Frequent, Short Physical Activity Breaks Reduce Prefrontal Cortex Activation but Preserve Working Memory in Middle-Aged Adults: ABBaH Study

Emerald G Heiland, Olga Tarassova, Maria Fernström, Coralie English, Örjan Ekblom, Maria M Ekblom, Emerald G Heiland, Olga Tarassova, Maria Fernström, Coralie English, Örjan Ekblom, Maria M Ekblom

Abstract

Prolonged sitting is increasingly common and may possibly be unfavorable for cognitive function and mood. In this randomized crossover study, the effects of frequent, short physical activity breaks during prolonged sitting on cognitive task-related activation of the prefrontal cortex were investigated. The effects on working memory, psychological factors, and blood glucose were also examined, and whether arterial stiffness moderated prefrontal cortex activation. Thirteen subjects (mean age 50.5 years; eight men) underwent three 3-h sitting conditions, interrupted every 30-min by a different 3-min break on separate, randomized-ordered days: seated social interactions (SOCIAL), walking (WALK), or simple resistance activities (SRA). Arterial stiffness was assessed at baseline. Before and after each 3-h condition, psychological factors (stress, mood, sleepiness, and alertness) were assessed through questionnaires and functional near-infrared spectroscopy (fNIRS) was used to measure changes in prefrontal oxygenated hemoglobin (Oxy-Hb), indicative of cortical activation, while performing working memory tasks [1- (baseline), 2-, and 3-back]. Blood glucose levels were continuously measured throughout the conditions. Results revealed no significant changes in Oxy-Hb during the 2-back compared with the 1-back test in any condition, and no time-by-condition interactions. During the 3-back test, there was a significant decrease in Oxy-Hb compared with the 1-back after the WALK condition in the right prefrontal cortex, but there were no time-by-condition interactions, although 3-back reaction time improved only in the WALK condition. Mood and alertness improved after the WALK condition, which was significantly different from the SOCIAL condition. Arterial stiffness moderated the effects, such that changes in Oxy-Hb were significantly different between WALK and SOCIAL conditions only among those with low arterial stiffness. Blood glucose during the interventions did not differ between conditions. Thus, breaking up prolonged sitting with frequent, short physical activity breaks may reduce right prefrontal cortex activation, with improvements in some aspects of working memory, mood, and alertness. Clinical Trial Registration:www.ClinicalTrials.gov, identifier NCT04137211.

Keywords: cerebral blood flow; cognition; exercise; functional near-infrared spectroscopy; sedentary.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2021 Heiland, Tarassova, Fernström, English, Ekblom and Ekblom.

Figures

FIGURE 1
FIGURE 1
Change in oxygenated hemoglobin (Oxy-Hb) during 1-back, 2-back, and 3-back cognitive tasks from pre-test to post-test, in the whole prefrontal cortex (A) and separated by left (B) and right (C) hemisphere. CI, confidence interval; SOCIAL, social break condition; WALK, walking break condition; SRA, simple resistance activity break condition. *Significant differences within conditions or compared to the baseline (1-back), q-values ≤ 0.05 (FDR-adjusted p-values for multiple comparisons).
FIGURE 2
FIGURE 2
Changes in oxygenated hemoglobin (Oxy-Hb) in the left and right prefrontal cortex among those with (A) high arterial stiffness (n = 7) and (B) low arterial stiffness (n = 6), during the 1-back, 2-back, and 3-back tasks from pre-test to post-test. CI, confidence interval; SOCIAL, social break condition; WALK, walking break condition; SRA, simple resistance activity break condition. *Significant differences within conditions or compared to the baseline (1-back), q-values ≤ 0.05 (FDR-adjusted p-values for multiple comparisons).

References

    1. Agbangla N. F., Audiffren M., Pylouster J., Albinet C. T. (2019). Working memory, cognitive load andcardiorespiratory fitness: testing the CRUNCH model with near-infrared spectroscopy. Brain Sci. 9:38. 10.3390/brainsci9020038
    1. Baddeley A. D., Hitch G. J. (1994). Developments in the concept of working memory. Neuropsychology 8 485–493. 10.1037/0894-4105.8.4.485
    1. Barker J. W., Aarabi A., Huppert T. J. (2013). Autoregressive model based algorithm for correcting motion and serially correlated errors in fNIRS. Biomed. Opt. Express 4 1366–1379. 10.1364/boe.4.001366
    1. Bediz C. S., Oniz A., Guducu C., Ural Demirci E., Ogut H., Gunay E., et al. (2016). Acute supramaximal exercise increases the brain oxygenation in relation to cognitive workload. Front. Hum. Neurosci. 10:174.
    1. Bojsen-Møller E., Ekblom M. M., Tarassova O., Dunstan D. W., Ekblom O. (2020). The effect of breaking up prolonged sitting on paired associative stimulation-induced plasticity. Exp. Brain Res. 238 2497–2506. 10.1007/s00221-020-05866-z
    1. Brehmer Y., Kalpouzos G., Wenger E., Lövdén M. (2014). Plasticity of brain and cognition in older adults. Psychol. Res. 78 790–802. 10.1007/s00426-014-0587-z
    1. Butlin M., Qasem A. (2017). Large Artery stiffness assessment using sphygmocor technology. Pulse 4 180–192. 10.1159/000452448
    1. Byun K., Hyodo K., Suwabe K., Ochi G., Sakairi Y., Kato M., et al. (2014). Positive effect of acute mild exercise on executive function via arousal-related prefrontal activations: an fNIRS study. Neuroimage 98 336–345. 10.1016/j.neuroimage.2014.04.067
    1. Carter S. E., Draijer R., Holder S. M., Brown L., Thijssen D. H. J., Hopkins N. D. (2018). Regular walking breaks prevent the decline in cerebral blood flow associated with prolonged sitting. J. Appl. Physiol. 125 790–798. 10.1152/japplphysiol.00310.2018
    1. Chandrasekaran B., Pesola A. J., Rao C. R., Arumugam A. (2021). Does breaking up prolonged sitting improve cognitive functions in sedentary adults? A mapping review and hypothesis formulation on the potential physiological mechanisms. BMC Musculoskelet. Disord. 22:274. 10.1186/s12891-021-04136-5
    1. Chang Y. K., Labban J. D., Gapin J. I., Etnier J. L. (2012). The effects of acute exercise on cognitive performance: a meta-analysis. Brain Res. 1453 87–101. 10.1016/j.brainres.2012.02.068
    1. Charlett O. P., Morari V., Bailey D. P. (2021). Impaired postprandial glucose and no improvement in other cardiometabolic responses or cognitive function by breaking up sitting with bodyweight resistance exercises: a randomised crossover trial. J. Sports Sci. 39 792–800. 10.1080/02640414.2020.1847478
    1. Chrismas B. C. R., Taylor L., Cherif A., Sayegh S., Bailey D. P. (2019). Breaking up prolonged sitting with moderate-intensity walking improves attention and executive function in Qatari females. PLoS One 14:e0219565. 10.1371/journal.pone.0219565
    1. Coetsee C., Terblanche E. (2017). Cerebral oxygenation during cortical activation: the differential influence of three exercise training modalities. A randomized controlled trial. Eur. J. Appl. Physiol. 117 1617–1627. 10.1007/s00421-017-3651-8
    1. Colcombe S. J., Erickson K. I., Scalf P. E., Kim J. S., Prakash R., McAuley E., et al. (2006). Aerobic exercise training increases brain volume in aging humans. J. Gerontol. A Biol. Sci. Med. Sci. 61 1166–1170. 10.1093/gerona/61.11.1166
    1. Colcombe S., Kramer A. F. (2003). Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol. Sci. 14 125–130. 10.1111/1467-9280.t01-1-01430
    1. Crawford J. R., Henry J. D. (2004). The positive and negative affect schedule (PANAS): construct validity, measurement properties and normative data in a large non-clinical sample. Br. J. Clin. Psychol. 43 245–265. 10.1348/0144665031752934
    1. da Silva de Vargas L., Neves B.-H. S. D., Roehrs R., Izquierdo I., Mello-Carpes P. (2017). One-single physical exercise session after object recognition learning promotes memory persistence through hippocampal noradrenergic mechanisms. Behav. Brain Res. 329 120–126. 10.1016/j.bbr.2017.04.050
    1. Dempsey P. C., Larsen R. N., Sethi P., Sacre J. W., Straznicky N. E., Cohen N. D., et al. (2016a). Benefits for Type 2 Diabetes of Interrupting Prolonged Sitting With Brief Bouts of Light Walking or Simple Resistance Activities. Diabetes Care 39 964–972. 10.2337/dc15-2336
    1. Dempsey P. C., Sacre J. W., Larsen R. N., Straznicky N. E., Sethi P., Cohen N. D., et al. (2016b). Interrupting prolonged sitting with brief bouts of light walking or simple resistance activities reduces resting blood pressure and plasma noradrenaline in type 2 diabetes. J. Hypertens. 34 2376–2382. 10.1097/hjh.0000000000001101
    1. Endo K., Matsukawa K., Liang N., Nakatsuka C., Tsuchimochi H., Okamura H., et al. (2013). Dynamic exercise improves cognitive function in association with increased prefrontal oxygenation. J. Physiol. Sci. 63 287–298. 10.1007/s12576-013-0267-6
    1. Falck R. S., Davis J. C., Liu-Ambrose T. (2017). What is the association between sedentary behaviour and cognitive function? A systematic review. Br. J. Sports Med. 51 800–811.
    1. Goldberg M. J., Boutcher S. H., Boutcher Y. N. (2012). The effect of 4 weeks of aerobic exercise on vascular and baroreflex function of young men with a family history of hypertension. J. Hum. Hypertens. 26 644–649. 10.1038/jhh.2011.95
    1. Hansen R. K., Andersen J. B., Vinther A. S., Pielmeier U., Larsen R. G. (2016). Breaking up Prolonged Sitting does not Alter Postprandial Glycemia in Young, Normal-Weight Men and Women. Int. J. Sports Med. 37 1097–1102. 10.1055/s-0042-113466
    1. Heiland E. G., Ekblom O., Tarassova O., Fernstrom M., English C., Ekblom M. M. (2020). ABBaH: activity breaks for brain health. a protocol for a randomized crossover trial. Front. Hum. Neurosci. 14:273.
    1. Herff C., Heger D., Fortmann O., Hennrich J., Putze F., Schultz T. (2014). Mental workload during n-back task—quantified in the prefrontal cortex using fNIRS. Front. Hum. Neurosci. 7:935.
    1. Herold F., Wiegel P., Scholkmann F., Müller N. G. (2018). Applications of functional near-infrared spectroscopy (fNIRS) neuroimaging in exercise–cognition science: a systematic, methodology-focused review. J. Clin. Med. 7:466. 10.3390/jcm7120466
    1. 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. 10.1152/jappl.2001.90.5.1657
    1. Huppert T. J. (2016). Commentary on the statistical properties of noise and its implication on general linear models in functional near-infrared spectroscopy. Neurophotonics 3:010401.
    1. Hyodo K., Dan I., Suwabe K., Kyutoku Y., Yamada Y., Akahori M., et al. (2012). Acute moderate exercise enhances compensatory brain activation in older adults. Neurobiol. Aging 33 2621–2632. 10.1016/j.neurobiolaging.2011.12.022
    1. Ichinose Y., Morishita S., Suzuki R., Endo G., Tsubaki A. (2020). Comparison of the Effects of Continuous and Intermittent Exercise on Cerebral Oxygenation and Cognitive Function. Adv. Exp. Med. Biol. 1232 209–214. 10.1007/978-3-030-34461-0_26
    1. Kujach S., Byun K., Hyodo K., Suwabe K., Fukuie T., Laskowski R., et al. (2018). A transferable high-intensity intermittent exercise improves executive performance in association with dorsolateral prefrontal activation in young adults. NeuroImage 169 117–125. 10.1016/j.neuroimage.2017.12.003
    1. Loh R., Stamatakis E., Folkerts D., Allgrove J. E., Moir H. J. (2020). Effects of interrupting prolonged sitting with physical activity breaks on blood glucose, insulin and triacylglycerol measures: a systematic review and meta-analysis. Sports Med. 50 295–330. 10.1007/s40279-019-01183-w
    1. Maasakkers C. M., Melis R. J. F., Kessels R. P. C., Gardiner P. A., Olde Rikkert M. G. M., Thijssen D. H. J., et al. (2020). The short-term effects of sedentary behaviour on cerebral hemodynamics and cognitive performance in older adults: a cross-over design on the potential impact of mental and/or physical activity. Alzheimers Res. Ther. 12:76.
    1. Maass A., Düzel S., Goerke M., Becke A., Sobieray U., Neumann K., et al. (2015). Vascular hippocampal plasticity after aerobic exercise in older adults. Mol. Psychiatry 20 585–593. 10.1038/mp.2014.114
    1. McMorris T., Sproule J., Turner A., Hale B. J. (2011). Acute, intermediate intensity exercise, and speed and accuracy in working memory tasks: a meta-analytical comparison of effects. Physiol. Behav. 102 421–428. 10.1016/j.physbeh.2010.12.007
    1. Monk T. H. (1989). A visual analogue scale technique to measure global vigor and affect. Psychiatry Res. 27 89–99. 10.1016/0165-1781(89)90013-9
    1. Moriarty T., Bourbeau K., Bellovary B., Zuhl M. N. (2019). Exercise intensity influences prefrontal cortex oxygenation during cognitive testing. Behav. Sci. 9:83. 10.3390/bs9080083
    1. Murata Y., Watanabe T., Terasawa S., Nakajima K., Kobayashi T., Yong Z., et al. (2015). Moderate exercise improves cognitive performance and decreases cortical activation in the go/no-go task. BAOJ Med. Nurs. 1 1–7.
    1. Nelson M. R., Stepanek J., Cevette M., Covalciuc M., Hurst R. T., Tajik A. J. (2010). Noninvasive measurement of central vascular pressures with arterial tonometry: clinical revival of the pulse pressure waveform? Mayo Clin. Proc. 85 460–472. 10.4065/mcp.2009.0336
    1. Neubauer A. C., Fink A. (2009). Intelligence and neural efficiency. Neurosci. Biobehav. Rev. 33 1004–1023. 10.1016/j.neubiorev.2009.04.001
    1. Niedermeier M., Weiss E. M., Steidl-Müller L., Burtscher M., Kopp M. (2020). Acute effects of a short bout of physical activity on cognitive function in sport students. Int. J. Environ. Res. Public Health. 17:3678. 10.3390/ijerph17103678
    1. Nilsson J., Ekblom Ö, Ekblom M., Lebedev A., Tarassova O., Moberg M., et al. (2020). Acute increases in brain-derived neurotrophic factor in plasma following physical exercise relates to subsequent learning in older adults. Sci. Rep. 10:4395.
    1. Olivo G., Nilsson J., Garzón B., Lebedev A., Wåhlin A., Tarassova O., et al. (2021). Immediate effects of a single session of physical exercise on cognition and cerebral blood flow: a randomized controlled study of older adults. Neuroimage 225:117500. 10.1016/j.neuroimage.2020.117500
    1. Perdomo S. J., Gibbs B. B., Kowalsky R. J., Taormina J. M., Balzer J. R. (2019). Effects of alternating standing and sitting compared to prolonged sitting on cerebrovascular hemodynamics. Sport Sci. Health 15 375–383. 10.1007/s11332-019-00526-4
    1. Pinti P., Tachtsidis I., Hamilton A., Hirsch J., Aichelburg C., Gilbert S., et al. (2020). The present and future use of functional near-infrared spectroscopy (fNIRS) for cognitive neuroscience. Ann. N. Y. Acad. Sci. 1464 5–29. 10.1111/nyas.13948
    1. Pontifex M. B., McGowan A. L., Chandler M. C., Gwizdala K. L., Parks A. C., Fenn K., et al. (2019). A primer on investigating the after effects of acute bouts of physical activity on cognition. Psychol. Sport Exerc. 40 1–22. 10.1016/j.psychsport.2018.08.015
    1. Putilov A. A., Donskaya O. G. (2013). Construction and validation of the EEG analogues of the Karolinska sleepiness scale based on the Karolinska drowsiness test. Clin. Neurophysiol. 124 1346–1352. 10.1016/j.clinph.2013.01.018
    1. Sallinen M., Holm A., Hiltunen J., Hirvonen K., Härmä M., Koskelo J., et al. (2008). Recovery of cognitive performance from sleep debt: do a short rest pause and a single recovery night help? Chronobiol. Int. 25 279–296. 10.1080/07420520802107106
    1. Santosa H., Zhai X., Fishburn F., Huppert T. (2018). The NIRS brain AnalyzIR toolbox. Algorithms 11:73. 10.3390/a11050073
    1. Santosa H., Zhai X., Fishburn F., Sparto P., Huppert T. (2020). Quantitative comparison of correction techniques for removing systemic physiological signal in functional near-infrared spectroscopy studies. Neurophotonics 7:035009.
    1. Sato H., Yahata N., Funane T., Takizawa R., Katura T., Atsumori H., et al. (2013). A NIRS–fMRI investigation of prefrontal cortex activity during a working memory task. NeuroImage 83 158–173. 10.1016/j.neuroimage.2013.06.043
    1. Sperlich B., De Clerck I., Zinner C., Holmberg H. C., Wallmann-Sperlich B. (2018). Prolonged sitting interrupted by 6-Min of high-intensity exercise: circulatory, metabolic, hormonal, thermal, cognitive, and perceptual responses. Front. Physiol. 9:1279.
    1. Stute K., Hudl N., Stojan R., Voelcker-Rehage C. (2020). Shedding light on the effects of moderate acute exercise on working memory performance in healthy older adults: an fNIRS study. Brain Sci. 10:813. 10.3390/brainsci10110813
    1. Tanaka H., Dinenno F. A., Monahan K. D., Clevenger C. M., DeSouza C. A., Seals D. R. (2000). Aging, habitual exercise, and dynamic arterial compliance. Circulation 102 1270–1275. 10.1161/01.cir.102.11.1270
    1. Tarumi T., Gonzales M. M., Fallow B., Nualnim N., Pyron M., Tanaka H., et al. (2013). Central artery stiffness, neuropsychological function, and cerebral perfusion in sedentary and endurance-trained middle-aged adults. J. Hypertens. 31 2400–2409. 10.1097/hjh.0b013e328364decc
    1. Tremblay M. S., Aubert S., Barnes J. D., Saunders T. J., Carson V., Latimer-Cheung A. E., et al. (2017). Sedentary behavior research network (SBRN) – terminology consensus project process and outcome. Int. J. Behav. Nutr. Phys. Act. 14:75.
    1. Tsukamoto H., Suga T., Takenaka S., Tanaka D., Takeuchi T., Hamaoka T., et al. (2016). Greater impact of acute high-intensity interval exercise on post-exercise executive function compared to moderate-intensity continuous exercise. Physiol. Behav. 155 224–230. 10.1016/j.physbeh.2015.12.021
    1. Vermeij A., van Beek A. H., Olde Rikkert M. G., Claassen J. A., Kessels R. P. (2012). Effects of aging on cerebral oxygenation during working-memory performance: a functional near-infrared spectroscopy study. PLoS One 7:e46210. 10.1371/journal.pone.0046210
    1. Vincent G. E., Jay S. M., Sargent C., Kovac K., Vandelanotte C., Ridgers N. D., et al. (2018). The impact of breaking up prolonged sitting on glucose metabolism and cognitive function when sleep is restricted. Neurobiol. Sleep Circadian Rhythms 4 17–23. 10.1016/j.nbscr.2017.09.001
    1. Wang C. C., Alderman B., Wu C. H., Chi L., Chen S. R., Chu I. H., et al. (2019). Effects of acute aerobic and resistance exercise on cognitive function and salivary cortisol responses. J. Sport Exerc. Psychol. 41 73–81. 10.1123/jsep.2018-0244
    1. Wennberg P., Boraxbekk C. J., Wheeler M., Howard B., Dempsey P. C., Lambert G., et al. (2016). Acute effects of breaking up prolonged sitting on fatigue and cognition: a pilot study. BMJ Open 6:e009630. 10.1136/bmjopen-2015-009630
    1. Wheeler M. J., Dempsey P. C., Grace M. S., Ellis K. A., Gardiner P. A., Green D. J., et al. (2017). Sedentary behavior as a risk factor for cognitive decline? A focus on the influence of glycemic control in brain health. Alzheimers Dement. 3 291–300. 10.1016/j.trci.2017.04.001
    1. Wheeler M. J., Dunstan D. W., Smith B., Smith K. J., Scheer A., Lewis J., et al. (2019). Morning exercise mitigates the impact of prolonged sitting on cerebral blood flow in older adults. J. Appl. Physiol. 126 1049–1055. 10.1152/japplphysiol.00001.2019
    1. Wheeler M. J., Green D. J., Ellis K. A., Cerin E., Heinonen I., Naylor L. H., et al. (2020). Distinct effects of acute exercise and breaks in sitting on working memory and executive function in older adults: a three-arm, randomised cross-over trial to evaluate the effects of exercise with and without breaks in sitting on cognition. Br. J. Sports Med. 54:776. 10.1136/bjsports-2018-100168
    1. Yanagisawa H., Dan I., Tsuzuki D., Kato M., Okamoto M., Kyutoku Y., et al. (2010). Acute moderate exercise elicits increased dorsolateral prefrontal activation and improves cognitive performance with Stroop test. Neuroimage 50 1702–1710. 10.1016/j.neuroimage.2009.12.023
    1. Yücel M., Lühmann A., Scholkmann F., Gervain J., Dan I., Ayaz H., et al. (2021). Best practices for fNIRS publications. Neurophotonics 8:012101.

Source: PubMed

3
Tilaa