Locomotion-respiration coupling: an account of the underlying dynamics

LETTERS TO THE EDITORLocomotion-respiration coupling: an account of the underlying dynamicsRaoul Huys, Andreas Daffertshofer, Peter Beek, David Sanderson, and Gunter SiegmundRaoul Huys, Andreas Daffertshofer, Peter Beek, David Sanderson, and Gunter SiegmundPublished Online:01 Jun 2004https://doi.org/10.1152/japplphysiol.01341.2003MoreSectionsPDF (16 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations To the Editor: Entrainment between cyclic movement and respiration has been observed in a wide variety of locomotor activities, including walking and running, manual wheelchair propulsion, and rowing. To date, however, few generic mechanisms for the occurrence of locomotion-respiration coupling (LRC) have been identified. In search of such causal principles, we reanalyzed recently published data showing LRC in rowing (4). In addition to the frequency doubling in respiration reported by Siegmund et al. (4), detailed time-resolved (cross-)spectral analyses revealed decreases in the stability of entrainment in the vicinity of bifurcations (abrupt changes in frequency relations) as well as switches in the relative phase between the rowing strokes and respiration.What is causing these patterns of synchronization, the loss of their stability, and subsequent switches to other entrainment forms? We submit that a single physiological although mechanically constrained quantity may be sufficient to explain preferences of frequency and phase locking between locomotion and respiration: energy or, more specifically, the effective value of oxygen concentration in the lungs. Oscillations in abdominal pressure (3) modulate the self-sustaining rhythmic respiration (2), superimposing on the total lung pressure, and cause (local) maxima at integer frequency ratios between movement (rowing strokes) and respiration. Hence, optimization of the effective oxygen concentration can be seen as a driving mechanism that forces respiration to synchronize with rhythmic movement. Because the rowing movements are constrained in a cadence, the optimization is realized by varying the respiration frequency and/or phase. One can model this adaptation dynamically as a stable limit cycle oscillator (“free” respiration) coupled to a periodic force (movement). The explicit coupling is given via the maximization of the effective oxygen level in the lungs. Indeed, such a model can exhibit the empirically observed synchronization patterns. In addition, it provides hints at certain distinct mechanisms that may induce switches between different modes of entrainment (1). In particular, amplitude and phase relations between respiration and movement affect the stability of specific frequency locking ratios and may therefore be seen as the corresponding bifurcation parameters. When searching for a maximal energy transfer, these parameters have to be adjusted properly. If the adjustment is limited and, consequently, the proper frequency relation can no longer be maintained, then the intrinsic structure of lung pressure modulation readily implies a spontaneous switch to another (sub)optimal rational frequency locking state because integer ratios always reflect (local) maxima of effective oxygen concentration. References 1 Daffertshofer A, Huys R, and Beek PJ. Dynamical coupling between locomotion and respiration. Biol Cybern 90: 157-164, 2004.Crossref | ISI | Google Scholar2 Del Negro CA, Morgado-Valle C, and Feldman JL. Respiratory rhythm: an emergent network property? Neuron 34: 821-830, 2002.Crossref | PubMed | ISI | Google Scholar3 Manning TS, Plowman A, Drake G, Looney MA, and Ball TE. Intraabdominal pressure and rowing: the effects of inspiring versus expiring during the drive. J Sports Med Phys Fitness 40: 223-232, 2000.ISI | Google Scholar4 Siegmund GP, Edwards MR, Moore KS, Tiessen DA, Sanderson DJ, and McKenzie DC. Ventilation and locomotion coupling in varsity male rowers. J Appl Physiol 87: 233-242, 1992.Google ScholarjapJ Appl PhysiolJournal of Applied PhysiologyJ Appl Physiol8750-75871522-1601American Physiological SocietyREPLYDonald C. McKenzieDivision of Sports Medicine University of British Columbia Vancouver, British Columbia, Canada V6T 1Z362004To the Editor: In their letter, Huys et al. have reanalyzed data from our study (6) in an attempt to elucidate a “causal principle” for LRC. They suggest that “optimization of the effective oxygen concentration can be seen as the driving mechanism that forces respiration to synchronize with rhythmic movement.” The original study showed that all rowers demonstrated LRC for some portion of the rowing test; the pattern of LRC was variable between subjects (different integral patterns; 1:1, 2:1, and 3:1) and was altered at different points during the performance task. The rowers appeared to alter their ventilation to match locomotion. The data from this descriptive paper did not permit more than speculation on the underlying causes of LRC.The model proposed by Huys et al. fails to consider many alternate possibilities, and the notion that optimization of the oxygen concentration in the lung drives LRC appears overly simplistic given the complexity of the relationship between exercise and ventilation. The mechanisms that mediate the ventilatory responses to exercise have been studied for more than a century and remain controversial. Forster (3) suggested this was because investigators have not yet devised an ideal preparation for its study. Most investigators have agreed on a three-component model to explain the regulation of exercise ventilation: a central medullary rhythm generator/integrator, neural inputs into this integrator from higher locomotor areas of the central nervous system and from the periphery, and the regulation of the distribution of efferent motor output to the muscles of respiration.Although LRC has been documented in humans engaged in a variety of exercise modalities and in many exercising mammals, little is known about the neural or biomechanical basis for it (1). Evidence for a locomotor-linked neural stimuli to hyperpnea has emerged from animal models with simulated locomotion (2, 5). A feed-forward mechanism (“central command”) originates in locomotor areas of the higher central nervous system; this is capable of producing parallel activation of medullary respiratory neurons and motor pathways to limb locomotor muscles and requires no feedback from the periphery. However, direct evidence for central command activation of ventilation during dynamic exercise in humans is lacking, although the rapid increase in ventilation at the onset of exercise supports the concept. Another locomotor-linked ventilatory stimulus is related to the chemical and mechanical conditions of the working muscle. Stimulation of thinly myelinated (group III) or unmyelinated (group IV) muscle afferents provokes powerful ventilatory and circulatory effects. These slowly conducting afferents respond to mechanical, chemical, and thermal stimuli (4).Clearly, the causal mechanism for LRC in humans is complex and not well understood. Although Huys et al. have proposed one possible mechanism, it is not clear how this fits into the general model of control of exercise hyperpnea. 1. Dempsey JA, Forster HV, and Ainsworth DM. Regulation of hyperpnea, hyperventilation, and respiratory muscle recruitment during exercise. In: Regulation of Breathing, edited by Dempsey JA and Pack AI. New York: Dekker, 1995, p. 1065-1134. Google Scholar2. Eldridge FL, Milhorn DE, Kily JP, and Waldrop TG. Stimulation by central command of locomotion, respiration and circulation during exercise. Respir Physiol 59: 313-337, 1985. Crossref | PubMed | Google Scholar3. Forster HV. Exercise hyperpnea: where do we go from here? Exerc Sport Sci Rev 28: 133-137, 2000. Google Scholar4. Kaufman MP and Forster HV. Reflexes controlling circulatory, ventilatory and airway responses to exercise. In: Exercise: Regulation and Integration of Multiple Systems, edited by Rowell LB and Shepard JT. New York: Oxford University Press, 1996, p. 381-442. Google Scholar5. Millhorn DE, Eldridge FL, Waldrop TG, and Kiley JP. Diencephalic regulation of respiration and arterial pressure during actual and fictive locomotion in cat. Circ Res 61, Suppl I: I53-I59, 1987. ISI | Google Scholar6. Siegmund GP, Edwards MR, Moore KS, Tiessen DA, Sanderson DJ, and McKenzie DC. Ventilation and locomotion coupling in varsity male rowers. J Appl Physiol 87: 233-242, 1999. Link | ISI | Google Scholar Download PDF Previous Back to Top Next FiguresReferencesRelatedInformation Cited ByCoordination between motor and cognitive tasks in dual task gaitGait & Posture, Vol. 85Human treadmill walking needs attention21 August 2006 | Journal of NeuroEngineering and Rehabilitation, Vol. 3, No. 1 More from this issue > Volume 96Issue 6June 2004Pages 2341-2342 Copyright & PermissionsCopyright © 2004 the American Physiological Societyhttps://doi.org/10.1152/japplphysiol.01341.2003PubMed15133019History Published online 1 June 2004 Published in print 1 June 2004 Metrics