Hemodynamic Changes in Response to Aerobic Exercise: Near-infrared Spectroscopy Study

Abstract

This study aimed to determine the neurophysiological mechanisms underlying the effects of aerobic exercise, which influence brain O2 consumption, on cognitive enhancement. Sixteen healthy men were asked to complete a 2-back test at rest and after moderate and high-intensity aerobic exercise. During the 2-back test, hemodynamic changes within the prefrontal cortex were assessed using high-density functional near-infrared spectroscopy. Scores of the 2-back test, regardless of the exercise intensity, were positively correlated with the hemodynamic changes within the right and left dorsolateral prefrontal cortex (DLPFC). During an 2-back test, there were differences in the hemodynamic changes within the DLPFC with moderate and high-intensity exercise conditions. In the 2-back condition, the accumulated oxyhemoglobin within the right DLPFC after moderate intensity exercise was 7.9% lower than that at baseline, while the accumulated oxyhemoglobin within the left DLPFC was 14.6% higher than that at baseline after high-intensity exercise. In response to the 2-back test, the accumulated oxygenated hemoglobin within the left DLPFC after high-intensity exercise increased more significantly than that observed after moderate intensity exercise. These results show that the right DLPFC consumes O2 more efficiently in response to moderate intensity aerobic exercise than in response to high-intensity aerobic exercise.

Key words

aerobic exercise - near-infrared spectroscopy - oxygenated hemoglobin - dorsolateral prefrontal cortex

Publikationsverlauf

Eingereicht: 09. Januar 2020

Angenommen: 03. Juni 2020

Artikel online veröffentlicht:
19. Oktober 2020

• References

• 1 Smith PJ, Blumenthal JA, Hoffman BM. et al. Aerobic exercise and neurocognitive performance: A meta-analytic review of randomized controlled trials. Psychosom Med 2010; 72: 239-252
• 2 Guiney H, Machado L. Benefits of regular aerobic exercise for executive functioning in healthy populations. Psychon Bull Rev 2013; 20: 73-86
• 3 Coles K, Tomporowski PD. Effects of acute exercise on executive processing, short-term and long-term memory. J Sports Sci 2008; 26: 333-344
• 4 Pontifex MB, Hillman CH, Fernhall B. et al. The effect of acute aerobic and resistance exercise on working memory. Med Sci Sports Exer 2009; 41: 927-934
• 5 D’esposito M, Detre JA, Alsop DC. et al. The neural basis of the central executive system of working memory. Nature 1995; 378: 279-281
• 6 Northey JM, Cherbuin N, Pumpa KL. et al. Exercise interventions for cognitive function in adults older than 50: A systematic review with meta-analysis. Br J Sports Med 2018; 52: 154-160
• 7 Angevaren M, Aufdemkampe G, Verhaar HJ. et al. Physical activity and enhanced fitness to improve cognitive function in older people without known cognitive impairment. Cochrane Database Syst Rev 2008; 3: CD005381
• 8 Kramer AF, Colcombe S. Fitness effects on the cognitive function of older adults: A meta-analytic study—revisited. Perspect Psychol Sci 2018; 13: 213-217
• 9 Nouchi R, Taki Y, Takeuchi H. et al. Four weeks of combination exercise training improved executive functions, episodic memory, and processing speed in healthy elderly people: Evidence from a randomized controlled trial. Age 2014; 36: 787-799
• 10 Chen A-G, Yan J, Yin H. et al. Effects of acute aerobic exercise on multiple aspects of executive function in preadolescent children. Psychol Sport Exer 2014; 15: 627-636
• 11 Verburgh L, Königs M, Scherder EJ. et al. Physical exercise and executive functions in preadolescent children, adolescents and young adults: A meta-analysis. Br J Sports Med 2014; 48: 973-979
• 12 Choi JW, Han DH, Kang KD. et al. Aerobic exercise and attention deficit hyperactivity disorder: Brain research. Med Sci Sports Exer 2015; 47: 33-39
• 13 Thomas R, Sanders S, Doust J. et al. Prevalence of attention-deficit/hyperactivity disorder: A systematic review and meta-analysis. Pediatrics 2015; 135: e994-e1001
• 14 Ferris LT, Williams JS, Shen CL. The effect of acute exercise on serum brain-derived neurotrophic factor levels and cognitive function. Med Sci Sports Exer 2007; 39: 728-734
• 15 Chmura J, Nazar K, Kaciuba-Uścilko H. Choice reaction time during graded exercise in relation to blood lactate and plasma catecholamine thresholds. Int J Sports Med 1994; 15: 172-176
• 16 Dupuy O, Gauthier CJ, Fraser SA. et al. Higher levels of cardiovascular fitness are associated with better executive function and prefrontal oxygenation in younger and older women. Front Hum Neurosci 2015; 9: 66
• 17 Cotman CW, Berchtold NC, Christie LA. Exercise builds brain health: Key roles of growth factor cascades and inflammation. Trends Neurosci 2007; 30: 464-472
• 18 Bolduc V, Thorin-Trescases N, Thorin E. Endothelium-dependent control of cerebrovascular functions through age: exercise for healthy cerebrovascular aging. Am J Physiol Heart Circ Physiol 2013; 305: H620-H633
• 19 Colcombe SJ, Kramer AF, Erickson KI. et al. Cardiovascular fitness, cortical plasticity, and aging. Proc Natl Acad Sci USA 2004; 101: 3316-3321
• 20 Colcombe SJ, Erickson KI, Raz N. et al. Aerobic fitness reduces brain tissue loss in aging humans. J Gerontol A Biol Sci Med Sci 2003; 58: 176-180
• 21 Yuki A, Lee S, Kim H. et al. Relationship between physical activity and brain atrophy progression. Med Sci Sports Exerc 2012; 44: 2362-2368
• 22 McMorris TE, Tomporowski PE, Audiffren ME. Exercise and Cognitive Function. Wiley-Blackwell. 2009
• 23 Audiffren M, Tomporowski PD, Zagrodnik J. Acute aerobic exercise and information processing: energizing motor processes during a choice reaction time task. Acta Psychol 2008; 129: 410-419
• 24 Tomporowski PD. Effects of acute bouts of exercise on cognition. Acta Psychol 2003; 112: 297-324
• 25 Cooper CJ. Anatomical and physiological mechanisms of arousal, with special reference to the effects of exercise. Ergonomics 1973; 16: 601-609
• 26 Davey CP. Physical exertion and mental performance. Ergonomics 1973; 16: 595-599
• 27 Kahneman D. Attention and Effort. Englewood Cliffs, NJ: Prentice-Hall, Inc; 1973: 1063
• 28 Yanagisawa H, Dan I, Tsuzuki D. et al. Acute moderate exercise elicits increased dorsolateral prefrontal activation and improves cognitive performance with Stroop test. Neuroimage 2010; 50: 1702-1710
• 29 Barbey AK, Koenigs M, Grafman J. Dorsolateral prefrontal contributions to human working memory. Cortex 2013; 49: 1195-1205
• 30 Tomporowski PD, Ellis NR. Effects of exercise on cognitive processes: A review. Psychol Bull 1986; 99: 338-346
• 31 Gill DL. A sport and exercise psychology perspective on stress. Quest 1994; 46: 20-27
• 32 McMorris T, Graydon J. The effect of exercise on cognitive performance in soccer-specific tests. J Sports Sci 1997; 15: 459-468
• 33 Hogervorst E, Riedel W, Jeukendrup A. et al. Cognitive performance after strenuous physical exercise. Percept Mot Skills 1996; 83: 479-488
• 34 Brisswalter J, Arcelin R, Audiffren M. et al. Influence of physical exercise on simple reaction time: Effect of physical fitness. Percept Mot Skills 1997; 85: 1019-1027
• 35 Alves CR, Tessaro VH, Teixeira LA. et al. Influence of acute high-intensity aerobic interval exercise bout on selective attention and short-term memory tasks. Percept Mot Skills 2014; 118: 63-72
• 36 Tsukamoto H, Suga T, Takenaka S. et al. Greater impact of acute high-intensity interval exercise on post-exercise executive function compared to moderate-intensity continuous exercise. Physiol Behav 2016; 155: 224-230
• 37 Miller E, Wallis J. Executive function and higher-order cognition: definition and neural substrates. In: Squire LR, ed. Encyclopedia of Neuroscience, Volume 4. Oxford, UK: Academic Press; 2009: 99-104
• 38 Baddeley AD, Logie RH. Working Memory: The Multiple-Component Model. In Miyake A, Shah P, eds. Models of Working Memory: Mechanisms of Active Maintenance and Executive Control. Cambridge, UK: Cambridge University Press; 1999: 28-61
• 39 Baddeley A. Working memory. Science 1992; 255: 556-559
• 40 Baddeley AD, Hitch G. Working memory. In Exploring Working Memory. Abingdon, UK: Routledge; 2017: 43-79
• 41 Agbangla NF, Audiffren M, Albinet CT. Use of near-infrared spectroscopy in the investigation of brain activation during cognitive aging: A systematic review of an emerging area of research. Ageing Res Rev 2017; 38: 52-66
• 42 Owen AM, McMillan KM, Laird AR. et al. N-back working memory paradigm: A meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp 2005; 25: 46-59
• 43 Shin J, von Lühmann A, Kim DW. et al. Simultaneous acquisition of EEG and NIRS during cognitive tasks for an open access dataset. Sci Data 2018; 5: 180003
• 44 Kane MJ, Conway ARA, Miura TK. et al. Working memory, attention control, and the N-back task: A question of construct validity. J Exp Psychol Learn Mem Cogn 2007; 33: 615-622
• 45 Jonides J, Schumacher EH, Smith EE. et al. Verbal working memory load affects regional brain activation as measured by PET. J Cogn Neurosci 1997; 9: 462-475
• 46 Baars BJ, Gage NM. Cognition, Brain, and Consciousness: Introduction to Cognitive Neuroscience. Cambridge, UK: Cambridge Academic Press; 2010
• 47 Miller KM, Price CC, Okun MS. et al. Is the n-back task a valid neuropsychological measure for assessing working memory?. Arch Clin Neuropsychol 2009; 24: 711-717
• 48 Callicott JH, Bertolino A, Mattay VS. et al. Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited. Cereb Cortex 2000; 10: 1078-1092
• 49 Jansma JM, Ramsey NF, van der Wee NJ. et al. Working memory capacity in schizophrenia: a parametric fMRI study. Schizophr Res 2004; 68: 159-171
• 50 Perlstein WM, Carter CS, Noll DC. et al. Relation of prefrontal cortex dysfunction to working memory and symptoms in schizophrenia. Am J Psychiatry 2001; 158: 1105-1113
• 51 Wilson SL, McMillan T. Computer-based assessment in neuropsychology. In: Crawford JR, Parker DM, McKinlay WW, eds A Handbook of Neuropsychological Assessment. Hove, UK: Lawrence Erlbaum Associates; 1992: 413-420
• 52 Ballard JC. Computerized assessment of sustained attention: A review of factors affecting vigilance performance. J Clin Exp Neuropsychol 1996; 18: 843-863
• 53 Gur RC, Ragland JD, Moberg PJ. et al. Computerized neurocognitive scanning: II. The profile of schizophrenia. Neuropsychopharmacology 2001; 25: 777-788
• 54 Ferrari M, Quaresima V. A brief review on the history of human functional near-infrared spectroscopy (fNIRS) development and fields of application. Neuroimage 2012; 63: 921-935
• 55 Scholkmann F, Kleiser S, Metz AJ. et al. A review on continuous wave functional near-infrared spectroscopy and imaging instrumentation and methodology. Neuroimage 2014; 85: 6-27
• 56 Tsujii T, Yamamoto E, Ohira T. et al. Effects of sedative and non-sedative H 1 antagonists on cognitive tasks: Behavioral and near-infrared spectroscopy (NIRS) examinations. Psychopharmacology (Berl) 2007; 194: 83-91
• 57 Pietrobelli A, Faith MS, Allison DB. et al. Body mass index as a measure of adiposity among children and adolescents: A validation study. J Pediatr 1998; 132: 204-210
• 58 Harriss DJ, MacSween A, Atkinson G. Ethical standards in sport and exercise science research: 2020 update. Int J Sports Med 2019; 40: 813-817
• 59 Hillman CH, Pontifex MB, Raine LB. et al. The effect of acute treadmill walking on cognitive control and academic achievement in preadolescent children. Neuroscience 2009; 159: 1044-1054
• 60 McMorris T, Sproule J, Turner A. et al. Acute, intermediate intensity exercise, and speed and accuracy in working memory tasks: A meta-analytical comparison of effects. Physiol Behav 2011; 102: 421-428
• 61 Karvonen J, Vuorimaa T. Heart rate and exercise intensity during sports activities. Practical application. Sports Med 1988; 5: 303-311
• 62 Robergs RA, Landwehr R. The surprising history of the “HRmax= 220-age” equation. J Exer Physiol Online 2002; 5: 1-10
• 63 Byun K, Hyodo K, Suwabe K. et al. Possible influences of exercise-intensity-dependent increases in non-cortical hemodynamic variables on NIRS-based neuroimaging analysis during cognitive tasks: Technical note. J Exer Nutr Biochem 2014; 18: 327-332
• 64 Choi J-K. et al. Time-divided spread-spectrum code-based 400 fW-detectable multichannel fNIRS IC for portable functional brain imaging. IEEE J Solid-State Circuits 2016; 51: 484-495
• 65 Yamamoto T, Maki A, Kadoya T. et al. Arranging optical fibres for the spatial resolution improvement of topographical images. Phys Med Biol 2002; 47: 3429-3440
• 66 Delpy DT, Cope M, van der Zee P. et al. Estimation of optical pathlength through tissue from direct time of flight measurement. Phys Med Biol 1988; 33: 1433-1442
• 67 Cui X, Bray S, Bryant DM. et al. A quantitative comparison of NIRS and fMRI across multiple cognitive tasks. Neuroimage 2011; 54: 2808-2821
• 68 Miyai I, Tanabe HC, Sase I. et al. Cortical mapping of gait in humans: A near-infrared spectroscopic topography study. Neuroimage 2001; 14: 1186-1192
• 69 Strangman G, Culver JP, Thompson JH. et al. A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. Neuroimage 2002; 17: 719-731
• 70 Hyodo K, Dan I, Suwabe K. et al. Acute moderate exercise enhances compensatory brain activation in older adults. Neurobiol Aging 2012; 33: 2621-2632
• 71 Kujach S, Byun K, Hyodo K. et al. A transferable high-intensity intermittent exercise improves executive performance in association with dorsolateral prefrontal activation in young adults. Neuroimage 2018; 169: 117-125
• 72 Brunoni AR, Vanderhasselt MA. Working memory improvement with non-invasive brain stimulation of the dorsolateral prefrontal cortex: A systematic review and meta-analysis. Brain Cogn 2014; 86: 1-9
• 73 Braz ID, Fisher JP. The impact of age on cerebral perfusion, oxygenation and metabolism during exercise in humans. J Physiol 2016; 594: 4471-4483
• 74 Ide K, Secher NH. Cerebral blood flow and metabolism during exercise. Prog Neurobiol 2000; 61: 397-414
• 75 Delp MD, Armstrong RB, Godfrey DA. et al. Exercise increases blood flow to locomotor, vestibular, cardiorespiratory and visual regions of the brain in miniature swine. J Physiol 2001; 533: 849-859
• 76 Reuter-Lorenz PA, Jonides J, Smith EE. et al. Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. J Cogn Neurosci 2000; 12: 174-187
• 77 Cwik JC, Vahle N, Woud ML. et al. Reduced gray matter volume in the left prefrontal, occipital, and temporal regions as predictors for posttraumatic stress disorder: A voxel-based morphometric study. Eur Arch Psychiatry Clin Neurosci 2019; 1-12
• 78 Sanders AF. Towards a model of stress and human performance. Acta Psychol 1983; 53: 61-97
• 79 Carnevali L, Pattini E, Sgoifo A. et al. Effects of prefrontal transcranial direct current stimulation on autonomic and neuroendocrine responses to psychosocial stress in healthy humans. Stress 2020; 23: 26-36
• 80 Woodcock EA, Greenwald MK, Khatib D. et al. Pharmacological stress impairs working memory performance and attenuates dorsolateral prefrontal cortex glutamate modulation. Neuroimage 2019; 186: 437-445
• 81 Chang YK, Labban JD, Gapin JI. et al. The effects of acute exercise on cognitive performance: A meta-analysis. Brain Res 2012; 1453: 87-101
• 82 Bediz CS, Oniz A, Guducu C. et al. Acute supramaximal exercise increases the brain oxygenation in relation to cognitive workload. Front Hum Neurosci 2016; 10: 174
• 83 Lucas SJ, Ainslie PN, Murrell CJ. et al. Effect of age on exercise-induced alterations in cognitive executive function: relationship to cerebral perfusion. Exp Gerontol 2012; 47: 541-551
• 84 Wintink AJ, Segalowitz SJ, Cudmore LJ. Task complexity and habituation effects on frontal P300 topography. Brain Cogn 2001; 46: 307-311
• 85 Gagnon L. et al. Short separation channel location impacts the performance of short channel regression in NIRS. Neuroimage 2012; 59: 2518-2528
• 86 Brigadoi S, Cooper RJ. How short is short? Optimum source–detector distance for short-separation channels in functional near-infrared spectroscopy. Neurophotonics 2015; 2: 025005
• 87 Perrey S. Non-invasive NIR spectroscopy of human brain function during exercise. Methods 2008; 45: 289-299
• 88 Strangman G, Boas DA, Sutton JP. Non-invasive neuroimaging using near-infrared light. Biol Psychiatry 2002; 52: 679-693