Control of hyperpnoea and pulmonary gas exchange during prolonged exercise: The role of group III/IV muscle afferent feedback.
arterial blood gases
exercise hyperpnoea
reflex
ventilatory control
Journal
The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262
Informations de publication
Date de publication:
24 Sep 2024
24 Sep 2024
Historique:
received:
26
05
2024
accepted:
05
09
2024
medline:
24
9
2024
pubmed:
24
9
2024
entrez:
24
9
2024
Statut:
aheadofprint
Résumé
It remains unclear whether feedback from group III/IV muscle afferents is of continuous significance for regulating the pulmonary response during prolonged (>5 min), steady-state exercise. To elucidate the influence of these sensory neurons on hyperpnoea, gas exchange efficiency, arterial oxygenation and acid-base balance during prolonged locomotor exercise, 13 healthy participants (4 females; 21 (3) years,
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : HHS | NIH | National Heart, Lung, and Blood Institute (NHLBI)
ID : HL-162856
Organisme : HHS | NIH | National Heart, Lung, and Blood Institute (NHLBI)
ID : HL-116579
Organisme : U.S. Veterann Affairs Rehabilitation Research and Development
ID : E3343-R
Informations de copyright
© 2024 The Author(s). The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.
Références
Amann, M., Blain, G. M., Proctor, L. T., Sebranek, J. J., Pegelow, D. F., & Dempsey, J. A. (2010). Group III and IV muscle afferents contribute to ventilatory and cardiovascular response to rhythmic exercise in humans. Journal of Applied Physiology, 109(4), 966–976.
Amann, M., Blain, G. M., Proctor, L. T., Sebranek, J. J., Pegelow, D. F., & Dempsey, J. A. (2011). Implications of group III and IV muscle afferents for high‐intensity endurance exercise performance in humans: Muscle afferents, peripheral fatigue and endurance exercise. The Journal of Physiology, 589(Pt 21), 5299–5309.
Amann, M., Eldridge, M. W., Lovering, A. T., Stickland, M. K., Pegelow, D. F., & Dempsey, J. A. (2006). Arterial oxygenation influences central motor output and exercise performance via effects on peripheral locomotor muscle fatigue in humans. The Journal of Physiology, 575(Pt 3), 937–952.
Amann, M., Proctor, L. T., Sebranek, J. J., Pegelow, D. F., & Dempsey, J. A. (2009). Opioid‐mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. The Journal of Physiology, 587(Pt 3), 271–283.
Amann, M., Runnels, S., Morgan, D. E., Trinity, J. D., Fjeldstad, A. S., Wray, D. W., Reese, V. R., & Richardson, R. S. (2011). On the contribution of group III and IV muscle afferents to the circulatory response to rhythmic exercise in humans. The Journal of Physiology, 589(Pt 15), 3855–3866.
Amann, M., Sidhu, S. K., Weavil, J. C., Mangum, T. S., & Venturelli, M. (2015). Autonomic responses to exercise: Group III/IV muscle afferents and fatigue. Autonomic Neuroscience, 188, 19–23.
Asmussen, E., Johansen, S. H., Jørgensen, M., & Nielsen, M. (1965). On the nervous factors controlling respiration and circulation during exercise experiments with curarization. Acta Physiologica Scandinavica, 63, 343–350.
Azzam, Z. S., Adir, Y., Crespo, A., Comellas, A., Lecuona, E., Dada, L. A., Krivoy, N., Rutschman, D. H., Sznajder, J. I., & Ridge, K. M. (2004). Norepinephrine increases alveolar fluid reabsorption and Na,K‐ATPase activity. American Journal of Respiratory and Critical Care Medicine, 170(7), 730–736.
Barr, P.‐O., Beckman, M., Bjurstedt, H., Brismar, J., Hesser, C. M., & Matell, G. (1964). Time courses of blood gas changes provoked by light and moderate exercise in man. Acta Physiologica Scandinavica, 60, 1–17.
Borg, E., Borg, G., Larsson, K., Letzter, M., & Sundblad, B.‐M. (2010). An index for breathlessness and leg fatigue: An index for breathlessness and leg fatigue. Scandinavian Journal of Medicine & Science in Sports, 20(4), 644–650.
Bradley, A. F., Stupfel, M., & Severinghaus, J. W. (1956). Effect of temperature on Pco2and Po2of blood in vitro. Journal of Applied Physiology, 9(2), 201–204.
Brice, A. G., Forster, H. V., Pan, L. G., Funahashi, A., Hoffman, M. D., Murphy, C. L., & Lowry, T. F. (1988). Is the hyperpnea of muscular contractions critically dependent on spinal afferents? Journal of Applied Physiology, 64(1), 226–233.
Casaburi, R., Barstow, T. J., Robinson, T., & Wasserman, K. (1989). Influence of work rate on ventilatory and gas exchange kinetics. Journal of Applied Physiology, 67(2), 547–555.
Cotes, J. E., Dabbs, J. M., Elwood, P. C., Hall, A. M., McDonald, A., & Saunders, M. J. (1972). Iron‐deficiency anaemia: Its effect on transfer factor for the lung (Diffusing Capacity) and ventilation and cardiac frequency during sub‐maximal exercise. Clinical Science, 42(3), 325–335.
Crystal, R., West, J., Weibel, E., & Barnes, P. (1997). Neural control of pulmonary vascular tone. In The lung: scientific foundations (2nd edn., pp. 1457–1472). Lippincott ‐ Raven, Philadelphia.
Dempsey, J. A., Blain, G. M., & Amann, M. (2014). Are type III–IV muscle afferents required for a normal steady‐state exercise hyperpnoea in humans? The Journal of Physiology, 592(3), 463–474.
Dempsey, J. A., Neder, J. A., Phillips, D. B., & O'Donnell, D. E. (2022). The physiology and pathophysiology of exercise hyperpnea. In Handbook of Clinical Neurology (pp. 201–232). Elsevier. Available at: https://linkinghub.elsevier.com/retrieve/pii/B9780323915342000011 [Accessed April 6, 2024].
Dempsey, J. A., & Wagner, P. D. (1999). Exercise‐induced arterial hypoxemia. Journal of Applied Physiology, 87(6), 1997–2006.
Elliott, J. E., Duke, J. W., Hawn, J. A., Halliwill, J. R., & Lovering, A. T. (2014). Increased cardiac output, not pulmonary artery systolic pressure, increases intrapulmonary shunt in healthy humans breathing room air and 40% O2. The Journal of Physiology, 592(20), 4537–4553.
Forster, H. V., Haouzi, P., & Dempsey, J. A. (2012). Control of breathing during exercise. Comprehensive Physiology, 2(1), 743–777.
Gagnon, P., Bussières, J. S., Ribeiro, F., Gagnon, S. L., Saey, D., Gagné, N., Provencher, S., & Maltais, F. (2012). Influences of spinal anesthesia on exercise tolerance in patients with chronic obstructive pulmonary disease. American Journal of Respiratory and Critical Care Medicine, 186(7), 606–615.
Glenny, R. W. (2008). Teaching ventilation/perfusion relationships in the lung. Advances in Physiology Education, 32(3), 192–195.
González‐Alonso, J., Calbet, J. A. L., Mora‐Rodríguez, R., & Kippelen, P. (2023). Pulmonary ventilation and gas exchange during prolonged exercise in humans: Influence of dehydration, hyperthermia and sympathoadrenal activity. Experimental Physiology, 108(2), 188–206.
Hegewald, M. J., DeCato, T. W., Weaver, L. K., & Jensen, R. L. (2023). Effect of barometric pressure on single‐breath carbon monoxide diffusing capacity. Respiratory Physiology & Neurobiology, 308, 103997.
Hogg, W., Brunton, J., Kryger, M., Brown, R., & MacKlem, P. (1972). Gas diffusion across collateral channels. Journal of Applied Physiology, 33(5), 568–575.
Hopkins, S. R., Gavin, T. P., Siafakas, N. M., Haseler, L. J., Olfert, I. M., Wagner, H., & Wagner, P. D. (1998). Effect of prolonged, heavy exercise on pulmonary gas exchange in athletes. Journal of Applied Physiology, 85(4), 1523–1532.
Hopkins, S. R., Olfert, I. M., & Wagner, P. D. (2009). Point:Counterpoint: Exercise‐induced intrapulmonary shunting is imaginary vs. real. Journal of Applied Physiology, 107(3), 993–994.
Hureau, T. J., Weavil, J. C., Thurston, T. S., Broxterman, R. M., Nelson, A. D., Bledsoe, A. D., Jessop, J. E., Richardson, R. S., Wray, D. W., & Amann, M. (2018). Identifying the role of group III/IV muscle afferents in the carotid baroreflex control of mean arterial pressure and heart rate during exercise. The Journal of Physiology, 596(8), 1373–1384.
Kane, D. W., Tesauro, T., Koizumi, T., Gupta, R., & Newman, J. H. (1994). Exercise‐induced pulmonary vasoconstriction during combined blockade of nitric oxide synthase and beta adrenergic receptors. Journal of Clinical Investigation, 93(2), 677–683.
Kaufman, M. P., Rybicki, K. J., & Mitchell, J. H. (1985). Hindlimb muscular contraction reflexly decreases total pulmonary resistance in dogs. Journal of Applied Physiology, 59(5), 1521–1526.
Kummer, W. (2011). Pulmonary vascular innervation and its role in responses to Hypoxia: Size Matters! Proceedings of the American Thoracic Society, 8(6), 471–476.
Lalley, P. M. (2003). μ‐Opioid receptor agonist effects on medullary respiratory neurons in the cat: Evidence for involvement in certain types of ventilatory disturbances. American Journal of Physiology‐Regulatory, Integrative and Comparative Physiology, 285(6), R1287–R1304.
Lalley, P. M. (2008). Opioidergic and dopaminergic modulation of respiration. Respiratory Physiology & Neurobiology, 164(1–2), 160–167.
Lovering, A. T., Eldridge, M. W., & Stickland, M. K. (2009). Counterpoint: Exercise‐induced intrapulmonary shunting is real. Journal of Applied Physiology, 107(3), 994–997.
MacIntyre, N. (2005). Standardisation of the single‐breath determination of carbon monoxide uptake in the lung. European Respiratory Journal, 26(4), 720–735.
Merton, P. A. (1954). Voluntary strength and fatigue. The Journal of Physiology, 123(3), 553–564.
Mohsenifar, Z., & Tashkin, D. P. (1979). Effect of carboxyhemoglobin on the single breath diffusing capacity: Derivation of an empirical correction factor. Respiration, 37(4), 185–191.
Nicolò, A., & Sacchetti, M. (2023). Differential control of respiratory frequency and tidal volume during exercise. European Journal of Applied Physiology, 123(2), 215–242.
Olson, T. P., Joyner, M. J., Eisenach, J. H., Curry, T. B., & Johnson, B. D. (2014). Influence of locomotor muscle afferent inhibition on the ventilatory response to exercise in heart failure. Experimental Physiology, 99(2), 414–426.
Petersson, J., & Glenny, R. W. (2014). Gas exchange and ventilation–perfusion relationships in the lung. European Respiratory Journal, 44(4), 1023–1041.
Poon, C.‐S., & Song, G. (2015). Type III–IV muscle afferents are not required for steady‐state exercise hyperpnea in healthy subjects and patients with COPD or heart failure. Respiratory Physiology & Neurobiology, 216, 78–85.
Rybicki, K. J., & Kaufman, M. P. (1985). Stimulation of group III and IV muscle afferents eflexly decreases total pulmonary resistance in dogs. Respiration Physiology, 59(2), 185–195.
Sidhu, S. K., Weavil, J. C., Mangum, T. S., Jessop, J. E., Richardson, R. S., Morgan, D. E., & Amann, M. (2017). Group III/IV locomotor muscle afferents alter motor cortical and corticospinal excitability and promote central fatigue during cycling exercise. Clinical Neurophysiology, 128(1), 44–55.
Sidhu, S. K., Weavil, J. C., Venturelli, M., Garten, R. S., Rossman, M. J., Richardson, R. S., Gmelch, B. S., Morgan, D. E., & Amann, M. (2014). Spinal μ‐opioid receptor‐sensitive lower limb muscle afferents determine corticospinal responsiveness and promote central fatigue in upper limb muscle. The Journal of Physiology, 592(Pt 22), 5011–5024.
Smith, C. A., Forster, H. V., Blain, G. M., & Dempsey, J. A. (2010). An interdependent model of central/peripheral chemoreception: Evidence and implications for ventilatory control. Respiratory Physiology & Neurobiology, 173(3), 288–297.
Smith, J. R., Joyner, M. J., Curry, T. B., Borlaug, B. A., Keller‐Ross, M. L., van Iterson, E. H., & Olson, T. P. (2022). Influence of locomotor muscle group III/IV afferents on cardiovascular and ventilatory responses in human heart failure during submaximal exercise. Journal of Applied Physiology, 132(4), 903–914.
Stickland, M. K., Lindinger, M. I., Olfert, I. M., Heigenhauser, G. J. F., & Hopkins, S. R. (2013). Pulmonary gas exchange and acid‐base balance during exercise. Comprehensive Physiology, 3(2), 693–739.
Strange, S., Secher, N. H., Pawelczyk, J. A., Karpakka, J., Christensen, N. J., Mitchell, J. H., & Saltin, B. (1993). Neural control of cardiovascular responses and of ventilation during dynamic exercise in man. The Journal of Physiology, 470, 693–704.
Thurston, T. S., Weavil, J. C., Georgescu, V. P., Wan, H., Birgenheier, N. M., Morrissey, C. K., Jessop, J. E., & Amann, M. (2023). The exercise pressor reflex – a pressure‐raising mechanism with a limited role in regulating leg perfusion during locomotion in young healthy men. The Journal of Physiology, 601(20), 4557–4572.
Thurston, T. S., Weavil, J. C., Hureau, T. J., Gifford, J. R., Georgescu, V. P., Wan, H.‐Y., La Salle, D. T., Richardson, R. S., & Amann, M. (2021). On the implication of dietary nitrate supplementation for the hemodynamic and fatigue response to cycling exercise. Journal of Applied Physiology, 131(6), 1691–1700.
Turino, G. M., Bergofsky, E. H., Goldring, R. M., & Fishman, A. P. (1963). Effect of exercise on pulmonary diffusing capacity. Journal of Applied Physiology, 18(3), 447–456.
Vogiatzis, I., Zakynthinos, S., Boushel, R., Athanasopoulos, D., Guenette, J. A., Wagner, H., Roussos, C., & Wagner, P. D. (2008). The contribution of intrapulmonary shunts to the alveolar‐to‐arterial oxygen difference during exercise is very small. The Journal of Physiology, 586(9), 2381–2391.
Wagner, P. D. (1992). Ventilation‐perfusion matching during exercise. Chest, 101(5), 192S–198S.
Waldrop, T. G., & Iwamoto, G. A. (2006). Point:Counterpoint: Supraspinal locomotor centers do/do not contribute significantly to the hyperpnea of dynamic exercise. Journal of Applied Physiology, 100(3), 1077–1083.
Wan, H., Weavil, J. C., Thurston, T. S., Georgescu, V. P., Hureau, T. J., Bledsoe, A. D., Buys, M. J., Jessop, J. E., Richardson, R. S., & Amann, M. (2020a). The exercise pressor reflex and chemoreflex interaction: Cardiovascular implications for the exercising human. The Journal of Physiology, 598(12), 2311–2321.
Wan, H.‐Y., Weavil, J. C., Thurston, T. S., Georgescu, V. P., Bledsoe, A. D., Jessop, J. E., Buys, M. J., Richardson, R. S., & Amann, M. (2020b). The muscle reflex and chemoreflex interaction: Ventilatory implications for the exercising human. Journal of Applied Physiology, 129(4), 691–700.
Wasserman, K., Hansen, J. E., Sue, D. Y., Whipp, B. J., & Froelicher, V. F. (1987). Principles of exercise testing and interpretation. Journal of Cardiopulmonary Rehabilitation and Prevention, 7(4), 189.
Wasserman, K., van Kessel, A. L., & Burton, G. G. (1966). Interaction mechanisms of physiological during exercise. Journal of Applied Physiology, 22(1), 71–85.
Weissman, M. L., Whipp, B. J., Huntsman, D. J., & Wasserman, K. (1980). Role of neural afferents from working limbs in exercise hyperpnea. Journal of Applied Physiology, 49(2), 239–248.
Whipp, B. J., Ward, S. A., Lamarra, N., Davis, J. A., & Wasserman, K. (1982). Parameters of ventilatory and gas exchange dynamics during exercise. Journal of Applied Physiology, 52(6), 1506–1513.