A transferable high-intensity intermittent exercise improves executive performance in association with dorsolateral prefrontal activation in young adults

ABSTRACT Although growing attention has been drawn to attainable, high‐intensity intermittent exercise (HIE)‐based intervention, which can improve cardiovascular and metabolic health, for sedentary individuals, there is limited information on the impact and potential benefit of an easily attainable HIE intervention for cognitive health. We aimed to reveal how acute HIE affects executive function focusing on underlying neural substrates. To address this issue, we examined the effects of acute HIE on executive function using the color‐word matching Stroop task (CWST), which produces a cognitive conflict in the decision‐making process, and its neural substrate using functional near infrared spectroscopy (fNIRS). Twenty‐five sedentary young adults (mean age: 21.0 ± 1.6 years; 9 females) participated in two counter‐balanced sessions: HIE and resting control. The HIE session consisted of two minutes of warm‐up exercise (50 W load at 60 rpm) and eight sets of 30 s of cycling exercise at 60% of maximal aerobic power (mean: 127 W ± 29.5 load at 100 rpm) followed by 30 s of rest on a recumbent‐ergometer. Participants performed a CWST before and after the 10‐minute exercise session, during both of which cortical hemodynamic changes in the prefrontal cortex were monitored using fNIRS. Acute HIE led to improved Stroop performance reflected by a shortening of the response time related to Stroop interference. It also evoked cortical activation related to Stroop interference on the left‐dorsal‐lateral prefrontal cortex (DLPFC), which corresponded significantly with improved executive performance. These results provide the first empirical evidence using a neuroimaging method, to our knowledge, that acute HIE improves executive function, probably mediated by increased activation of the task‐related area of the prefrontal cortex including the left‐DLPFC. HighlightsWe establish an attainable acute high‐intensity intermittent exercise (HIE) model.We examine how acute HIE affects executive performance using a Stroop task.We investigate the neural substrate for HIE‐induced behavioral changes with fNIRS.HIE‐improved performance is related with boosted dorsolateral prefrontal activation.HIE improves executive function in relation with task‐related prefrontal activation.

[1]  Leanna M. Ross,et al.  High-intensity interval training (HIIT) for patients with chronic diseases , 2016, Journal of sport and health science.

[2]  G. Lohmann,et al.  Color-Word Matching Stroop Task: Separating Interference and Response Conflict , 2001, NeuroImage.

[3]  Frithjof Kruggel,et al.  Near‐infrared spectroscopy can detect brain activity during a color–word matching Stroop task in an event‐related design , 2002, Human brain mapping.

[4]  Colin M. Macleod Half a century of research on the Stroop effect: an integrative review. , 1991, Psychological bulletin.

[5]  Jonathan D. Cohen,et al.  An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. , 2005, Annual review of neuroscience.

[6]  T. McMorris,et al.  A test of the catecholamines hypothesis for an acute exercise–cognition interaction , 2008, Pharmacology, Biochemistry and Behavior.

[7]  T. Venckunas,et al.  Interval Running Training Improves Cognitive Flexibility and Aerobic Power of Young Healthy Adults , 2016, Journal of strength and conditioning research.

[8]  Yosuke Sakairi,et al.  Development of the Two‐Dimensional Mood Scale for self‐monitoring and self‐regulation of momentary mood states , 2013 .

[9]  M. Tarnopolsky,et al.  Low-volume interval training improves muscle oxidative capacity in sedentary adults. , 2011, Medicine and science in sports and exercise.

[10]  P. Tomporowski,et al.  The effect of exercise-induced arousal on cognitive task performance: A meta-regression analysis , 2010, Brain Research.

[11]  S. Ogoh,et al.  Repeated high-intensity interval exercise shortens the positive effect on executive function during post-exercise recovery in healthy young males , 2016, Physiology & Behavior.

[12]  M. Tarnopolsky,et al.  Low-volume high-intensity interval training reduces hyperglycemia and increases muscle mitochondrial capacity in patients with type 2 diabetes. , 2011, Journal of applied physiology.

[13]  J. Ridley Studies of Interference in Serial Verbal Reactions , 2001 .

[14]  Ippeita Dan,et al.  Spatial registration for functional near-infrared spectroscopy: From channel position on the scalp to cortical location in individual and group analyses , 2014, NeuroImage.

[15]  Thomas Elbert,et al.  Dissociation in human prefrontal cortex of affective influences on working memory-related activity , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Ippeita Dan,et al.  Positive effect of acute mild exercise on executive function via arousal-related prefrontal activations: An fNIRS study , 2014, NeuroImage.

[17]  Frédéric Lesage,et al.  A fNIRS investigation of switching and inhibition during the modified Stroop task in younger and older adults , 2013, NeuroImage.

[18]  T. Hamaoka,et al.  Greater impact of acute high-intensity interval exercise on post-exercise executive function compared to moderate-intensity continuous exercise , 2016, Physiology & Behavior.

[19]  B. Franklin,et al.  American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. , 2011, Medicine and science in sports and exercise.

[20]  C. J. McGrath,et al.  Effect of exchange rate return on volatility spill-over across trading regions , 2012 .

[21]  J. Davis,et al.  Neuroendocrine and substrate responses to altered brain 5-HT activity during prolonged exercise to fatigue. , 1993, Journal of applied physiology.

[22]  Jonathan D. Bartlett,et al.  High-intensity interval running is perceived to be more enjoyable than moderate-intensity continuous exercise: Implications for exercise adherence , 2011, Journal of sports sciences.

[23]  Masako Okamoto,et al.  Mapping of optical pathlength of human adult head at multi-wavelengths in near infrared spectroscopy. , 2010, Advances in experimental medicine and biology.

[24]  Ippeita Dan,et al.  The association between aerobic fitness and cognitive function in older men mediated by frontal lateralization , 2016, NeuroImage.

[25]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

[26]  S. Siegel,et al.  Nonparametric Statistics for the Behavioral Sciences , 2022, The SAGE Encyclopedia of Research Design.

[27]  Masako Okamoto,et al.  Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping , 2004, NeuroImage.

[28]  M. Tarnopolsky,et al.  Acute high‐intensity interval exercise reduces the postprandial glucose response and prevalence of hyperglycaemia in patients with type 2 diabetes , 2012, Diabetes, obesity & metabolism.

[29]  J. Hawley,et al.  Physiological adaptations to low‐volume, high‐intensity interval training in health and disease , 2012, The Journal of physiology.

[30]  Wanda C. Stutts,et al.  Physical Activity Determinants in Adults , 2002, AAOHN journal : official journal of the American Association of Occupational Health Nurses.

[31]  J. N. Cameron Physiological adaptations. , 1981, Science.

[32]  H. Buschke,et al.  Leisure activities and the risk of dementia in the elderly. , 2003, The New England journal of medicine.

[33]  N. Cohen,et al.  The relative involvement of anterior cingulate and prefrontal cortex in attentional control depends on nature of conflict. , 2001, Brain research. Cognitive brain research.

[34]  T. Baguley Standardized or simple effect size: what should be reported? , 2009, British journal of psychology.

[35]  J. Foster,et al.  Effect of physical activity on cognitive function in older adults at risk for Alzheimer disease: a randomized trial. , 2008, JAMA.

[36]  Colin M. Macleod,et al.  Interdimensional interference in the Stroop effect: uncovering the cognitive and neural anatomy of attention , 2000, Trends in Cognitive Sciences.

[37]  J. Nielsen,et al.  Acute Exercise Improves Motor Memory Consolidation in Preadolescent Children , 2017, Front. Hum. Neurosci..

[38]  A F Kramer,et al.  Attentional selection and the processing of task-irrelevant information: insights from fMRI examinations of the Stroop task. , 2001, Progress in brain research.

[39]  R. Meeusen,et al.  Brain Microdialysis in Exercise Research , 2001, Sports medicine.

[40]  R. Dishman Brain monoamines, exercise, and behavioral stress: animal models. , 1997, Medicine and science in sports and exercise.

[41]  A. Kramer,et al.  Be smart, exercise your heart: exercise effects on brain and cognition , 2008, Nature Reviews Neuroscience.

[42]  A. Sockloff,et al.  Statistical power analysis for the behavioral sciences: (revised edition), by Jacob Cohen. New York: Academic Press, 1977, xv + 474 pp., $24.50. , 1978 .

[43]  T. Karlsen,et al.  Aerobic high-intensity intervals improve VO2max more than moderate training. , 2007, Medicine and science in sports and exercise.

[44]  M. Tarnopolsky,et al.  Interval training in the fed or fasted state improves body composition and muscle oxidative capacity in overweight women , 2013, Obesity.

[45]  Masako Okamoto,et al.  Virtual spatial registration of stand-alone fNIRS data to MNI space , 2007, NeuroImage.

[46]  I. Dan,et al.  Acute moderate exercise enhances compensatory brain activation in older adults , 2012, Neurobiology of Aging.

[47]  Frithjof Kruggel,et al.  Age dependency of the hemodynamic response as measured by functional near-infrared spectroscopy , 2003, NeuroImage.

[48]  Masako Okamoto,et al.  Automated cortical projection of head-surface locations for transcranial functional brain mapping , 2005, NeuroImage.

[49]  A. Bauman,et al.  Correlates of adults' participation in physical activity: review and update. , 2002, Medicine and science in sports and exercise.

[50]  A. Arnsten Catecholamine Influences on Dorsolateral Prefrontal Cortical Networks , 2011, Biological Psychiatry.

[51]  Arthur F. Kramer,et al.  fMRI Studies of Stroop Tasks Reveal Unique Roles of Anterior and Posterior Brain Systems in Attentional Selection , 2000, Journal of Cognitive Neuroscience.

[52]  M. Tarnopolsky,et al.  A practical model of low‐volume high‐intensity interval training induces mitochondrial biogenesis in human skeletal muscle: potential mechanisms , 2010, The Journal of physiology.

[53]  E. Watanabe,et al.  Spatial and temporal analysis of human motor activity using noninvasive NIR topography. , 1995, Medical physics.

[54]  Arne Dietrich,et al.  The reticular-activating hypofrontality (RAH) model of acute exercise , 2011, Neuroscience & Biobehavioral Reviews.

[55]  Arthur W. Toga,et al.  Construction of a 3D probabilistic atlas of human cortical structures , 2008, NeuroImage.

[56]  J. Hallén,et al.  High‐Intensity Interval Training Improves Peak Oxygen Uptake and Muscular Exercise Capacity in Heart Transplant Recipients , 2012, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[57]  M. Buckley,et al.  Transcranial magnetic stimulation to dorsolateral prefrontal cortex affects conflict-induced behavioural adaptation in a Wisconsin Card Sorting Test analogue , 2017, Neuropsychologia.

[58]  M. Milham,et al.  Competition for priority in processing increases prefrontal cortex's involvement in top-down control: an event-related fMRI study of the stroop task. , 2003, Brain research. Cognitive brain research.

[59]  Thomas A Hammeke,et al.  Neural basis of the Stroop interference task: Response competition or selective attention? , 2002, Journal of the International Neuropsychological Society.

[60]  J. Faulkner,et al.  The effectiveness of a high-intensity games intervention on improving indices of health in young children , 2016, Journal of sports sciences.

[61]  L. Leyman,et al.  The influence of rTMS over the left dorsolateral prefrontal cortex on Stroop task performance , 2006, Experimental Brain Research.

[62]  D. Delpy,et al.  Methods of quantitating cerebral near infrared spectroscopy data. , 1988, Advances in experimental medicine and biology.

[63]  I. Johnsrude,et al.  The problem of functional localization in the human brain , 2002, Nature Reviews Neuroscience.

[64]  T. McMorris History of Research into the Acute Exercise–Cognition Interaction: A Cognitive Psychology Approach , 2016 .

[65]  Carl Doss A Test for , 2009 .

[66]  A. Arnsten Catecholamine modulation of prefrontal cortical cognitive function , 1998, Trends in Cognitive Sciences.

[67]  R. Westendorp,et al.  Leisure activities and the risk of dementia. , 2003, The New England journal of medicine.

[68]  M. Fiatarone Singh,et al.  A randomized controlled trial of high versus low intensity weight training versus general practitioner care for clinical depression in older adults. , 2005, The journals of gerontology. Series A, Biological sciences and medical sciences.

[69]  T. McMorris,et al.  Beyond the Catecholamines Hypothesis for an Acute Exercise–Cognition Interaction: A Neurochemical Perspective , 2016 .

[70]  H. Roschel,et al.  Influence of Acute High-Intensity Aerobic Interval Exercise Bout on Selective Attention and Short-Term Memory Tasks , 2014, Perceptual and motor skills.

[71]  W. B. Webb,et al.  What is a test? , 1955, Medical technicians bulletin.

[72]  B. Winblad,et al.  Leisure-time physical activity at midlife and the risk of dementia and Alzheimer's disease , 2005, The Lancet Neurology.

[73]  Y. Michotte,et al.  Acute running stimulates hippocampal dopaminergic neurotransmission in rats, but has no influence on brain-derived neurotrophic factor. , 2012, Journal of applied physiology.

[74]  D. Bishop,et al.  An acute bout of high-intensity interval training increases the nuclear abundance of PGC-1α and activates mitochondrial biogenesis in human skeletal muscle. , 2011, American journal of physiology. Regulatory, integrative and comparative physiology.

[75]  Jacob Cohen Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[76]  A. Björklund,et al.  Dopamine neuron systems in the brain: an update , 2007, Trends in Neurosciences.

[77]  D. Laude,et al.  Amphetamine and α-methyl-p-tyrosine affect the exercise-induced imbalance between the availability of tryptophan and synthesis of serotonin in the brain of the rat , 1987, Neuropharmacology.

[78]  M. Kurosawa,et al.  Extracellular release of acetylcholine, noradrenaline and serotonin increases in the cerebral cortex during walking in conscious rats , 1993, Neuroscience Letters.

[79]  C. Cotman,et al.  Exercise: a behavioral intervention to enhance brain health and plasticity , 2002, Trends in Neurosciences.

[80]  M. Grierson,et al.  The effect of exercise-induced arousal on chosen tempi for familiar melodies , 2014, Psychonomic Bulletin & Review.

[81]  J S Fowler,et al.  PET studies of the effects of aerobic exercise on human striatal dopamine release. , 2000, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[82]  Masako Okamoto,et al.  Acute moderate exercise elicits increased dorsolateral prefrontal activation and improves cognitive performance with Stroop test , 2010, NeuroImage.