High intensity exercise decreases global brain glucose uptake in humans.
Abstract
Physiological activation increases glucose uptake locally in the brain. However, it is not known how high intensity exercise affects regional and global brain glucose uptake. The effect of exercise intensity and exercise capacity on brain glucose uptake was directly measured using positron emission tomography (PET) and [18 F]fluoro‐deoxy‐glucose ([18 F]FDG). Fourteen healthy, right‐handed men were studied after 35 min of bicycle exercise at exercise intensities corresponding to 30, 55 and 75% of on three separate days. [18 F]FDG was injected 10 min after the start of the exercise. Thereafter exercise was continued for another 25 min. PET scanning of the brain was conducted after completion of the exercise. Regional glucose metabolic rate (rGMR) decreased in all measured cortical regions as exercise intensity increased. The mean decrease between the highest and lowest exercise intensity was 32% globally in the brain (38.6 ± 4.6 versus 26.1 ± 5.0 μmol (100 g)−1 min−1, P < 0.001). Lactate availability during exercise tended to correlate negatively with the observed brain glucose uptake. In addition, the decrease in glucose uptake in the dorsal part of the anterior cingulate cortex (37%versus 20%, P < 0.05 between 30% and 75% of ) was significantly more pronounced in subjects with higher exercise capacity. These results demonstrate that brain glucose uptake decreases with increase in exercise intensity. Therefore substrates other than glucose, most likely lactate, are utilized by the brain in order to compensate the increased energy needed to maintain neuronal activity during high intensity exercise. Moreover, it seems that exercise training could be related to adaptive metabolic changes locally in the frontal cortical regions.
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A larger aMCC response during exercise is associated with greater exercise intensity.
“Consistent with this observation, studies of brain metabolism during exercise indicate that a larger aMCC response is associated with greater exercise intensity (Kemppainen et al., 2005).”
From Motivation in the Service of Allostasis: The Role of Anterior Mid-Cingulate Cortex (2019) · cites this paper as Kemppainen et al., 2005
Peripheral blood lactate can cross the blood-brain barrier and provides energy to the brain.
“peripheral blood lactate (e.g., from muscles) can cross the blood–brain barrier and provides energy to the brain”
From Dose-Response Matters! - A Perspective on the Exercise Prescription in Exercise-Cognition Research (2019) · cites this paper as Kemppainen et al., 2005
Cites
Statistical parametric maps in functional imaging: A general linear approach
Friston, K. J., Holmes, A. P., Worsley, K. J., Poline, J. ‐., Frith, C. D., & Frackowiak, R. S. J. (1994) · Human Brain Mapping · doi:10.1002/hbm.460020402 · Cited by 9,688 · see citing works
Cognitive and emotional influences in anterior cingulate cortex
Bush, G., Luu, P., & Posner, M. I. (2000) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(00)01483-2 · Cited by 6,259 · see citing works
Sokoloff, L., Reivich, M., Kennedy, C., Rosiers, M. H. D., Patlak, C. S., Pettigrew, K. D., Sakurada, O., & Shinohara, M. (1977) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1977.tb10649.x · Cited by 6,000 · see citing works
Pellerin, L., & Magistretti, P. J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.22.10625 · Cited by 2,927 · cited 3× · see citing works
“…lactate shuttle hypothesis where lactate along with glucose serves as an oxidative fuel for elevated neuronal energy metabolism so that the largely glycolytic metabolism in astrocytes is linked with the largely oxidative metabolism of lactate in neurones (Pellerin & Magistretti, 1994, 2003).”
BackgroundHamacher, K., Coenen, H. H., & Stöcklin, G. (1986) · PubMed · Cited by 1,368 · see citing works
Lactate metabolism: a new paradigm for the third millennium
Gladden, L. B. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2003.058701 · Cited by 1,283 · see citing works
Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence
Critchley, H. D., Mathias, C. J., Josephs, O., O’Doherty, J., Zanini, S., Dewar, B., Cipolotti, L., Shallice, T., & Dolan, R. J. (2003) · Brain · doi:10.1093/brain/awg216 · Cited by 1,201 · see citing works
The problem of functional localization in the human brain
Brett, M., Johnsrude, I. S., & Owen, A. M. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn756 · Cited by 1,154 · see citing works
The problem of functional localization in the human brain
Morgan, T. (2002) · Cited by 968 · see citing works
Lactate-supported synaptic function in the rat hippocampal slice preparation.
Schurr, A., West, C. A., & Rigor, B. (1988) · Science · doi:10.1126/science.3375817 · Cited by 594 · see citing works
Marbach, E. P., & Weil, M. H. (1967) · PubMed · Cited by 480 · see citing works
Brooks, G. A. (2002) · Biochemical Society Transactions · doi:10.1042/bst0300258 · Cited by 429 · see citing works
Reivich, M., Alavi, A. A., Wolf, A. P., Fowler, J. S., Russell, J. A. G., Arnett, C. D., MacGregor, R. R., Shiue, C., Atkins, H. L., Anand, A., et al. (1985) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1985.24 · Cited by 415 · see citing works
Rapid Enzymatic Measurement of Blood Lactate and Pyruvate
Marbach, E. P., & Weil, M. H. (1967) · Clinical Chemistry · doi:10.1093/clinchem/13.4.314 · Cited by 396 · see citing works
Kubota, Y., Sato, W., Toichi, M., Murai, T., Okada, T., Hayashi, A., & Sengoku, A. (2001) · Cognitive Brain Research · doi:10.1016/s0926-6410(00)00086-0 · Cited by 369 · cited 1× · see citing works
“Regional analysis indicated that this finding was restricted to dorsal anterior cingulate cortex which is associated with cognitive, motor planning, emotional processing and autonomic functions (Bush et al. 2000; Kubota et al. 2001; Critchley et al. 2003).”
MethodTHE FINE STRUCTURE OF THE LATERAL VESTIBULAR NUCLEUS IN THE RAT
Sotelo, C., & Palay, S. L. (1968) · The Journal of Cell Biology · doi:10.1083/jcb.36.1.151 · Cited by 324 · see citing works
Kennedy, C., Rosiers, M. H. D., Sakurada, O., Shinohara, M., Reivich, M., Jehle, J. W., & Sokoloff, L. (1976) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.73.11.4230 · Cited by 306 · see citing works
Cerebral energetics and the glycogen shunt: Neurochemical basis of functional imaging
Shulman, R. G., Hyder, F., & Rothman, D. L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.101129298 · Cited by 299 · see citing works
Schurr, A., Miller, J. J., Payne, R. S., & Rigor, B. M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-01-00034.1999 · Cited by 295 · see citing works
Lactate: A Preferred Fuel for Human Brain Metabolism in Vivo
Smith, D., Pernet, A., Hallett, W. A., Bingham, E., Marsden, P. K., & Amiel, S. A. (2003) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/01.wcb.0000063991.19746.11 · Cited by 282 · see citing works
Sharp, F. R., Kauer, J. S., & Shepherd, G. M. (1975) · Brain Research · doi:10.1016/0006-8993(75)90377-7 · Cited by 275 · see citing works
Madsen, P. L., Hasselbalch, S. G., Hagemann, L. P., Olsen, K. S., Bülow, J., Holm, S., Wildschiødtz, G., Paulson, O. B., & Lassen, N. A. (1995) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1995.60 · Cited by 264 · see citing works
Bayesian image reconstruction for emission tomography based on median root prior
Sakari Alenius, B., & Ruotsalainen, U. (1997) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/bf01728761 · Cited by 243 · see citing works
Cerebral metabolic response to submaximal exercise
Ide, K., Horn, A., & Secher, N. H. (1999) · Journal of Applied Physiology · doi:10.1152/jappl.1999.87.5.1604 · Cited by 240 · see citing works
Lactate, glucose and O2 uptake in human brain during recovery from maximal exercise
Ide, K., Schmalbruch, I. K., Quistorff, B., Horn, A., & Secher, N. H. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.t01-2-00159.xm · Cited by 230 · see citing works
Dalsgaard, M. K., Quistorff, B., Danielsen, E. R., Selmer, C., Vogelsang, T. W., & Secher, N. H. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.055053 · Cited by 191 · see citing works
Cruz, N. F., & Dienel, G. A. (2002) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/01.wcb.0000034362.37277.c0 · Cited by 178 · see citing works
Madsen, P. L., Cruz, N. F., Sokoloff, L., & Dienel, G. A. (1999) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199904000-00005 · Cited by 174 · see citing works
Greenberg, J. H., Reivich, M., Alavi, A. A., Hand, P. J., Rosenquist, A. C., Rintelmann, W. F., Stein, A. D., Tusa, R. J., Dann, R., Christman, D. R., et al. (1981) · Science · doi:10.1126/science.6971492 · Cited by 173 · see citing works
Cortical organization of voluntary behavior in man.
Roland, P. E. (1985) · PubMed · Cited by 155 · see citing works
Myocardial and skeletal muscle glucose uptake during exercise in humans
Kemppainen, J., Fujimoto, T., Kalliokoski, K. K., Viljanen, T., Nuutila, P., & Knuuti, J. M. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.018135 · Cited by 141 · see citing works
Self-citationMonocarboxylate transporter expression in mouse brain
Koehler-Stec, E. M., Simpson, I. A., Vannucci, S. J., Landschulz, K. T., & Landschulz, W. H. (1998) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1998.275.3.e516 · Cited by 136 · see citing works
Lactate Metabolism and Its Effects on Glucose Metabolism in an Excised Neural Tissue
Larrabee, M. G. (1995) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1995.64041734.x · Cited by 129 · see citing works
Cortical 6-[18F]fluoro-l-dopa uptake and frontal cognitive functions in early Parkinson's disease
Brück, A., Aalto, S., Nurmi, E., Bergman, J. R., & Rinne, J. O. (2004) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2004.07.014 · Cited by 124 · see citing works
Self-citationEffects of Subanesthetic Ketamine on Regional Cerebral Glucose Metabolism in Humans
Långsjö, J. W., Salmi, E., Kaisti, K. K., Aalto, S., Hinkka, S., Aantaa, R., Oikonen, V., Viljanen, T., Kurki, T., Silvanto, M., et al. (2004) · Anesthesiology · doi:10.1097/00000542-200405000-00006 · Cited by 123 · see citing works
Self-citationThe intent to exercise influences the cerebral O 2 /carbohydrate uptake ratio in humans
Dalsgaard, M. K., Ide, K., Cai, Y., Quistorff, B., & Secher, N. H. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.013062 · Cited by 109 · see citing works
Neurohumoral responses during prolonged exercise in humans
Nybo, L., Nielsen, B., Blomstrand, E., Møller, K., & Secher, N. H. (2003) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00241.2003 · Cited by 101 · see citing works
How to balance the brain energy budget while spending glucose differently
Pellerin, L., & Magistretti, P. J. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.035105 · Cited by 87 · see citing works
Knudsen, G. M., Paulson, O. B., & Hertz, M. M. (1991) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1991.107 · Cited by 84 · see citing works
Sites and Mechanisms of Function-Related Changes in Energy Metabolism in the Nervous System
Sokoloff, L. (1994) · Developmental Neuroscience · doi:10.1159/000111335 · Cited by 81 · see citing works
Ginsberg, M. D., Dietrich, W. D., & Busto, R. (1987) · Neurology · doi:10.1212/wnl.37.1.11 · Cited by 77 · see citing works
Cerebral carbohydrate cost of physical exertion in humans
Dalsgaard, M. K., Ogoh, S., Dawson, E. A., Yoshiga, C. C., Quistorff, B., & Secher, N. H. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00256.2004 · Cited by 64 · see citing works
Metabolic Coupling during Activation
Magistretti, P. J., & Pellerin, L. (1997) · Advances in experimental medicine and biology · doi:10.1007/978-1-4899-0056-2_18 · Cited by 61 · see citing works
18F-FDG PET mapping of regional brain activity in runners.
Tashiro, M., Itoh, M., Fujimoto, T., Fujiwara, T., Ota, H., Kubota, K., Higuchi, M., Okamura, N., Ishii, K., Bereczki, D., et al. (2001) · PubMed · Cited by 54 · see citing works
Self-citationLactate Transport in Cultured Glial Cells
Dringen, R., Peters, H., Wiesinger, H., & Hamprecht, B. (2007) · Developmental Neuroscience · doi:10.1159/000111275 · Cited by 48 · see citing works
Cerebral Metabolism is Influenced by Muscle Ischaemia During Exercise in Humans
Dalsgaard, M. K., Nybo, L., Cai, Y., & Secher, N. H. (2003) · Experimental Physiology · doi:10.1113/eph8802469 · Cited by 46 · see citing works
Brain Substrate Utilization during Prolonged Exercise
AHLBORG, G., & Wahren, J. (1972) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.3109/00365517209080256 · Cited by 35 · see citing works
Vaughn, J. E., & Grieshaber, J. A. (1972) · Journal of Neurocytology · doi:10.1007/bf01102942 · Cited by 29 · see citing works
Nagano, A. S., Ito, K., Kato, T., Arahata, Y., Kachi, T., Hatano, K., Kawasumi, Y., Nakamura, A., Yamada, T., Abe, Y., et al. (2000) · NeuroImage · doi:10.1006/nimg.2000.0584 · Cited by 24 · see citing works
Brain glucose utilization under high sensory activation: hypoactivation of prefrontal cortex.
Goffinet, A. M., Volder, A. D., Bol, A., & Michel, C. J. (1990) · PubMed · Cited by 6 · see citing works
Lurito (2000) · doi:10.1002/1097-0193(200007)10:3
Flagged first, then by citations
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Sorted by citations
Lactate in the brain: from metabolic end-product to signalling molecule
Magistretti, P. J., & Allaman, I. (2018) · Nature Reviews Neuroscience · doi:10.1038/nrn.2018.19 · Cited by 1,298 · see citing works
Brain metabolism in health, aging, and neurodegeneration
Camandola, S., & Mattson, M. P. (2017) · The EMBO Journal · doi:10.15252/embj.201695810 · Cited by 752 · see citing works
Blood lactate is an important energy source for the human brain.
van Hall, G., Stømstad, M., Rasmussen, P., Jans, Ø., Zaar, M., Gam, C., Quistorff, B., Secher, N. H., & Nielsen, H. B. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.35 · Cited by 522 · see citing works
Ament, W., & Verkerke, G. J. (2009) · Sports Medicine · doi:10.2165/00007256-200939050-00005 · Cited by 504 · see citing works
Brain lactate metabolism: the discoveries and the controversies
Dienel, G. A. (2012) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2011.175 · Cited by 479 · see citing works
The reticular-activating hypofrontality (RAH) model of acute exercise
Dietrich, A., & Audiffren, M. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.02.001 · Cited by 365 · see citing works
Boumezbeur, F., Petersen, K. F., Cline, G. W., Mason, G. F., Behar, K. L., Shulman, G. I., & Rothman, D. L. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2040-10.2010 · Cited by 362 · see citing works
Cerebral blood flow and metabolism during exercise: implications for fatigue
Secher, N. H., Seifert, T., & Van Lieshout, J. J. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00853.2007 · Cited by 344 · see citing works
Regulation of Cerebral Blood Flow During Exercise
Querido, J. S., & Sheel, A. W. (2007) · Sports Medicine · doi:10.2165/00007256-200737090-00002 · Cited by 340 · see citing works
Falkowska, A., Gutowska, I., Goschorska, M., Nowacki, P., Chlubek, D., & Baranowska-Bosiacka, I. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161125939 · Cited by 277 · see citing works
Lactate fuels the human brain during exercise.
Quistorff, B., Secher, N. H., & Van Lieshout, J. J. (2008) · The FASEB Journal · doi:10.1096/fj.08-106104 · Cited by 262 · see citing works
Lactate and BDNF: Key Mediators of Exercise Induced Neuroplasticity?
Müller, P., Duderstadt, Y., Lessmann, V., & Müller, N. G. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9041136 · Cited by 241 · see citing works
Kemppainen, N. M., Aalto, S., Karrasch, M., Någren, K., Savisto, N., Oikonen, V., Viitanen, M., Parkkola, R., & Rinne, J. O. (2008) · Annals of Neurology · doi:10.1002/ana.21212 · Cited by 239 · see citing works
Self-citationPhysical activity and the brain: A review of this dynamic, bi-directional relationship
Loprinzi, P. D., Herod, S. M., Cardinal, B. J., & Noakes, T. D. (2013) · Brain Research · doi:10.1016/j.brainres.2013.10.004 · Cited by 222 · see citing works
Tsukamoto, H., Suga, T., Takenaka, S., Tanaka, D., Takeuchi, T., Hamaoka, T., Isaka, T., & Hashimoto, T. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.12.021 · Cited by 216 · see citing works
Hippocampal neurogenesis and gene expression depend on exercise intensity in juvenile rats
Lou, S., Liu, J., Chang, H., & Chen, P. (2008) · Brain Research · doi:10.1016/j.brainres.2008.02.080 · Cited by 206 · see citing works
Dose-Response Matters! - A Perspective on the Exercise Prescription in Exercise-Cognition Research
Herold, F., Müller, P., Gronwald, T., & Müller, N. G. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.02338 · Cited by 196 · see citing works
Increased slow wave sleep and reduced stage 2 sleep in children depending on exercise intensity
Dworak, M., Wiater, A., Alfer, D., Stephan, E., Hollmann, W., & Strüder, H. K. (2008) · Sleep Medicine · doi:10.1016/j.sleep.2007.04.017 · Cited by 185 · see citing works
Wheeler, M. J., Dempsey, P. C., Grace, M. S., Ellis, K. A., Gardiner, P. A., GREEN, D. J., & Dunstan, D. W. (2017) · Alzheimer s & Dementia Translational Research & Clinical Interventions · doi:10.1016/j.trci.2017.04.001 · Cited by 186 · see citing works
Fueling and Imaging Brain Activation
Dienel, G. A. (2012) · ASN NEURO · doi:10.1042/an20120021 · Cited by 175 · see citing works
Fuelling Cerebral Activity in Exercising Man
Dalsgaard, M. K. (2006) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600256 · Cited by 158 · see citing works
Kao, S., Westfall, D. R., Soneson, J., Gurd, B. J., & Hillman, C. H. (2017) · Psychophysiology · doi:10.1111/psyp.12889 · Cited by 153 · see citing works
Maintained exercise‐enhanced brain executive function related to cerebral lactate metabolism in men
Hashimoto, T., Tsukamoto, H., Takenaka, S., Olesen, N. D., Petersen, L. G., Sørensen, H., Nielsen, H. B., Secher, N. H., & Ogoh, S. (2018) · The FASEB Journal · doi:10.1096/fj.201700381rr · Cited by 156 · see citing works
The influence of a single bout of aerobic exercise on short-interval intracortical excitability
Smith, A. E., Goldsworthy, M. R., Garside, T., Wood, F. M., & Ridding, M. C. (2014) · Experimental Brain Research · doi:10.1007/s00221-014-3879-z · Cited by 147 · see citing works
Stavrinos, E. L., & Coxon, J. P. (2016) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01078 · Cited by 125 · see citing works
Effects of Insulin on Brain Glucose Metabolism in Impaired Glucose Tolerance
Hirvonen, J., Virtanen, K. A., Nummenmaa, L., Hannukainen, J. C., Honka, M., Bucci, M., Nesterov, S. V., Parkkola, R. K., Rinne, J. O., Iozzo, P., et al. (2011) · Diabetes · doi:10.2337/db10-0940 · Cited by 128 · see citing works
Self-citationOrgan-Specific Physiological Responses to Acute Physical Exercise and Long-Term Training in Humans
HEINONEN, I. H. A., Kalliokoski, K. K., Hannukainen, J. C., Duncker, D. J., Nuutila, P., & Knuuti, J. M. (2014) · Physiology · doi:10.1152/physiol.00067.2013 · Cited by 127 · see citing works
Self-citationHypercarnivory and the brain: protein requirements of cats reconsidered
Eisert, R. (2010) · Journal of Comparative Physiology B · doi:10.1007/s00360-010-0528-0 · Cited by 117 · see citing works
Dmitriev, L. F., & Titov, V. N. (2009) · Ageing Research Reviews · doi:10.1016/j.arr.2009.09.004 · Cited by 103 · see citing works
Cerebral glucose and lactate consumption during cerebral activation by physical activity in humans
Rasmussen, P. V., Wyss, M. T., & Lundby, C. (2011) · The FASEB Journal · doi:10.1096/fj.11-183822 · Cited by 104 · see citing works
Sympathetic influence on cerebral blood flow and metabolism during exercise in humans
Seifert, T., & Secher, N. H. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.09.008 · Cited by 100 · see citing works
Kujach, S., Olek, R. A., Byun, K., Suwabe, K., Sitek, E. J., Ziemann, E., Laskowski, R., & Soya, H. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01455 · Cited by 106 · see citing works
The Effects of Acute Aerobic Exercise on the Primary Motor Cortex
Singh, A. M., & Staines, R. W. (2015) · Journal of Motor Behavior · doi:10.1080/00222895.2014.983450 · Cited by 99 · see citing works
Coxon, J. P., Cash, R. F. H., Hendrikse, J. J., Rogasch, N. C., Stavrinos, E. L., Suo, C., & Yücel, M. (2017) · The Journal of Physiology · doi:10.1113/jp274660 · Cited by 94 · see citing works
Impaired Cognitive Performance in Youth Athletes Exposed to Repetitive Head Impacts
Koerte, I. K., Nichols, E., Tripodis, Y., Schultz, V., Lehner, S., Igbinoba, R., Chuang, A. Z., Mayinger, M. C., Klier, E. M., Muehlmann, M., et al. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2016.4960 · Cited by 94 · see citing works
Shah, T., Verdile, G., Sohrabi, H., Campbell, A., Putland, E., Cheetham, C., Dhaliwal, S., Weinborn, M., Maruff, P., Darby, D., et al. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.122 · Cited by 94 · see citing works
Effect of Exercise on Brain Health: The Potential Role of Lactate as a Myokine
Hashimoto, T., Tsukamoto, H., Ando, S., & Ogoh, S. (2021) · Metabolites · doi:10.3390/metabo11120813 · Cited by 92 · see citing works
Causes of obesity: Looking beyond the hypothalamus
Peters, A., Pellerin, L., DALLMAN, M., Oltmanns, K. M., Schweiger, U., Jan Born, A., & Fehm, H. L. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.12.004 · Cited by 92 · see citing works
Tsukamoto, H., Suga, T., Takenaka, S., Tanaka, D., Takeuchi, T., Hamaoka, T., Isaka, T., Ogoh, S., & Hashimoto, T. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.03.029 · Cited by 88 · see citing works
Sudo, M., Costello, J. T., McMorris, T., & Ando, S. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.957677 · Cited by 91 · see citing works
State-Dependent Performance of Optic-Flow Processing Interneurons
Longden, K. D., & Krapp, H. G. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00395.2009 · Cited by 83 · see citing works
Hertz, L., & Rothman, D. L. (2016) · Advances in neurobiology · doi:10.1007/978-3-319-45096-4_2 · Cited by 85 · see citing works
Pushing to the limits: The dynamics of cognitive control during exhausting exercise
Schmit, C., Davranche, K., Easthope, C. A., Colson, S. S., Brisswalter, J., & Radel, R. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.01.006 · Cited by 82 · see citing works
Endurance Exercise as an “Endogenous” Neuro-enhancement Strategy to Facilitate Motor Learning
Taubert, M., Villringer, A., & Lehmann, N. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00692 · Cited by 83 · see citing works
Kao, S., Drollette, E. S., Ritondale, J. P., Khan, N. A., & Hillman, C. H. (2018) · Psychology of sport and exercise · doi:10.1016/j.psychsport.2018.05.011 · Cited by 74 · see citing works
Establishment of In Vivo Brain Imaging Method in Conscious Mice
Mizuma, H., Shukuri, M., Hayashi, T., Watanabe, Y., & Onoe, H. (2010) · Journal of Nuclear Medicine · doi:10.2967/jnumed.110.075184 · Cited by 76 · see citing works
Larsen, T. S., Rasmussen, P. V., Overgaard, M., Secher, N. H., & Nielsen, H. B. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.151449 · Cited by 68 · see citing works
Intermittent Maximal Exercise Improves Attentional Performance Only in Physically Active Students
Budde, H., Brunelli, A., Machado, S. E. D. C., Velasques, B., Ribeiro, P. F. M., Arias-Carrión, Ó., & Voelcker‐Rehage, C. (2012) · Archives of Medical Research · doi:10.1016/j.arcmed.2012.02.005 · Cited by 67 · see citing works
Effects of Xenon Anesthesia on Cerebral Blood Flow in Humans
Laitio, R. M., Kaisti, K. K., Långsjö, J., Aalto, S., Salmi, E., Maksimow, A. T., Aantaa, R., Oikonen, V., Sipilä, H. T., Parkkola, R. K., et al. (2007) · Anesthesiology · doi:10.1097/01.anes.0000267596.57497.92 · Cited by 66 · see citing works
Self-citationThe tenacious brain: How the anterior mid-cingulate contributes to achieving goals
Touroutoglou, A., Andreano, J. M., Dickerson, B. C., & Barrett, L. F. (2019) · Cortex · doi:10.1016/j.cortex.2019.09.011 · Cited by 63 · see citing works
The brain at work: A cerebral metabolic manifestation of central fatigue?
Dalsgaard, M. K., & Secher, N. H. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21274 · Cited by 63 · see citing works
Effect of Exercise Intensity and Duration on Postexercise Executive Function
Tsukamoto, H., Takenaka, S., Suga, T., Tanaka, D., Takeuchi, T., Hamaoka, T., Isaka, T., & Hashimoto, T. (2016) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001155 · Cited by 64 · see citing works
Neurovascular coupling and distribution of cerebral blood flow during exercise
Willie, C. K., Cowan, E. C., Ainslie, P. N., Taylor, C. E., Smith, K. J., Sin, P. Y. W., & Tzeng, Y. (2011) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2011.03.017 · Cited by 59 · see citing works
Aerobic exercise enhances neural correlates of motor skill learning
Singh, A. M., Neva, J. L., & Staines, R. W. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.12.020 · Cited by 59 · see citing works
Volianitis, S., Fabricius-Bjerre, A., Overgaard, A., Strømstad, M., Bjarrum, M., Carlson, C., Petersen, N., Rasmussen, P. V., Secher, N. H., & Nielsen, H. B. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.142273 · Cited by 58 · see citing works
Wang, Z., Myers, K. G., Guo, Y., Ocampo, M. A., Pang, R. D., Jakowec, M. W., & Holschneider, D. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080058 · Cited by 57 · see citing works
Robinson, M. M., Lowe, V. J., & Nair, K. S. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-01571 · Cited by 55 · see citing works
Herold, F., Aye, N., Lehmann, N., Taubert, M., & Müller, N. G. (2020) · Brain Sciences · doi:10.3390/brainsci10030175 · Cited by 53 · see citing works
Beneficial Effects of Whole Body Vibration on Brain Functions in Mice and Humans
Boerema, A. S., Heesterbeek, M., Boersma, S. A., Schoemaker, R. G., de Vries, E. F. J., van Heuvelen, M. J. G., & van der Zee, E. A. (2018) · Dose-Response · doi:10.1177/1559325818811756 · Cited by 54 · see citing works
Huang, Z., Zhang, Y., Zhou, R., Yang, L., & Pan, H. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.656455 · Cited by 55 · see citing works
Bakirtzi, K., Belfort, G. M., G.‐Coviella, I. L., Kuruppu, D., Cao, L. R., Abel, E. D., Brownell, A., & Kandror, K. V. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0858-09.2009 · Cited by 54 · see citing works
Dougherty, R. J., Schultz, S. A., Kirby, T., Boots, E. A., Oh, J. M., Edwards, D. F., Gallagher, C. L., Carlsson, C. M., Bendlin, B. B., Asthana, S., et al. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-161067 · Cited by 50 · see citing works
Chen, H., Dong, G., & Li, K. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1094583 · Cited by 47 · see citing works
Cerebral non‐oxidative carbohydrate consumption in humans driven by adrenaline
Seifert, T. S., Brassard, P., Jørgensen, T. B., Hamada, A. J., Rasmussen, P., Quistorff, B., Secher, N. H., & Nielsen, H. B. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.162073 · Cited by 47 · see citing works
Application of positron emission tomography to neuroimaging in sports sciences
Tashiro, M., Itoh, M., Fujimoto, T., Masud, M. M., Watanuki, S., & Yanai, K. (2008) · Methods · doi:10.1016/j.ymeth.2008.05.001 · Cited by 46 · see citing works
Self-citationMahboubi, S., Nasehi, M., Imani, A., Sadat‐Shirazi, M., Zarrindast, M., Vousooghi, N., & Noroozıan, M. (2019) · Nature and Science of Sleep · doi:10.2147/nss.s207339 · Cited by 47 · see citing works
A trade-off between cognitive and physical performance, with relative preservation of brain function
Longman, D. P., Stock, J. T., & Wells, J. C. K. (2017) · Scientific Reports · doi:10.1038/s41598-017-14186-2 · Cited by 43 · see citing works
Salmi, E., Aalto, S., Hirvonen, J., Långsjö, J., Maksimow, A. T., Oikonen, V., Metsähonkala, L., Virkkala, J., Någren, K., & Scheinin, H. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.02.035 · Cited by 43 · see citing works
Self-citationA Single Bout of Aerobic Exercise Improves Motor Skill Consolidation in Parkinson’s Disease
Steib, S., Wanner, P., Adler, W., Winkler, J., Klucken, J., & Pfeifer, K. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00328 · Cited by 43 · see citing works
Wang, Z., Guo, Y., Myers, K. G., Heintz, R., & Holschneider, D. P. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.02.020 · Cited by 42 · see citing works
Boecker, H., Henriksen, G., Sprenger, T., Miederer, I., Willoch, F., Valet, M., Berthele, A., & Tölle, T. R. (2008) · Methods · doi:10.1016/j.ymeth.2008.07.003 · Cited by 41 · see citing works
Cardiovascular control during whole body exercise
Volianitis, S., & Secher, N. H. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00674.2015 · Cited by 37 · see citing works
de Senna, P. N., Bagatini, P. B., Galland, F., Bobermin, L. D., do Nascimento, P. S., Nardin, P., Tramontina, A. C., Gonçalves, C. A., Achaval, M., & Xavier, L. L. (2016) · Brain Research · doi:10.1016/j.brainres.2016.10.024 · Cited by 35 · see citing works
Multiple Mechanisms Linking Type 2 Diabetes and Alzheimer’s Disease: Testosterone as a Modifier
Asih, P. R., Tegg, M., Sohrabi, H. R., Carruthers, M. E., Gandy, S., Saad, F., Verdile, G., Ittner, L. M., & Martins, R. N. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-161259 · Cited by 34 · see citing works
Aalto, S., Scheinin, N. M., Kemppainen, N. M., Någren, K., Kailajärvi, M., Leinonen, M., Scheinin, M., & Rinne, J. O. (2009) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-009-1174-1 · Cited by 34 · see citing works
Self-citationA perspective on the future role of brain pet imaging in exercise science
Boecker, H., & Drzezga, A. E. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.10.021 · Cited by 35 · see citing works
Jacob, N., So, I., Sharma, B., Marzolini, S., Tartaglia, M. C., OH, P. I., & Green, R. (2023) · Sports Medicine · doi:10.1007/s40279-023-01815-2 · Cited by 37 · see citing works
Chen, H., Cheng, F., Pan, H.-C., Hsu, J.-C., & Wang, M.-F. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085486 · Cited by 33 · see citing works
Schwarck, S., Schmicker, M., Dordevic, M., Rehfeld, K., Müller, N. G., & Müller, P. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8081101 · Cited by 34 · see citing works
Potential Roles of Exercise-Induced Plasma Metabolites Linking Exercise to Health Benefits
Yang, Y. R., & Kwon, K. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.602748 · Cited by 32 · see citing works
Pani, J., Reitlo, L. S., Evensmoen, H. R., Lydersen, S., Wisløff, U., Stensvold, D., & Haberg, A. K. (2021) · Clinical Interventions in Aging · doi:10.2147/cia.s318679 · Cited by 32 · see citing works
Decreased brain FDG uptake in patients with extensive non-Hodgkin’s lymphoma lesions
Hanaoka, K., Hosono, M., Shimono, T., Usami, K., Komeya, Y., Tsuchiya, N., Yamazoe, Y., Ishii, K., Tatsumi, Y., & Sumita, M. (2010) · Annals of Nuclear Medicine · doi:10.1007/s12149-010-0415-5 · Cited by 32 · see citing works
Rahmati, M., & Kazemi, A. (2019) · Gene · doi:10.1016/j.gene.2019.01.013 · Cited by 31 · see citing works
Short-term interval training alters brain glucose metabolism in subjects with insulin resistance
Honkala, S. M., Johansson, J. J., Motiani, K. K., Eskelinen, J., Virtanen, K. A., Löyttyniemi, E., Knuuti, J. M., Nuutila, P., Kalliokoski, K. K., & Hannukainen, J. C. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x17734998 · Cited by 31 · see citing works
Self-citationPorto, F. H. D. G., Coutinho, A. M., Pinto, A. L. D. S., Gualano, B., Duran, F., Prando, S., Ono, C. R., Spíndola, L., de Oliveira, M. O., do Vale, P. H. F., et al. (2015) · Journal of Alzheimer s Disease · doi:10.3233/jad-150033 · Cited by 30 · see citing works
Metformin May Contribute to Inter-individual Variability for Glycemic Responses to Exercise
Malin, S. K., & Stewart, N. R. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00519 · Cited by 29 · see citing works
Prefrontal lactate predicts exercise-induced cognitive dysfunction in Gulf War Illness.
Rayhan, R. U., Raksit, M. P., Timbol, C. R., Adewuyi, O., VanMeter, J. W., & Baraniuk, J. N. (2013) · Europe PMC (PubMed Central) · Cited by 29 · see citing works
Rasmussen, P., Nyberg, N. T., Jaroszewski, J. W., Krogh‐Madsen, R., Secher, N. H., & Quistorff, B. (2010) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2010.25 · Cited by 29 · see citing works
Motivation in the Service of Allostasis: The Role of Anterior Mid-Cingulate Cortex
Touroutoglou, A., Andreano, J. M., Adebayo, M., Lyons, S., & Barrett, L. F. (2019) · Advances in Motivation Science · doi:10.1016/bs.adms.2018.09.002 · Cited by 25 · see citing works
“Consistent with this observation, studies of brain metabolism during exercise indicate that a larger aMCC response is associated with greater exercise intensity (Kemppainen et al., 2005).”
ResultLaitio, R. M., Långsjö, J., Aalto, S., Kaisti, K. K., Salmi, E., Maksimow, A. T., Aantaa, R., Oikonen, V., Viljanen, T., Parkkola, R., et al. (2009) · Anesthesia & Analgesia · doi:10.1213/ane.0b013e31818ffc9d · Cited by 27 · see citing works
Self-citationThe Reticular-Activating Hypofrontality (RAH) Model of Acute Exercise
Audiffren, M. F. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800778-5.00007-4 · Cited by 27 · see citing works
The interplay between neuropathology and activity based rehabilitation after traumatic brain injury
Kreber, L. A., & Griesbach, G. S. (2016) · Brain Research · doi:10.1016/j.brainres.2016.01.016 · Cited by 27 · see citing works
Maninger, N., Hinde, K., Mendoza, S. P., Mason, W. A., Larke, R. H., Ragen, B., Jarcho, M. R., Cherry, S. R., Rowland, D. J., Ferrer, E. E., et al. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.02.028 · Cited by 27 · see citing works
Wang, Z., Xu, X., Yang, X., Wang, S., Zhou, Y., & Li, Y. (2024) · International Journal of Nursing Studies · doi:10.1016/j.ijnurstu.2024.104843 · Cited by 26 · see citing works
Tian, S., Mou, H., & Qiu, F. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph18052687 · Cited by 22 · see citing works
Insulin blood-brain barrier transport and interactions are greater following exercise in mice
Brown, C., Pemberton, S., Babin, A., Abdulhameed, N., Noonan, C., Brown, M. B., Banks, W. A., & Rhea, E. M. (2022) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00866.2021 · Cited by 23 · see citing works
A short bout of high-intensity exercise alters ipsilesional motor cortical excitability post-stroke
Li, X., Charalambous, C. C., Reisman, D. S., & Morton, S. M. (2019) · Topics in Stroke Rehabilitation · doi:10.1080/10749357.2019.1623458 · Cited by 22 · see citing works
Best, J. G., Stagg, C. J., & Dennis, A. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-401688-0.00010-0 · Cited by 21 · see citing works
Wu, Q., Niu, X., Zhang, Y., Song, J., & Chi, A. (2023) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph20042859 · Cited by 20 · see citing works
Reid, W. C., Casas, R., Papadakis, G. Z., Muthusamy, S., Lee, D. E., Ibrahim, W. G., Nair, A. R., Koziol, D. E., Maric, D., & Hammoud, D. A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0152265 · Cited by 19 · see citing works
- Authors
- Kemppainen, J., Aalto, S., Fujimoto, T., Kalliokoski, K. K., Långsjö, J., Oikonen, V., Rinne, J., Nuutila, P., & Knuuti, J.
- Affiliations
- University of Turku (FI)
- Åbo Akademi University (FI)
- Tohoku University (JP)
- Turku PET Centre (FI)
- ORCID
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2005-09-28
- Volume
- 568
- Issue
- 1
- Pages
- 323-332
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- OpenAlex
- W2170725206
- Cited by
- 179
- References
- 51
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 6 · 2023: 9 · 2022: 5 · 2021: 8 · 2020: 10 · 2019: 12 · 2018: 8 · 2017: 15 · 2016: 13 · 2015: 15 · 2014: 6 · 2013: 4 · 2012: 4
- FWCI
- 18.69
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Novo Nordisk Fonden
- Topics
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Health Sciences › Medicine › Physiology › Physical Activity and Health
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Keywords
- high-intensity exercise, brain glucose uptake, regional cerebral glucose metabolism, exercise intensity, exercise capacity, anterior cingulate cortex, brain energy metabolism, training effects, cerebral blood flow
- MeSH terms
- Blood Glucose, Brain, Cerebrovascular Circulation, Energy Metabolism, Physical Exertion, Frontal Lobe, Glucose, Humans, Insulin, Male, Time Factors, Tomography, Emission-Computed, Exercise, Radiopharmaceuticals, Lactic Acid, Fluorodeoxyglucose F18
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