An increase in prefrontal oxygenation at the start of voluntary cycling exercise was observed independently of exercise effort and muscle mass
- 102 Downloads
We have reported using near-infrared spectroscopy that an increase in prefrontal oxygenated-hemoglobin concentration (Oxy-Hb) at the start of cycling exercise has relation to central command, defined as a feedforward signal descending from higher brain centers. The final output of central command evokes the exercise effort-dependent cardiovascular responses. If the prefrontal cortex may output the final signal of central command toward the autonomic nervous system, the prefrontal oxygenation should increase depending on exercise effort. To test the hypothesis, we investigated the effects of exercise intensity and muscle mass on prefrontal oxygenation in 13 subjects.
The subjects performed one- or two-legged cycling at various relative intensities for 1 min. The prefrontal Oxy-Hb and cardiovascular variables were simultaneously measured during exercise.
The increase in cardiac output and the decrease in total peripheral resistance at the start of one- and two-legged cycling were augmented in proportion to exercise intensity and muscle mass recruitment. The prefrontal Oxy-Hb increased at the start of voluntary cycling, while such increase was not developed during passive cycling. Mental imagery of cycling also increased the prefrontal Oxy-Hb, concomitantly with peripheral muscle vasodilatation. However, the increase in prefrontal Oxy-Hb at the start of voluntary cycling seemed independent of exercise intensity and muscle mass recruitment.
It is likely that the increased prefrontal activity at the start of cycling exercise is not representative of the final output signal of central command itself toward the autonomic nervous system but may trigger neuronal activity in the caudal brain responsible for the generation of central command.
KeywordsCentral command Regional cerebral blood flow Exercise effort Near-infrared spectroscopy
Analysis of variance
Autonomic nervous system
Arterial blood pressure
Mean arterial blood pressure
Maximal voluntary exercise intensity
The midbrain periaqueductal gray area
Regional cerebral blood flow
The rating of perceived exertion
Total peripheral resistance
The midbrain ventral tegmental area
This study was funded by Grant-in-Aid (15H03061) for Scientific Research (B) from the Japan Society for the Promotion of Science (JSPS). R. A. was a Research Fellow supported by JSPS.
RA and KM: conception and design of research; RA, KE, NL, and KM performed experiments; RA analyzed data; RA and KM interpreted results of experiments; RA prepared figures; RA and KM drafted manuscript; RA, KE, NL, and KM edited and revised manuscript; RA, KE, NL, and KM approved the final version of manuscript and had responsibility for all aspects of the work.
Compliance with ethical standards
Conflict of interest
All authors declare that they have no conflict of interest with regard to this study.
All procedures and protocols performed in this study were in accordance with the ethical standards by the Physiological Society of Japan and with the 1964 Helsinki declaration and its later amendments and were approved by the Institutional Ethical Committee of Hiroshima University (permit no. E-532). Informed written consent was obtained from all participants included in this study.
- Basnayake SD, Hyam JA, Pereira EA, Schweder PM, Brittain JS, Aziz TZ, Green AL, Paterson DJ (2011) Identifying cardiovascular neurocircuitry involved in the exercise pressor reflex in humans using functional neurosurgery. J Appl Physiol 110:881–891. https://doi.org/10.1152/japplphysiol.00639.2010 CrossRefPubMedGoogle Scholar
- Fadel PJ, Keller DM, Watanabe H, Raven PB, Thomas GD (2004) Noninvasive assessment of sympathetic vasoconstriction in human and rodent skeletal muscle using near-infrared spectroscopy and Doppler ultrasound. J Appl Physiol 96:1323–1330. https://doi.org/10.1152/japplphysiol.01041.2003 CrossRefPubMedGoogle Scholar
- Furubayashi T, Mochizuki H, Terao Y, Arai N, Hanajima R, Hamada M, Matsumoto H, Nakatani-Enomoto S, Okabe S, Yugeta A, Inomata-Terada S, Ugawa Y (2013) Cortical hemoglobin concentration changes underneath the coil after single-pulse transcranial magnetic stimulation: a near-infrared spectroscopy study. J Nerurophysiol 109:1626–1637. https://doi.org/10.1152/jn.00980.2011 CrossRefGoogle Scholar
- Hirasawa A, Yanagisawa S, Tanaka N, Funane T, Kiguchi M, Sørensen H, Secher NH, Ogoh S (2015) Influence of skin blood flow and source-detector distance on near-infrared spectroscopy-determined cerebral oxygenation in humans. Clin Physiol Funct Imaging 35:237–244. https://doi.org/10.1111/cpf.12156 CrossRefPubMedGoogle Scholar
- Ishii K, Liang N, Oue A, Hirasawa A, Sato K, Sadamoto T, Matsukawa K (2012) Central command contributes to increased blood flow in the noncontracting muscle at the start of one-legged dynamic exercise in humans. J Appl Physiol 112:1961–1974. https://doi.org/10.1152/japplphysiol.00075.2012 CrossRefPubMedGoogle Scholar
- Ishii K, Matsukawa K, Liang N, Endo K, Idesako M, Hamada H, Ueno K, Kataoka T (2013) Evidence for centrally-induced cholinergic vasodilation in skeletal muscle during voluntary one-legged cycling and motor imagery in humans. Physiol Rep 1:e00092. https://doi.org/10.1002/phy2.92 CrossRefPubMedPubMedCentralGoogle Scholar
- Ishii K, Matsukawa K, Liang N, Endo K, Idesako M, Hamada H, Kataoka T, Ueno K, Watanabe T (2014) Differential contribution of Ach-muscarinic and β-adrenergic receptors to vasodilatation in noncontracting muscle during voluntary one-legged exercise. Physiol Rep 2:e12202. https://doi.org/10.14814/phy2.12202 CrossRefPubMedPubMedCentralGoogle Scholar
- Ishii K, Matsukawa K, Liang N, Endo K, Idesako M, Asahara R, Kadowaki A, Wakasugi R, Takahashi M (2016) Central command generated prior to arbitrary motor execution induces muscle vasodilatation at the beginning of dynamic exercise. J Appl Physiol 120:1424–1433. https://doi.org/10.1152/japplphysiol.00103.2016 CrossRefPubMedGoogle Scholar
- Matsukawa K, Murata J, Wada T (1998) Augmented renal sympathetic nerve activity by central command during overground locomotion in decerebrate cats. Am J Physiol 275:H1115–H1121Google Scholar
- Matsukawa K, Ishii K, Liang N, Endo K, Ohtani R, Nakamoto T, Wakasugi R, Kadowaki A, Komine H (2015) Increased oxygenation of the cerebral prefrontal cortex prior to the onset of voluntary exercise in humans. J Appl Physiol 119:452–462. https://doi.org/10.1152/japplphysiol.00406.2015 CrossRefPubMedGoogle Scholar
- Matsukawa K, Ishii K, Asahara R, Idesako M (2016) Central command does not suppress baroreflex control of cardiac sympathetic nerve activity at the onset of spontaneous motor activity in the decerebrate cat. J Appl Physiol 121:932–943. https://doi.org/10.1152/japplphysiol.00299.2016 CrossRefPubMedGoogle Scholar
- Nakamoto T, Matsukawa K, Liang N, Wakasugi R, Wilson LB, Horiuchi J (2011) Coactivation of renal sympathetic neurons and somatic motor neurons by chemical stimulation of the midbrain ventral tegmental area. J Appl Physiol 110:1342–1353. https://doi.org/10.1152/japplphysiol.01233.2010 CrossRefPubMedGoogle Scholar
- O’Leary DS, Robinson ED, Butler JL (1997) Is active skeletal muscle functionally vasoconstricted during dynamic exercise in conscious dogs? Am J Physiol 272:R386-R391Google Scholar
- van der Zee P, Cope M, Arridge SR, Essenpreis M, Potter LA, Edwards AD, Wyatt JS, McCormick DC, Roth SC, Reynolds EO, Delpy DT (1992) Experimentally measured optical path lengths for the adult head, calf and forearm and the head of the newborn infant as a function of inter optode spacing. Adv Exp Med Biol 316:143–153CrossRefPubMedGoogle Scholar