C, Bosone D, Cavallini A, Viotti E & Nappi G (1994). Intracerebral vascular changes induced by cold pressor test: a model of sympathetic activation. Neurol Res 16, 163–167.
67. Miller RM & Tenney SM (1956). Dead space ventilation in old age. J Appl Physiol 9, 321–327.
68. Moraine JJ, Lamotte M, Berre J, Niset G, Leduc A & Naeije R (1993). Relationship of middle cerebral artery blood flow velocity to intensity during dynamic exercise in normal subjects. Eur J Appl Physiol Occup Physiol 67, 35–38.
69. Murrell CJ, Cotter JD, Thomas KN, Lucas SJ, Williams MJ & Ainslie PN (2013). Cerebral blood flow and cerebrovascular reactivity at rest and during sub-maximal exercise: effect of age and 12-week exercise training. Age (Dordr) 35, 905–920.
70. Nugent S, Tremblay S, Chen KW, Ayutyanont N, Roontiva A, Castellano CA, Fortier M, Roy M, Courchesne-Loyer A, Bocti C, Lepage M, Turcotte E, Fulop T, Reiman EM & Cunnane SC (2014). Brain glucose and acetoacetate metabolism: a comparison of young and older adults. Neurobiol Aging 35, 1386–1395.
71. Nybo L, Nielsen B, Blomstrand E, Moller K & Secher N (2003). Neurohumoral responses during prolonged exercise in humans. J Appl Physiol (1985) 95, 1125–1131.
72. Ogoh S, Fisher JP, Young CN & Fadel PJ (2011). Impact of age on critical closing pressure of the cerebral circulation during dynamic exercise in humans. Exp Physiol 96, 417–425.
73. Olesen J (1971). Contralateral focal increase of cerebral blood flow in man during arm work. Brain 94, 635–646.
74. Olesen J (1972). The effect of intracarotid epinephrine, norepinephrine, and angiotensin on the regional cerebral blood flow in man. Neurology 22, 978–987.
75. Pantano P, Baron JC, Lebrun-Grandie P, Duquesnoy N, Bousser MG & Comar D (1984). Regional cerebral blood flow and oxygen consumption in human aging. Stroke 15, 635–641.
76. Paulson OB, Strandgaard S & Edvinsson L (1990). Cerebral autoregulation. Cerebrovasc Brain Metab Rev 2, 161–192.
77. Petit-Taboue MC, Landeau B, Desson JF, Desgranges B & Baron JC (1998). Effects of healthy aging on the regional cerebral metabolic rate of glucose assessed with statistical parametric mapping. Neuroimage 7, 176–184.
78. Pott F, Knudsen L, Nowak M, Nielsen HB, Hanel B & Secher NH (1997). Middle cerebral artery blood velocity during rowing. Acta Physiol Scand 160, 251–255.
79. Querido JS & Sheel AW (2007). Regulation of cerebral blood flow during exercise. Sports Med 37, 765–782.
80. Rasmussen P, Nielsen J, Overgaard M, Krogh-Madsen R, Gjedde A, Secher NH & Petersen NC (2010). Reduced muscle activation during exercise related to brain oxygenation and metabolism in humans. J Physiol 588, 1985–1995.
81. 2 in men. J Appl Physiol (1985) 68, 1727–1731.
82. Roebuck J (1979). When does “old age begin?”: The evolution of the English definition. J Soc Hist 12, 416–428.
83. Sacco RL, Benjamin EJ, Broderick JP, Dyken M, Easton JD, Feinberg WM, Goldstein LB, Gorelick PB, Howard G, Kittner SJ, Manolio TA, Whisnant JP & Wolf PA (1997). American Heart Association Prevention Conference. IV. Prevention and Rehabilitation of Stroke. Risk factors. Stroke 28, 1507–1517.
84. Salomon JA, Wang H, Freeman MK, Vos T, Flaxman AD, Lopez AD & Murray CJ (2012). Healthy life expectancy for 187 countries, 1990–2010: a systematic analysis for the Global Burden Disease Study 2010. Lancet 380, 2144–2162.
85. Sato K, Ogoh S, Hirasawa A, Oue A & Sadamoto T (2011). The distribution of blood flow in the carotid and vertebral arteries during dynamic exercise in humans. J Physiol 589, 2847–2856.
86. Sato K, Sadamoto T, Ueda-Sasahara C, Shibuya K, Shimizu-Okuyama S, Osada T, Kamo M, Saito M & Kagaya A (2009). Central command and the increase in middle cerebral artery blood flow velocity during static arm exercise in women. Exp Physiol 94, 1132–1138.
87. Scahill RI, Frost C, Jenkins R, Whitwell JL, Rossor MN & Fox NC (2003). A longitudinal study of brain volume changes in normal aging using serial registered magnetic resonance imaging. Arch Neurol 60, 989–994.
88. Scheinberg P, Blackburn LI, Rich M & Saslaw M (1954). Effects of vigorous physical exercise on cerebral circulation and metabolism. Am J Med 16, 549–554.
89. Schoning M, Walter J & Scheel P (1994). Estimation of cerebral blood flow through color duplex sonography of the carotid and vertebral arteries in healthy adults. Stroke 25, 17–22.
90. Secher NH, Seifert T & Van Lieshout JJ (2008). Cerebral blood flow and metabolism during exercise: implications for fatigue. J Appl Physiol (1985) 104, 306–314.
91. Seifert T, Fisher JP, Young CN, Hartwich D, Ogoh S, Raven PB, Fadel PJ & Secher NH (2010). Glycopyrrolate abolishes the exercise-induced increase in cerebral perfusion in humans. Exp Physiol 95, 1016–1025.
92. Seifert T, Rasmussen P, Brassard P, Homann PH, Wissenberg M, Nordby P, Stallknecht B, Secher NH & Nielsen HB (2009a). Cerebral oxygenation and metabolism during exercise following three months of endurance training in healthy overweight males. Am J Physiol Regul Integr Comp Physiol 297, R867–876.
93. Seifert T, Rasmussen P, Secher NH & Nielsen HB (2009b). Cerebral oxygenation decreases during exercise in humans with beta-adrenergic blockade. Acta Physiol (Oxf) 196, 295–302.
94. Siesjö B (1978). Brain energy metabolism. Ann Neurol 5, 308–308.
95. Smith D, Pernet A, Hallett WA, Bingham E, Marsden PK & Amiel SA (2003). Lactate: a preferred fuel for human brain metabolism in vivo. J Cereb Blood Flow Metab 23, 658–664.
96. Smith KJ, MacLeod D, Willie CK, Lewis NC, Hoiland RL, Ikeda K, Tymko MM, Donnelly J, Day TA, MacLeod N, Lucas SJ & Ainslie PN (2014). Influence of high altitude on cerebral blood flow and fuel utilization during exercise and recovery. J Physiol 592, 5507–5527.
97. Smith KJ, Wong LE, Eves ND, Koelwyn GJ, Smirl JD, Willie CK & Ainslie PN (2012). Regional cerebral blood flow distribution during exercise: influence of oxygen. Respir Physiol Neurobiol 184, 97–105.
98. 2 in the elderly. J Appl Physiol (1985) 79, 2086–2093.
99. Subudhi AW, Olin JT, Dimmen AC, Polaner DM, Kayser B & Roach RC (2011). Does cerebral oxygen delivery limit incremental exercise performance? J Appl Physiol (1985) 111, 1727–1734.
100. Terman JW & Newton JL (1964). Changes in alveolar and arterial gas tensions as related to altitude and age. J Appl Physiol 19, 21–24.
101. Trangmar SJ, Chiesa ST, Stock CG, Kalsi KK, Secher NH & Gonzalez-Alonso J (2014). Dehydration affects cerebral blood flow but not its metabolic rate for oxygen during maximal exercise in trained humans. J Physiol 592, 3143–3160.
102. van Lieshout JJ & Secher NH (2008). Last Word on Point:Counterpoint: Sympathetic activity does/does not influence cerebral blood flow. J Appl Physiol (1985) 105, 1374.
103. Verbree J, Bronzwaer AS, Ghariq E, Versluis MJ, Daemen MJ, van Buchem MA, Dahan A, van Lieshout JJ & van Osch MJ (2014). Assessment of middle cerebral artery diameter during hypocapnia and hypercapnia in humans using ultra-high-field MRI. J Appl Physiol (1985) 117, 1084–1089.
104. Volianitis S, Fabricius-Bjerre A, Overgaard A, Stromstad M, Bjarrum M, Carlson C, Petersen NT, Rasmussen P, Secher NH & Nielsen HB (2008). The cerebral metabolic ratio is not affected by oxygen availability during maximal exercise in humans. J Physiol 586, 107–112.
105. Williamson JW, McColl R, Mathews D, Ginsburg M & Mitchell JH (1999). Activation of the insular cortex is affected by the intensity of exercise. J Appl Physiol (1985) 87, 1213–1219.
106. Zobl EG, Talmers FN, Christensen RC & Baer LJ (1965). Effect of exercise on the cerebral circulation and metabolism. J Appl Physiol 20, 1289–1293.