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The acute effect of moderate-intensity exercise on inhibitory control and activation of prefrontal cortex in younger and older adults

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Abstract

Exercise has a significant effect on maintaining the health of inhibitory function, a fundamental cognitive ability that supports daily mental processes. While previous studies have shown that a single bout of exercise, called acute exercise, could improve inhibitory control by stimulating the prefrontal cortex (PFC) and the arousal state, few studies have focused on the differences in the effects of exercise by age. In this study, young and older adults (mean age, 22.7 ± 1.4 and 68.7 ± 5.3 years, respectively) engaged in acute moderate-intensity exercise and inhibitory control. Before and at 5 and 30 min after exercise, the participants were asked to complete the reverse Stroop task, and their arousal state and PFC activity were measured using functional near-infrared spectroscopy. The findings showed that the overall inhibitory control improved immediately after performing acute exercise and remained improved even after 30 min. Particularly, there was a difference in the arousal state and middle PFC activity between the two age groups. Especially, the young adults showed an increase in the arousal state post-exercise, while the older adults tended to show an increase in the middle PFC activity. These results suggested that the acute exercise effects on the arousal state and PFC activity may vary depending on the developmental stage, but not for inhibitory control overtime. When these findings are considered, it is important to note that the exercise impact on cognitive control remained the same throughout the generations despite the observed changes in its impact on internal states.

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References

  • Banich MT, Milham MP, Atchley R, Cohen NJ, Webb A, Wszalek T, Kramer AF, Liang ZP, Wright A, Shenker J, Magin R (2000) fMri studies of Stroop tasks reveal unique roles of anterior and posterior brain systems in attentional selection. J Cogn Neurosci 12:988–1000

    Article  CAS  PubMed  Google Scholar 

  • Banich MT, Milham MP, Jacobson BL, Webb A, Wszalek T, Cohen NJ, Kramer AF (2001) Attentional selection and the processing of task-irrelevant information: insights from fMRI examinations of the Stroop task. Prog Brain Res 134:459–470

    Article  CAS  PubMed  Google Scholar 

  • Baudic S, Tzortzis C, Dalla Barba G, Traykov L (2004) Executive deficits in elderly patients with major unipolar depression. J Geriatr Psychiatry Neurol 17:195–201

    Article  PubMed  Google Scholar 

  • Blais C, Besner D (2006) Reverse Stroop effects with untranslated responses. J Exp Psychol Hum Percept Perform 32:1345–1353

    Article  PubMed  Google Scholar 

  • Blais C, Besner D (2007) Reading aloud: when the effect of stimulus quality distinguishes between cascaded and thresholded components. Exp Psychol 54:215–224

    Article  PubMed  Google Scholar 

  • Borg G (1998) Borg’s perceived exertion and pain scales. Human Kinetics, Illinois

    Google Scholar 

  • Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD (2001) Conflict monitoring and cognitive control. Psychol Rev 108:624–652

    Article  CAS  PubMed  Google Scholar 

  • Bradley MM, Miccoli L, Escrig MA, Lang PJ (2008) The pupil as a measure of emotional arousal and automatic activation. Psychophysiology 45:602–607

    Article  PubMed  PubMed Central  Google Scholar 

  • Butters MA, Whyte EM, Nebes RD, Begley AE, Dew MA, Mulsant BH, Zmada MD, Bhalla R, Meltzer CC, Pollock BG, Reynolds CF, Becker JT (2004) The nature and determinants of neuropsychological functioning in late-life depression. Arch Gen Psychiatry 61:587–595

    Article  PubMed  Google Scholar 

  • Byun K, Hyodo K, Suwabe K, Ochi G, Sakairi Y, Kato M, Dan I, Soya H (2014) Positive effect of acute mild exercise on executive function via arousal-related prefrontal activations: An fNIRS study. Neuroimage 98:336–345

    Article  PubMed  Google Scholar 

  • Chang YK, Labban J, Gapin JI, Etnier J (2012) The effects of acute exercise on cognitive performance: a meta-analysis. Brain Res 1453:87–101

    Article  CAS  PubMed  Google Scholar 

  • Chu CH, Kramer AF, Song TF, Wu CH, Hung TM, Chang YK (2017) Acute exercise and neurocognitive development in preadolescents and young adults: an ERP study. Neural Plast 2017:2631909

    Article  PubMed  PubMed Central  Google Scholar 

  • Comalli PE Jr, Wapner S, Werner H (1962) Interference effects of Stroop color-word test in childhood, adulthood, and aging. J Genet Psychol 100:47–53

    Article  PubMed  Google Scholar 

  • Craig A (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666

    Article  CAS  PubMed  Google Scholar 

  • Critchley HD, Tang J, Glaser D, Butterworth B, Dolan RJ (2005) Anterior cingulate activity during error and autonomic response. Neuroimage 27:885–895

    Article  PubMed  Google Scholar 

  • Del Giorno JM, Hall EE, O’Leary KC, Bixby WR, Miller PC (2010) Cognitive function during acute exercise: a test of the transient hypofrontality theory. J Sport Exerc Psychol 32:312–323

    Article  PubMed  Google Scholar 

  • Demetriou EA, Lampit A, Quintana DS, Naismith SL, Song YJC, Pye JE, Hickie I, Guastella AJ (2018) Autism spectrum disorders: a meta-analysis of executive function. Mol Psychiatry 23:1198–1204

    Article  CAS  PubMed  Google Scholar 

  • Dupuy FE, Clarke AR, Barry RJ, Selikowitz M, McCarthy R (2014) EEG and electrodermal activity in girls with attention-deficit/hyperactivity disorder. Clin Neurophysiol 125:491–499

    Article  CAS  PubMed  Google Scholar 

  • Dupuy O, Gauthier CJ, Fraser SA, Desjardins-Crèpeau L, Desjardins M, Mekary S, Lesage F, Hoge RD, Pouliot P, Bherer L (2015) Higher levels of cardiovascular fitness are associated with better executive function and prefrontal oxygenation in younger and older women. Front Hum Neurosci 9:66

    Article  PubMed  PubMed Central  Google Scholar 

  • Ebbeling CB, Ward A, Puleo EM, Widrick J, Rippe JM (1991) Development of a single-stage submaximal treadmill walking test. Med Sci Sports Exerc 23:966–973

    Article  CAS  PubMed  Google Scholar 

  • Faulkner J, Stoner L, Grigg R, Fryer S, Stone K, Lambrick D (2017) Acute effects of exercise posture on executive function in transient ischemic attack patients. Psychophysiology 54:1239–1248

    Article  PubMed  Google Scholar 

  • Friedman NP, Miyake A (2004) The relations among inhibition and interference control functions: a latent-variable analysis. J Exp Psychol General 133:101–135

    Article  Google Scholar 

  • Hama H, Hashimoto E (1985) Change in conflict strength measured by color-word test in childhood, adulthood, and the aged. Shinrigaku Kenkyu 56:175–179

    Article  CAS  PubMed  Google Scholar 

  • Hasher L, Zacks RT (1988) Working memory, comprehension, and aging: a review and a new view. Psychol Learn Motiv 22:193–225

    Article  Google Scholar 

  • Herold F, Wiegel P, Scholkmann F, Müller NG (2018) Applications of functional near-infrared spectroscopy (fNIRS) neuroimaging in exercise-cognition science: a systematic, methodology-focused review. J Clin Med 7:E466

    Article  PubMed  Google Scholar 

  • Hillman CH, Pontifex MB, Raine LB, Castelli DM, Hall EE, Kramer AF (2009) The effect of acute treadmill walking on cognitive control and academic achievement in preadolescent children. Neuroscience 159:1044–1054

    Article  CAS  PubMed  Google Scholar 

  • Hogan CL, Mata J, Carstensen LL (2013) Exercise holds immediate benefits for affect and cognition in younger and older adults. Psychol Aging 28:587–594

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoshi Y, Kobayashi N, Tamura M (2001) Interpretation of near-infrared spectroscopy signals: a study with a newly developed perfused rat brain model. J Appl Physiol 90:1657–1662

    Article  CAS  PubMed  Google Scholar 

  • Humphreys MS, Revelle W (1984) Personality, motivation, and performance: a theory of the relationship between individual differences and information processing. Psychol Rev 91:153–184

    Article  CAS  PubMed  Google Scholar 

  • Hyodo K, Dan I, Suwabe K, Kyutoku Y, Yamada Y, Akahori M, Byun K, Kato M, Soya H (2012) Acute moderate exercise enhances compensatory brain activation in older adults. Neurobiol Aging 33:2621–2632

    Article  PubMed  Google Scholar 

  • Hyodo K, Suwabe K, Soya H, Nagamatsu T (2017) The effect of an acute bout of slow aerobic dance on mood and executive function in older adults: a pilot study. Bull Phys Fitness Res Inst 115:35–41

    Google Scholar 

  • Joyce J, Graydon J, McMorris T, Davranche K (2009) The time course effect of moderate intensity exercise on response execution and response inhibition. Brain Cogn 71:14–19

    Article  PubMed  Google Scholar 

  • Kamijo K, Hayashi Y, Sakai T, Yahiro T, Tanaka K, Nishihira Y (2009) Acute effects of aerobic exercise on cognitive function in older adults. J Gerontol B Psychol Sci Soc Sci 64B:356–363

    Article  Google Scholar 

  • Karvonen MJ, Kentala E, Mustala O (1957) The effects of training on heart rate: a longitudinal study. Ann Med Exp Biol Fenn 35:307–315

    CAS  PubMed  Google Scholar 

  • Khalsa SS, Lapidus RC (2016) Can Interoception improve the pragmatic search for biomarkers in psychiatry? Front Psychiatry 7:121

    Article  PubMed  PubMed Central  Google Scholar 

  • Kimura A, Okada K, Sato A, Suzuki H (1994) Regional cerebral blood flow in the frontal, parietal and occipital cortices increases independently of systemic arterial pressure during slow walking in conscious rats. Neurosci Res 20:309–315

    Article  CAS  PubMed  Google Scholar 

  • Kita Y, Gunji A, Inoue Y, Goto T, Sakihara K, Kaga M, Inagaki M, Hosokawa T (2011) Self-face recognition in children with autism spectrum disorders: a near-infrared spectroscopy study. Brain Dev 33:494–503

    Article  PubMed  Google Scholar 

  • Kurosawa M, Okada K, Sato A, Uchida S (1993) Extracellular release of acetylcholine, noradrenaline and serotonin increases in the cerebral cortex during walking in conscious rats. Neurosci Lett 161:73–76

    Article  CAS  PubMed  Google Scholar 

  • American College of Sports Medicine (2014) ACSM’s guidelines for exercise testing and prescription, 9th edn. Lippincott Williams & Wilkins, Baltimore. http://antoinedl.com/fichiers/public/ACSM-guidelines-2014.pdf. Accessed 26 Mar 2020

  • Lowenstein O, Feinberg R, Loewenfeld IE (1963) Pupillary movements during acute and chronic fatigue. Invest Ophthalmol Vis Sci 2:138–157

    Google Scholar 

  • MacLeod CM (1991) Half a century of research on the Stroop effect: an integrative review. Psychol Bull 109:163–203

    Article  CAS  PubMed  Google Scholar 

  • Matsuda G, Hiraki K (2006) Sustained decrease in oxygenated hemoglobin during video games in the dorsal prefrontal cortex: a NIRS study of children. Neuroimage 29:706–711

    Article  PubMed  Google Scholar 

  • Matsuda K, Ikeda S, Mitsutake T, Nakahara M, Nagai Y, Ikeda T, Horikawa E (2017) Factors influencing executive function by physical activity level among young adults: a near-infrared spectroscopy study. J Phys Ther Sci 29:470–475

    Article  PubMed  PubMed Central  Google Scholar 

  • Matsumoto A, Hakoda Y, Watanabe M (2012) Life-span development of Stroop and reverse-Stroop interference measured using matching responses. Shinrigaku Kenkyu 83:337–346

    Article  PubMed  Google Scholar 

  • Mead LA, Mayer AR, Bobholz JA, Woodley SJ, Cunningham JM, Hammeke TA, Rao SM (2002) Neural basis of the Stroop interference task: response competition or selective attention? J Int Neuropsychol Soc 8:735–742

    Article  PubMed  Google Scholar 

  • Milham MP, Erickson KI, Banich MT, Kramer AF, Webb A, Wszalek T, Cohen NJ (2002) Attentional control in the aging brain: insights from an fMRI study of the Stroop task. Brain Cogn 49:277–296

    Article  PubMed  Google Scholar 

  • Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD (2000) The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: a latent variable analysis. Cogn Psychol 41:49–100

    Article  CAS  PubMed  Google Scholar 

  • Moriguchi Y, Hiraki K (2009) Neural origin of cognitive shifting in young children. Proc Natl Acad Sci USA 106:6017–6021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murata Y, Watanabe T, Terasawa S, Nakajima K, Kobayashi T, Yong Z, Okuhara M, Nakade K, Terasawa K, Maruo SK (2015) Moderate exercise improves cognitive performance and decreases cortical activation in the go/no-go task. BAOJ Med Nurs 1:002

    Google Scholar 

  • Nemeth BA, Carrel AL, Eickhoff J, Clark RR, Peterson SE, Allen DB (2009) Submaximal treadmill test predicts VO2max in overweight children. J Pediatr 154:677–681

    Article  PubMed  Google Scholar 

  • Netz Y, Abu-Rukun M, Tsuk S, Dwolatzky T, Carasso R, Levin O, Dunsky A (2016) Acute aerobic activity enhances response inhibition for less than 30 min. Brain Cogn 109:59–65

    Article  PubMed  Google Scholar 

  • Nguyen-Tri D, Overbury O, Faubert J (2003) The role of lenticular senescence in age-related color vision changes. Invest Ophthalmol Vis Sci 44:3698–3704

    Article  PubMed  Google Scholar 

  • Noonan V, Dean E (2000) Submaximal exercise testing: clinical application and interpretation. Phys Ther 80:782–807

    Article  CAS  PubMed  Google Scholar 

  • Pardo JV, Pardo PJ, Janer KW, Raichle ME (1990) The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. Proc Natl Acad Sci USA 87:256–259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Physical Activity Guidelines Advisory Committee (2008) Physical activity guidelines advisory committee report. U.S. Department of Health and Human Services, Washington, DC

    Google Scholar 

  • Pokorny J, Smith VC, Lutze M (1987) Aging of the human lens. Appl Opt 26:1437–1440

    Article  CAS  PubMed  Google Scholar 

  • Pontifex MB, Hillman CH, Fernhall B, Thompson KM, Valentini TA (2009) The effect of acute aerobic and resistance exercise on working memory. Med Sci Sports Exerc 41:927–934

    Article  PubMed  Google Scholar 

  • Raven JC, Court JH, Raven J (1976) Manual for Raven’s coloured progressive matrices. H K Lewis, London

    Google Scholar 

  • Robbins TW (1997) Arousal systems and attentional processes. Biol Psychol 45:57–71

    Article  CAS  PubMed  Google Scholar 

  • Rushworth MFS, Walton ME, Kennerley SW, Bannerman DM (2004) Action sets and decisions in the medial frontal cortex. Trends Cogn Sci 8:410–417

    Article  CAS  PubMed  Google Scholar 

  • Sakairi Y, Nakatsuka K, Shimizu T (2013) Development of the two-dimensional mood scale for self-monitoring and self-regulation of momentary mood states. Jpn Psychol Res 55:338–349

    Article  Google Scholar 

  • Schweitzer I, Tuckwell V, O’Brien J, Ames D (2002) Is late onset depression a prodrome to dementia? Int J Geriatr Psychiatry 17:997–1005

    Article  PubMed  Google Scholar 

  • Sheline YI, Barch DM, Garcia K, Gersing K, Pieper C, Welsh-Bohmer K, Steffens DC, Doraiswamy PM (2006) Cognitive function in late life depression: relationships to depression severity, cerebrovascular risk factors and processing speed. Biol Psychiatry 60:58–65

    Article  PubMed  Google Scholar 

  • Shimada S, Hiraki K (2006) Infant’s brain responses to live and televised action. Neuroimage 32:930–939

    Article  PubMed  Google Scholar 

  • Strangman G, Culver JP, Thompson JH, Boas DA (2002) A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. Neuroimage 17:719–731

    Article  PubMed  Google Scholar 

  • Stroop JR (1935) Studies of interference in serial verbal reactions. J Exp Psychol 18:643–662

    Article  Google Scholar 

  • Sudo M, Komiyama T, Aoyagi R, Nagamatsu T, Higaki Y, Ando S (2017) Executive function after exhaustive exercise. Eur J Appl Physiol 117:2029–2038

    Article  PubMed  Google Scholar 

  • Tang SW, Chu E, Hui T, Helmeste D, Law C (2008) Influence of exercise on serum brain-derived neurotrophic factor concentrations in healthy human subjects. Neurosci Lett 431:65–65

    Article  CAS  Google Scholar 

  • Terasawa Y, Fukushima H, Umeda S (2013) How does interoceptive awareness interact with the subjective experience of emotion? An fMRI study. Hum Brain Mapp 34:598–612

    PubMed  Google Scholar 

  • Tomporowski PD, Ganio MS (2006) Short-term effects of aerobic exercise on executive processing, memory, and emotional reactivity. Int J Sport Exerc Psychol 4:57–72

    Article  Google Scholar 

  • Tsujii T, Komatsu K, Sakatani K (2013) Acute effects of physical exercise on prefrontal cortex activity in older adults: a functional near-infrared spectroscopy study. Adv Exp Med Biol 765:293–298

    Article  CAS  PubMed  Google Scholar 

  • Villringer A, Chance B (1997) Non-invasive optical spectroscopy and imaging of human brain function. Trends Neurosci 20:435–442

    Article  CAS  PubMed  Google Scholar 

  • Waddoups L, Wagner D, Fallon J, Heath E (2008) Validation of a single-stage submaximal treadmill walking test. J Sports Sci 26:491–497

    Article  PubMed  Google Scholar 

  • Wang W, Qiu C, Ota T, Sawada M, Kishimoto N, Kishimoto T (2013) Effects of Tai-Chi exercise on attention in healthy elderly subjects as measured by near-infrared spectroscopy during the Stroop task. J Nara Med Assoc 64:79–86

    Google Scholar 

  • World Health Organization (2010) Global recommendations on physical activity for health. WHO Press, Switzerland. https://www.who.int/dietphysicalactivity/global-PA-recs-2010.pdf. Accessed 15 Apr 2020

  • Wyczesany M, Kaiser J, Coenen AML (2008) Subjective mood estimation co-varies with spectral power EEG characteristics. Acta Neurobiol Exp (Wars) 68:180–192

    Google Scholar 

  • Yamagata S, Takahashi Y, Shigemasu K, Ono Y, Kijima N (2005) Development and validation of Japanese version of effortful control scale for adults. Jap J Pers 14:30–41

    Google Scholar 

  • Yamazaki Y, Sato D, Yamashiro K, Tsubaki A, Yamaguchi Y, Takehara N, Maruyama A (2017) Inter-individual differences in exercise-induced spatial working memory improvement: a near infra-red spectroscopy study. Adv Exp Med Biol 977:81–88

    Article  CAS  PubMed  Google Scholar 

  • Yanagisawa H, Dan I, Tsuzuki D, Kato M, Okamoto M, Kyutoku Y, Soya H (2010) Acute moderate exercise elicits increased dorsolateral prefrontal activation and improves cognitive performance with Stroop test. Neuroimage 50:1702–1710

  • Yasumura A, Kokubo N, Yamamoto H, Yasumura Y, Nakagawa E, Kaga M, Hiraki K, Inagaki M (2014) Neurobehavioral and hemodynamic evaluation of Stroop and reverse Stroop interference in children with attention-deficit/hyperactivity disorder. Brain Dev 36:97–106

    Article  PubMed  Google Scholar 

  • Yasumura A, Omori M, Fukuda A, Takahashi J, Yasumura Y, Nakagawa E, Koike T, Yamashita Y, Miyajima T, Koeda T, Aihara M, Inagaki M (2019) Age-related differences in frontal lobe function in children with ADHD. Brain Dev 41:577–586

    Article  PubMed  Google Scholar 

  • Zillmann D (1979) Hostility and aggression. Wiley, New York

    Google Scholar 

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Acknowledgements

The authors would like to thank the staff members of Higashi Clinic and h3 Support in Tamana city, Japan, for their support during our research, when the main results of this paper were obtained. We also thank Editage (https://www.editage.com) for English editing. This work was supported by the Japan Society for the Promotion of Science KAKENHI Grants 19K14300 and 19H00631 to AY and WT, respectively.

Funding

This work was supported by the Japan Society for the Promotion of Science KAKENHI Grants 19K14300 and 19H00631 to AY and WT, respectively.

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Authors and Affiliations

  1. Graduate School of Education, Kyoto University, Yoshida Honmachi, Sakyo-ku, Kyoto, 606-8501, Japan

    Hideaki Fujihara

  2. Faculty of Education, Kumamoto University, 2-40-1 Kurokami, Kumamoto, 860-8555, Japan

    Hideaki Fujihara

  3. Graduate School of Social and Cultural Sciences, Kumamoto University, 2-40-1 Kurokami, Kumamoto, 860-8555, Japan

    Akiko Megumi

  4. Graduate School of Humanities and Social Sciences, Kumamoto University, 2-40-1 Kurokami, Kumamoto, 860-8555, Japan

    Akira Yasumura

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  1. Hideaki Fujihara
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Contributions

HF analyzed and corrected the participants’ data regarding behavioral and neural indices, and was a major contributor in writing the manuscript. AM and AY corrected and analyzed the data on the participants’ medical history and organized the experiments. All authors read and approved the final manuscript.

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Correspondence to Hideaki Fujihara.

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The Ethics Committee of the Graduate School of Social and Cultural Sciences of Kumamoto University approved this study (Approval number: 45, 2020).

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Communicated by Winston D. Byblow.

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Fujihara, H., Megumi, A. & Yasumura, A. The acute effect of moderate-intensity exercise on inhibitory control and activation of prefrontal cortex in younger and older adults. Exp Brain Res 239, 1765–1778 (2021). https://doi.org/10.1007/s00221-021-06086-9

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