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Runners maintain locomotor–respiratory coupling following isocapnic voluntary hyperpnea to task failure

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Abstract

Introduction

Evidence has long suggested that mammalian ventilatory and locomotor rhythms are linked, yet determinants and implications of locomotor–respiratory coupling (LRC) continue to be investigated. Anecdotally, respiratory muscle fatigue seen at the end of heavy exercise may result in an uncoupling of movement–ventilation rhythms; however, there is no scientific evidence to substantiate this claim.

Purpose

We sought to determine whether or not fatigue of the respiratory muscles alters locomotor–respiratory coupling patterns typically observed in highly trained individuals while running. A related query was to examine the relationship between the potential changes in LRC and measures of running economy.

Method

Twelve male distance runners ran at four submaximal workloads (68–89 % \({\dot{V}}\)O2peak) on two separate days while LRC was quantified. One LRC trial served as a control (CON), while the other was performed following an isocapnic voluntary hyperpnea to task failure to induce respiratory muscle fatigue (FT+). LRC was assessed as stride-to-breathing frequency ratios (SF/fB) and degree of LRC (percentage of breaths occurring during the same decile of the step cycle).

Result

Hyperpnea resulted in significant declines in maximal voluntary inspiratory (MIP) and expiratory (MEP) mouth pressures (ΔMIP = −10 ± 12 cm H2O; ΔMEP = −6 ± 9 cm H2O). There were no differences in minute ventilation between CON and FT+ (CON, all speeds pooled = 104 ± 25 L min−1; FT+ pooled = 106 ± 23 L min−1). Stride frequency was not different between trials; however, breathing frequency was significantly greater during FT+ compared to CON at all speeds (CON pooled = 47 ± 10 br min−1; FT+ pooled = 52 ± 9 br min−1), resulting in smaller corresponding SF/fB. Yet, the degree of LRC was the same during CON and FT+ (CON pooled = 63 ± 15 %; FT+ pooled = 64 ± 18 %).

Conclusion

The results indicate that trained runners are able to continue entraining breath and step cycles, despite marked changes in exercise breathing frequency, after a fatiguing hyperpnea challenge.

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Abbreviations

BTPS:

Body temperature and pressure, saturated

DYS:

Rating of perceived dyspnea

fB :

Breathing frequency

FECO2 :

Fraction of expired carbon dioxide

FEO2 :

Fraction of expired oxygen

FEV1 :

Forced expiratory volume in one second

FVC:

Forced vital capacity

IVH:

Isocapnic voluntary hyperpnea

LRC:

Locomotor–respiratory coupling

MEP:

Maximal volitional expiratory mouth pressure

MIP:

Maximal volitional inspiratory mouth pressure

MVV:

Maximal voluntary ventilation

RE:

Running economy

RMF:

Respiratory muscle fatigue

RPE:

Rating of perceived exertion

RPM:

Revolutions per minute

SF:

Step frequency

STPD:

Standard temperature and pressure, dry

\({\dot{V}}\)CO2 :

Volume of expired carbon dioxide

\({\dot{V}}\)E:

Minute ventilation

\({\dot{V}}\)O2peak :

Maximal rate of oxygen consumption

V T :

Tidal volume

References

  • Aaron EA, Seow KC, Johnson BD, Dempsey JA (1992) Oxygen cost of exercise hyperpnea: implications for performance. J Appl Physiol 72:1818–1825

    CAS  PubMed  Google Scholar 

  • American Thoracic Society/European Respiratory S (2002) ATS/ERS Statement on respiratory muscle testing. Am J Respir Crit Care Med 166:518–624. doi:10.1164/rccm.166.4.518

    Article  Google Scholar 

  • Babcock MA, Pegelow DF, McClaran SR, Suman OE, Dempsey JA (1995) Contribution of diaphragmatic power output to exercise-induced diaphragm fatigue. J Appl Physiol 78:1710–1719

    CAS  PubMed  Google Scholar 

  • Bai TR, Rabinovitch BJ, Pardy RL (1984) Near-maximal voluntary hyperpnea and ventilatory muscle function. J Appl Physiol 57:1742–1748

    CAS  PubMed  Google Scholar 

  • Banzett RB, Mead J, Reid MB, Topulos GP (1992) Locomotion in men has no appreciable mechanical effect on breathing. J Appl Physiol 72:1922–1926

    CAS  PubMed  Google Scholar 

  • Bartlett D Jr, Leiter JC (2012) Coordination of breathing with nonrespiratory activities Comprehensive. Physiology 2:1387–1415. doi:10.1002/cphy.c110004

    Google Scholar 

  • Bechbache RR, Duffin J (1977) The entrainment of breathing frequency by exercise rhythm. J Physiol 272:553–561

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bernasconi P, Kohl J (1993) Analysis of co-ordination between breathing and exercise rhythms in man. J Physiol 471:693–706

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Berry MJ, Dunn CJ, Pittman CL, Kerr WC, Adair NE (1996) Increased ventilation in runners during running as compared to walking at similar metabolic rates. Eur J Appl Physiol 73:245–250

    Article  CAS  Google Scholar 

  • Boggs DF (2002) Interactions between locomotion and ventilation in tetrapods. Comparative biochemistry and physiology Part A. Mol Integr Physiol 133:269–288

    Article  Google Scholar 

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

    Google Scholar 

  • Bramble DM, Carrier DR (1983) Running and breathing in mammals. Science 219:251–256

    Article  CAS  PubMed  Google Scholar 

  • Cavanagh PR, Kram R (1989) Stride length in distance running: velocity, body dimensions, and added mass effects. Med Sci Sports Exerc 21:467–479

    Article  CAS  PubMed  Google Scholar 

  • Cavanagh PR, Williams KR (1982) The effect of stride length variation on oxygen uptake during distance running. Med Sci Sports Exerc 14:30–35

    Article  CAS  PubMed  Google Scholar 

  • Coast JR, Haverkamp HC, Finkbone CM, Anderson KL, George SO, Herb RA (1999) Alterations in pulmonary function following exercise are not caused by the work of breathing alone. Int J Sports Med 20:470–475. doi:10.1055/s-1999-8828

    Article  CAS  PubMed  Google Scholar 

  • Cordain L, Rode EJ, Gotshall RW, Tucker A (1994) Residual lung volume and ventilatory muscle strength changes following maximal and submaximal exercise. Int J Sports Med 15:158–161. doi:10.1055/s-2007-1021039

    Article  CAS  PubMed  Google Scholar 

  • Daffertshofer A, Huys R, Beek PJ (2004) Dynamical coupling between locomotion and respiration. Biol Cybern 90:157–164. doi:10.1007/s00422-004-0462-x

    Article  PubMed  Google Scholar 

  • Daley MA, Bramble DM, Carrier DR (2013) Impact loading and locomotor-respiratory coordination significantly influence breathing dynamics in running humans. PloS One 8:e70752. doi:10.1371/journal.pone.0070752

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Daniels J, Daniels N (1992) Running economy of elite male and elite female runners. Med Sci Sports Exerc 24:483–489

    Article  CAS  PubMed  Google Scholar 

  • Fabre N, Perrey S, Passelergue P, Rouillon JD (2007) No influence of hypoxia on coordination between respiratory and locomotor rhythms during rowing at moderate intensity. J Sports Sci Med 6:526–531

    PubMed Central  PubMed  Google Scholar 

  • Foster C, Lucia A (2007) Running economy : the forgotten factor in elite performance. Sports Med 37:316–319

    Article  PubMed  Google Scholar 

  • Garlando F, Kohl J, Koller EA, Pietsch P (1985) Effect of coupling the breathing- and cycling rhythms on oxygen uptake during bicycle ergometry. Eur J Appl Physiol 54:497–501

    Article  CAS  Google Scholar 

  • Hamnegard CH et al (1996) Diaphragm fatigue following maximal ventilation in man. Eur Respir J 9:241–247

    Article  CAS  PubMed  Google Scholar 

  • Hankinson JL, Odencrantz JR, Fedan KB (1999) Spirometric reference values from a sample of the general US population. Am J Respir Crit Care Med 159:179–187. doi:10.1164/ajrccm.159.1.9712108

    Article  CAS  PubMed  Google Scholar 

  • Hodges PW, Heijnen I, Gandevia SC (2001) Postural activity of the diaphragm is reduced in humans when respiratory demand increases. J Physiol 537:999–1008

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hoffmann CP, Torregrosa G, Bardy BG (2012) Sound stabilizes locomotor-respiratory coupling and reduces energy cost. Plos One 7:e45206. doi:10.1371/journal.pone.0045206

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hunter I, Smith GA (2007) Preferred and optimal stride frequency, stiffness and economy: changes with fatigue during a 1-h high-intensity run. Eur J Appl Physiol 100:653–661. doi:10.1007/s00421-007-0456-1

    Article  PubMed  Google Scholar 

  • Johnson BD, Babcock MA, Suman OE, Dempsey JA (1993) Exercise-induced diaphragmatic fatigue in healthy humans. J Physiol 460:385–405

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lafortuna CL, Reinach E, Saibene F (1996) The effects of locomotor-respiratory coupling on the pattern of breathing in horses. J Physiol 492(Pt 2):587–596

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lomax M, Castle S (2011) Inspiratory muscle fatigue significantly affects breathing frequency, stroke rate, and stroke length during 200-m front-crawl swimming. J Strength Condition Res Natl Strength Condition Assoc 25:2691–2695. doi:10.1519/JSC.0b013e318207ead8

  • Lomax ME, McConnell AK (2003) Inspiratory muscle fatigue in swimmers after a single 200 m swim. J Sports Sci 21:659–664. doi:10.1080/0264041031000101999

    Article  PubMed  Google Scholar 

  • Mador MJ, Acevedo FA (1991a) Effect of respiratory muscle fatigue on breathing pattern during incremental exercise. Am Rev Respir Dis 143:462–468. doi:10.1164/ajrccm/143.3.462

    Article  CAS  PubMed  Google Scholar 

  • Mador MJ, Acevedo FA (1991b) Effect of respiratory muscle fatigue on subsequent exercise performance. J Appl Physiol 70:2059–2065

    CAS  PubMed  Google Scholar 

  • Mador JM, Rodis A, Diaz J (1996) Diaphragmatic fatigue following voluntary hyperpnea. Am J Respir Crit Care Med 154:63–67. doi:10.1164/ajrccm.154.1.8680701

    Article  CAS  PubMed  Google Scholar 

  • Martin B, Heintzelman M, Chen HI (1982) Exercise performance after ventilatory work. J Appl Physiol Respir Environ Exerc Physiol 52:1581–1585

  • McConnell AK, Romer LM (2004) Respiratory muscle training in healthy humans: resolving the controversy. Int J Sports Med 25:284–293. doi:10.1055/s-2004-815827

    Article  CAS  PubMed  Google Scholar 

  • McDermott WJ, Van Emmerik RE, Hamill J (2003) Running training and adaptive strategies of locomotor-respiratory coordination. Eur J Appl Physiol 89:435–444. doi:10.1007/s00421-003-0831-5

    Article  PubMed  Google Scholar 

  • Miller MR et al (2005) Standardisation of spirometry. Eur Respir J 26:319–338. doi:10.1183/09031936.05.00034805

    Article  CAS  PubMed  Google Scholar 

  • Morgan DW, Martin PE (1986) Effects of stride length alteration on racewalking economy. Can J Appl Sport Sci 11:211–217

    CAS  PubMed  Google Scholar 

  • O’Halloran J, Hamill J, McDermott WJ, Remelius JG, Van Emmerik RE (2012) Locomotor-respiratory coupling patterns and oxygen consumption during walking above and below preferred stride frequency. Eur J Appl Physiol 112:929–940. doi:10.1007/s00421-011-2040-y

    Article  PubMed  Google Scholar 

  • Paterson DJ (2014) Defining the neurocircuitry of exercise hyperpnoea. J Physiol 592:433–444. doi:10.1113/jphysiol.2013.261586

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paterson DJ, Wood GA, Morton AR, Henstridge JD (1986) The entrainment of ventilation frequency to exercise rhythm. Eur J Appl Physiol 55:530–537

    Article  CAS  Google Scholar 

  • Paterson DJ, Wood GA, Marshall RN, Morton AR, Harrison AB (1987) Entrainment of respiratory frequency to exercise rhythm during hypoxia. J Appl Physiol 62:1767–1771

    CAS  PubMed  Google Scholar 

  • Persegol L, Jordan M, Viala D (1991) Evidence for the entrainment of breathing by locomotor pattern in human. J Physiol 85:38–43

    CAS  Google Scholar 

  • Rassler B, Kohl J (1996) Analysis of coordination between breathing and walking rhythms in humans. Respir Physiol 106:317–327

    Article  CAS  PubMed  Google Scholar 

  • Renggli AS, Verges S, Notter DA, Spengler CM (2008) Development of respiratory muscle contractile fatigue in the course of hyperpnoea. Respir Physiol Neurobiol 164:366–372. doi:10.1016/j.resp.2008.08.008

    Article  PubMed  Google Scholar 

  • Romer LM, McConnell AK, Jones DA (2002) Inspiratory muscle fatigue in trained cyclists: effects of inspiratory muscle training. Med Sci Sports Exerc 34:785–792

    Article  PubMed  Google Scholar 

  • Saunders PU, Pyne DB, Telford RD, Hawley JA (2004) Reliability and variability of running economy in elite distance runners. Med Sci Sports Exerc 36:1972–1976

    Article  PubMed  Google Scholar 

  • Sheel AW, Romer LM (2012) Ventilation and respiratory mechanics. Compr Physiol 2:1093–1142. doi:10.1002/cphy.c100046

    PubMed  Google Scholar 

  • Sliwinski P, Yan S, Gauthier AP, Macklem PT (1996) Influence of global inspiratory muscle fatigue on breathing during exercise. J Appl Physiol 80:1270–1278

    CAS  PubMed  Google Scholar 

  • Spengler CM, Knopfli-Lenzin C, Birchler K, Trapletti A, Boutellier U (2000) Breathing pattern and exercise endurance time after exhausting cycling or breathing. Eur J Appl Physiol 81:368–374. doi:10.1007/s004210050056

    Article  CAS  PubMed  Google Scholar 

  • Takano N (1995) Phase relation and breathing pattern during locomotor/respiratory coupling in uphill and downhill running. Jpn J Physiol 45:47–58

    Article  CAS  PubMed  Google Scholar 

  • Takano N, Deguchi H (1997) Sensation of breathlessness and respiratory oxygen cost during cycle exercise with and without conscious entrainment of the breathing rhythm. Eur J Appl Physiol 76:209–213. doi:10.1007/s004210050238

    Article  CAS  Google Scholar 

  • Taylor BJ, Romer LM (2008) Effect of expiratory muscle fatigue on exercise tolerance and locomotor muscle fatigue in healthy humans. J Appl Physiol 104:1442–1451. doi:10.1152/japplphysiol.00428.2007

    Article  PubMed  Google Scholar 

  • van Alphen J, Duffin J (1994) Entrained breathing and oxygen consumption during treadmill walking. Can J Appl Physiol 19:432–440

  • Verges S, Notter D, Spengler CM (2006) Influence of diaphragm and rib cage muscle fatigue on breathing during endurance exercise. Respir Physiol Neurobiol 154:431–442. doi:10.1016/j.resp.2005.12.007

    Article  PubMed  Google Scholar 

  • Verges S, Sager Y, Erni C, Spengler CM (2007) Expiratory muscle fatigue impairs exercise performance. Eur J Appl Physiol 101:225–232. doi:10.1007/s00421-007-0491-y

    Article  CAS  PubMed  Google Scholar 

  • Villard S, Casties JF, Mottet D (2005) Dynamic stability of locomotor respiratory coupling during cycling in humans. Neurosci Lett 383:333–338. doi:10.1016/j.neulet.2005.04.047

    Article  CAS  PubMed  Google Scholar 

  • Volianitis S, McConnell AK, Koutedakis Y, McNaughton L, Backx K, Jones DA (2001) Inspiratory muscle training improves rowing performance. Med Sci Sports Exerc 33:803–809

    Article  CAS  PubMed  Google Scholar 

  • Yonge RP, Petersen ES (1983) Entrainment of breathing in rhythmic exercise. In: Whipp BJ, Wiber DM (eds) Modelling and control of breathing. Elsevier, New York, pp 197–203

    Google Scholar 

  • Young IS, Alexander R, Woakes AJ, Butler PJ, Anderson L (1992) The synchronization of ventilation and locomotion in horses (Equus caballus). J Exp Biol 166:19–31

    CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank Drs. Bruce Martin and David Koceja for their invaluable feedback on the project. This research was supported in part by an Indiana University School of Public Health Student Research Grant and a University Graduate School Grant-in-Aid of Doctoral Research.

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Correspondence to Abigail S. L. Stickford.

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Communicated by David C. Poole.

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Stickford, A.S.L., Stickford, J.L., Tanner, D.A. et al. Runners maintain locomotor–respiratory coupling following isocapnic voluntary hyperpnea to task failure. Eur J Appl Physiol 115, 2395–2405 (2015). https://doi.org/10.1007/s00421-015-3220-y

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