Top

Published in:

Open Access 01-04-2023 | Research Article

Differences in the prefrontal cortex responses of healthy young men performing either water-based or land-based exercise at light to moderate intensity

Authors: Tatsuya Hashitomi, Daisuke Hoshi, Marina Fukuie, Takashi Tarumi, Jun Sugawara, Koichi Watanabe

Published in: Experimental Brain Research | Issue 4/2023

Abstract

Cerebral blood flow increases more during water-based exercise than land-based exercise owing to the effects of end-tidal CO₂ (PETCO₂) and mean arterial pressure (MAP) changes due to water immersion. However, it is unclear whether oxygenated hemoglobin (oxy-Hb) concentrations in the prefrontal cortex (PFC) are increased more by water-based or land-based exercise. We hypothesized that oxy-Hb concentrations in the PFC are higher during water-based exercise than land-based exercise when the exercise intensity is matched. To test this hypothesis, 10 healthy participants (age: 24.2 ± 1.7 years; height: 1.75 ± 0.04 m; weight: 69.5 ± 5.2 kg) performed light- to moderate-intensity cycling exercise in water (water-based cycling (WC); chest-high water at 30 °C) and on land (LC). Stroke volume, cardio output, heart rate, MAP, respiratory rate, PETCO₂, and oxy-Hb in the PFC were assessed during 15 min of exercise, with exercise intensity increased every 5 min. Both WC and LC significantly increased oxy-Hb concentrations in the PFC as exercise intensity was increased (intensity effect: p < 0.001). There was no significant difference in oxy-Hb concentrations during WC and LC in most prefrontal areas, although significant differences were found in areas corresponding to the left dorsolateral PFC (exercise effect: p < 0.001). Thus, WC and LC increase oxy-Hb concentrations in the PFC in a similar manner with increasing exercise intensity, but part of the PFC exhibits enhanced oxy-Hb levels during WC. The neural response of the PFC may differ during water-based and land-based exercise owing to differences in external information associated with water immersion.

Anwar AR, Muthalib M, Perrey S, Galka A, Granert O, Wolff S, Heute U, Deuschl G, Raethjen J, Muthuraman M (2016) Effective connectivity of cortical sensorimotor networks during finger movement tasks: a simultaneous fNIRS, fMRI, EEG study. Brain Topogr 29:645–660. https://doi.org/10.1007/s10548-016-0507-1CrossRefPubMed

Brothers RM, Wingo JE, Hubing KA, Crandall CG (2009) The effects of reduced end-tidal carbon dioxide tension on cerebral blood flow during heat stress. J Physiol 587:3921–3297. https://doi.org/10.1113/jphysiol.2009.172023CrossRefPubMedPubMedCentral

Carter HH, Spence AL, Pugh CJ, Ainslie P, Naylor LH, Green DJ (2014) Cardiovascular responses to water immersion in humans: impact on cerebral perfusion. Am J Physiol Regul Integr Comp Physiol 306:R636–R640. https://doi.org/10.1152/ajpregu.00516.2013CrossRefPubMedPubMedCentral

Christie JL, Sheldahl LM, Tristani FE, Wann LS, Sagar KB, Levandoski SG, Ptacin MJ, Sobocinski KA, Morris RD (1990) Cardiovascular regulation during head-out water immersion exercise. J Appl Physiol 69:657–664. https://doi.org/10.1152/japplCrossRefPubMed

Clark DJ (2015) Automaticity of walking: functional significance, mechanisms, measurement and rehabilitation strategies. Front Hum Neurosci 9:246. https://doi.org/10.3389/fnhum.2015.00246CrossRefPubMedPubMedCentral

Cohen J (1992) A power primer. Psychol Bull 1:155–159. https://doi.org/10.1037//0033-2909.112.1.155CrossRef

Dalecki M, Bock O (2013) Changed joint position sense and muscle activity in simulated weightlessness by water immersion. Aviat Space Environ Med 84:110–115. https://doi.org/10.3357/asem.3394.2013CrossRefPubMed

Ekkekakis P, Parfitt G, Petruzzello SJ (2011) The pleasure and displeasure people feel when they exercise at different intensities: decennial update and progress towards a tripartite rationale for exercise intensity prescription. Sports Med 41:641–671. https://doi.org/10.2165/11590680-000000000-00000CrossRefPubMed

Garzon M, Juneau M, Dupuy O, Nigam A, Bosquet L, Comtois A, Gayda M (2015) Cardiovascular and hemodynamic responses on dryland vs. immersed cycling. J Sci Med Sport 18:619–623. https://doi.org/10.1016/j.jsams.2014.08.005CrossRefPubMed

Girouard H, Iadecola C (2006) Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol 100:328–335. https://doi.org/10.1152/japplphysiol.00966.2005CrossRefPubMed

Guadagni V, Drogos LL, Tyndall AV, Davenport MH, Anderson TJ, Eskes GA, Longman RS, Hill MD, Hogan DB, Poulin MJ (2020) Aerobic exercise improves cognition and cerebrovascular regulation in older adults. Neurology 94:e2245–e2257. https://doi.org/10.1212/WNL.0000000000009478CrossRefPubMedPubMedCentral

Hillman CH, Erickson KI, Kramer AF (2008) Be smart, exercise your heart: exercise effects on brain and cognition. Nat Rev Neurosci 9:58–65. https://doi.org/10.1038/nrn2298CrossRefPubMed

Ide K, Eliasziw M, Poulin MJ (2003) Relationship between middle cerebral artery blood velocity and end-tidal PCO2 in the hypocapnic-hypercapnic range in humans. J Appl Physiol 95:129–137. https://doi.org/10.1152/japplphysiol.01186.2002CrossRefPubMed

Maidan I, Shustak S, Sharon T, Bernad-Elazari H, Geffen N, Giladi N, Hausdorff JM, Mirelman A (2018) Prefrontal cortex activation during obstacle negotiation: what’s the effect size and timing? Brain Cogn 122:45–51. https://doi.org/10.1016/j.bandc.2018.02.006CrossRefPubMed

Mihara M, Miyai I (2016) Review of functional near-infrared spectroscopy in neurorehabilitation. Neurophotonics 3:031414. https://doi.org/10.1117/1.NPh.3.3.031414CrossRefPubMedPubMedCentral

Nybo L, Møller K, Volianitis S, Nielsen B, Secher NH (2002) Effects of hyperthermia on cerebral blood flow and metabolism during prolonged exercise in humans. J Appl Physiol 93:58–64. https://doi.org/10.1152/japplphysiol.00049.2002CrossRefPubMed

Oyanagi K, Tsubaki A (2021) Effects of increased respiratory rate on cortical oxygenated hemoglobin during low-intensity exercise. Respir Physiol Neurobiol 291:103691. https://doi.org/10.1016/j.resp.2021.103691CrossRefPubMed

Park KS, Choi JK, Park YS (1999) Cardiovascular regulation during water immersion. Appl Human Sci 18:233–241. https://doi.org/10.2114/jpa.18.233CrossRefPubMed

Paulson OB, Strandgaard S, Edvinsson L (1990) Cerebral autoregulation. Cerebrovasc Brain Metab Rev Summer 2:161–192

Pendergast DR, Moon RE, Krasney JJ, Held HE, Zamparo P (2015) Human physiology in an aquatic environment. Compr Physiol 20(5):1705–1750. https://doi.org/10.1002/cphy.c140018CrossRef

Pugh CJ, Sprung VS, Ono K, Spence AL, Thijssen DH, Carter HH, Green DJ (2015) The effect of water immersion during exercise on cerebral blood flow. Med Sci Sports Exerc 47:299–306. https://doi.org/10.1249/MSS.0000000000000422CrossRefPubMed

Querido JS, Sheel AW (2007) Regulation of cerebral blood flow during exercise. Sports Med 37:765–782. https://doi.org/10.2165/00007256-200737090-00002CrossRefPubMed

Rooks CR, Thom NJ, McCully KK, Dishman RK (2010) Effects of incremental exercise on cerebral oxygenation measured by near-infrared spectroscopy: a systematic review. Prog Neurobiol 92:134–150. https://doi.org/10.1016/j.pneurobio.2010.06.002CrossRefPubMed

Sackett JR, Schlader ZJ, Sarker S, Chapman CL, Johnson BD (2017) Peripheral chemosensitivity is not blunted during 2 h of thermoneutral head out water immersion in healthy men and women. Physiol Rep 5:e13472. https://doi.org/10.14814/phy2.13472CrossRefPubMedPubMedCentral

Sato D, Onishi H, Yamashiro K, Iwabe T, Shimoyama Y, Maruyama A (2012) Water immersion to the femur level affects cerebral cortical activity in humans: functional near-infrared spectroscopy study. Brain Topogr 25(2):220–227. https://doi.org/10.1007/s10548-011-0204-zCrossRefPubMed

Smith KJ, Ainslie PN (2017) Regulation of cerebral blood flow and metabolism during exercise. Exp Physiol 102:1356–1371. https://doi.org/10.1113/EP086249CrossRefPubMed

Sørensen H, Secher NH, Siebenmann C, Nielsen HB, Kohl-Bareis M, Lundby C, Rasmussen P (2012) Cutaneous vasoconstriction affects near-infrared spectroscopy determined cerebral oxygen saturation during administration of norepinephrine. Anesthesiology 117(2):263–270. https://doi.org/10.1097/ALN.0b013e3182605afeCrossRefPubMed

Takahashi T, Takikawa Y, Kawagoe R, Shibuya S, Iwano T, Kitazawa S (2011) Influence of skin blood flow on near-infrared spectroscopy signals measured on the forehead during a verbal fluency task. NeuroImage 57:991–1002. https://doi.org/10.1016/j.neuroimage.2011.05.012CrossRefPubMed

Tsubaki A, Takai H, Oyanagi K, Kojima S, Tokunaga Y, Miyaguchi S, Sugawara K, Sato D, Tamaki H, Onishi H (2016) Correlation between the cerebral oxyhaemoglobin signal and physiological signals during cycling exercise: a near-infrared spectroscopy study. Adv Exp Med Biol 923:159–166. https://doi.org/10.1007/978-3-319-38810-6_21CrossRefPubMed

Voss MW, Heo S, Prakash RS, Erickson KI, Alves H, Chaddock L, Szabo AN, Mailey EL, Wójcicki TR, White SM, Gothe N, Mcauley E, Sutton BP, Kramer AF (2013) The influence of aerobic fitness on cerebral white matter integrity and cognitive function in older adults: results of a one-year exercise intervention. Hum Brain Mapp 34:2972–2985. https://doi.org/10.1002/hbm.22119CrossRefPubMed

Zenko Z, Ekkekakis P, Ariely D (2016) Can you have your vigorous exercise and enjoy it too? Ramping intensity down increases postexercise, remembered, and forecasted pleasure. J Sport Exerc Psychol 38:149–159. https://doi.org/10.1123/jsep.2015-0286CrossRefPubMed

Title: Differences in the prefrontal cortex responses of healthy young men performing either water-based or land-based exercise at light to moderate intensity
Authors: Tatsuya Hashitomi
Daisuke Hoshi
Marina Fukuie
Takashi Tarumi
Jun Sugawara
Koichi Watanabe
Publication date: 01-04-2023
Publisher: Springer Berlin Heidelberg
Published in: Experimental Brain Research / Issue 4/2023
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-023-06583-z

Advances in Alzheimer's

Alzheimer's Disease
Independent Medical Education

Alzheimer's research and care is changing rapidly. Keep up with the latest developments from key international conferences, together with expert insights on how to integrate these advances into practice.

This content is intended for healthcare professionals outside of the UK.

Supported by:

Lilly

Developed by: Springer Healthcare IME

Learn more

ERS Congress 2024

Springer Medicine

Differences in the prefrontal cortex responses of healthy young men performing either water-based or land-based exercise at light to moderate intensity

Abstract

Advances in Alzheimer's

ERS Congress 2024

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2023

Connexin 43 regulates astrocyte dysfunction and cognitive deficits in early life stress-treated mice

Faces, English words and Chinese characters: a study of dual-task interference in mono-and bilingual speakers

Vestibular perceptual thresholds for rotation about the yaw, roll, and pitch axes

Synchronous motor imagery and visual feedback of finger movement elicit the moving rubber hand illusion, at least in illusion-susceptible individuals

The effect of elastic and viscous force fields on bimanual coordination

Tool use acquisition induces a multifunctional interference effect during object processing: evidence from the sensorimotor mu rhythm

Advances in Alzheimer's