Summary
To investigate the relative contributions of the central and peripheral neural drive to hyperventilation at the onset of muscular exercise, five volunteers were tested during the first ten breaths while performing both voluntary (VM) and passive (PM) ankle rotations with a frequency of 1 Hz and through an angle of 10°. Resulting breathing patterns for the two movements were compared. Hypocapnic hyperventilation, found in both PM and VM, indicated its neural origin. Respiratory changes were higher in VM than in PM. In both experimental conditions, increases in ventilation (\(\dot V_E \)) depended more on respiratory frequency (f) than on tidal volume (V T). Moreover, increases inV T adapted, breath-by-breath, to values lower than the initial ones, while increases inf rose progressively. Expiratory time was reduced more than inspiratory time (T I); increases in inspiratory flow (V T/T I) depended to the same extent on changes in bothT I andV T. Increases in expiratory tidal volume were initially higher than in inspiratory tidal volume, thereby producing a reduction in functional residual capacity. Because PM respiratory changes could be considered to be of nervous reflex origin only, the identical breathing patterns in PM and VM indicated that the hyperventilation found also in VM was mainly of reflex origin. The increase in\(\dot V_E \) was considered to be dependent on a greater stimulus from muscle proprioreceptors.
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Adams L, Garlick J, Guz A, Murphy K, Semple SJG (1984) Is the voluntary control of exercise in man necessary for the ventilatory response? J Physiol 355:71–83
Agostoni E, D'Angelo E (1976) The effect of limb movements on the regulation of depth and rate of breathing. Respir Physiol 27:33–52
Bechbache RR, Duffin J (1977) The entrainment of breathing frequency by exercise rhythm. J Physiol 272:553–561
Carcassi AM, Concu A, Decandia M, Onnis M, Orani GP, Piras MB (1983) Respiratory responses to stimulation of large fibers afferent from muscle receptors in cats. Pflügers Arch 399:309–314
Carcassi AM, Concu A, Decandia M, Onnis M, Orani GP, Piras MB (1984) Effects of long-lasting stimulation of extensor muscle nerves on pulmonary ventilation in cats. Pflügers Arch 400:409–412
Clark FJ, Von Euler C (1972) On the regulation of depth and rate of breathing. J Physiol 222:267–295
Dejours P (1963) The regulation of breathing during muscular exercise in man. A neuro-humoral theory. In: Cunningham DJC, Lloyd BB (eds) The regulation of human respiration. Blackwell, Oxford, pp 535–547
Dejours P (1967) Neurogenic factors in the control of ventilation during exercise. Circ Res 20 [Suppl I]:146–153
Eldridge FL, Gill-Kumar P, Millhorn DE, Waldrop TG (1981) Spinal inhibition of phrenic motoneurones by stimulation of afferents from peripheral muscles. J Physiol 311:67–69
Eldridge FL, Millhorn DE, Kiley JP, Waldrop TG (1985) Stimulation by central command of locomotion, respiration and circulation during exercise. Respir Physiol 59:313–337
Favier R, Desplanches D, Frutoso J, Grandmontagne M, Flandrois R (1983a) Ventilatory and circulatory transients during exercise: new arguments for a neurohumoral theory. J Appl Physiol 54:647–653
Favier R, Desplanches D, Frutoso J, Grandmontagne M, Flandrois R (1983b) Ventilatory transient during exercise: peripheral or central control? Pflügers Arch 396:269–276
Flandrois R, Lacour JR, Islas-Maoquin J, Charlot J (1967) Limb mechanoreceptors inducing the reflex hyperpnea of exercise. Respir Physiol 2:335–343
Fordyce WE, Bennet FM, Edelman SK, Grodins FS (1982) Evidence in man for a fast neural mechanism during the early phase of exercise hyperpnea. Respir Physiol 48:27–43
Green JF, Schertel ER, Coleridge HM, Coleridge JCG (1986) Effect of pulmonary arterial PCO2 on slowly adapting pulmonary stretch receptors. J Appl Physiol 60:2048–2055
Goodwin GM, McCloskey DI, Mitchell JH (1972) Cardiovascular and respiratory responses to changes in central command during isometric exercise at constant muscle tension. J Physiol 226:173–190
Iscoe S, Polosa C (1976) Synchronization of respiratory frequency by somatic afferent stimulation. J Appl Physiol 40:138–148
Jammes Y, Mathiot MJ, Roll JP, Prefaut C, Berthelin F, Grimaud C, Milic-Emili J (1981) Ventilatory responses to muscular vibrations in healthy humans. J Appl Physiol 51:262–269
Kagawa J, Kerr HD (1970) Effects of brief graded exercise on specific airway conductance in normal subjects. J Appl Physiol 28:138–144
Kao FF, Schlig BB, McC Brooks C (1955) Regulation of respiration during induced muscular work in decerebrate dogs. J Appl Physiol 7:379–386
Kaufman MP, Rybicki KJ, Mitchell JH (1985) Hindlimb muscular contraction reflexly decreased total pulmonary resistance in dogs. J Appl Physiol 59:1521–1526
Kay JDS, Petersen ES, Vejby-Christensen H (1975) Breathing in man during steady-state exercise on the bicycle at two pedalling frequencies, and during treadmill walking. J Physiol 251:645–656
Koizumi K. Ushiyama J, Brooks C McC (1961) Muscle afferents and activity of respiratory neurons. Am J Physiol 200:679–684
Martin BJ, Weil JV (1979) CO2 and exercise tidal volume. J Appl Physiol 46:322–325
McCloskey DI, Mitchell JH (1972) Reflex cardiovascular and respiratory responses originating in exercising muscle. J Physiol 224:173–186
McIlroy MB, Marshall R, Christie RV (1954) The work of breathing in normal subjects. Clin Sci 13:127–136
Sargeant AJ, Rouleau MY, Sutton JR, Jones NL (1981) Ventilation in exercise studied with circulatory occlusion. J Appl Physiol 50:718–723
Senapati JM (1966) Effect of stimulation of muscle afferents on ventilation of dogs. J Appl Physiol 21:242–246
Sharratt MT, Henke KG, Aaron EA, Pegelow DF, Dempsey JA (1987) Exercise-induced changes in functional residual capacity. Respir Physiol 70:313–326
Tobin MJ, Perez W, Guenther SM, D'Alonzo G, Dantzker DR (1986) Breathing pattern and metabolic behavior during anticipation of exercise. J Appl Physiol 60:1306–1312
Von Euler C (1977) The functional organization of the respiratory phase-switching mechanisms. Fed Proc 36:2375–2380
Waldrop TG, Mullins DC, Henderson MC (1986a) Effects of hypothalamic lesions on the cardiorespiratory responses to muscular contraction. Respir Physiol 66:215–224
Waldrop TG, Mullins DC, Millhorn DE (1986b) Control of respiration by the hypothalamus and by feedback from contracting muscles in cats. Respir Physiol 64:317–328
Ward SA (1979) The effects of sudden airway hypercapnia on the initiation of exercise hyperpnoea in man. J Physiol 296:203–214
Wasserman K, Whipp BJ, Castagna J (1974) Cardiodynamic hyperpnea: hyperpnea secondary to cardiac output increase. J Appl Physiol 36:457–464
Yamashiro SM, Grodins FS (1973) Respiratory cycle optimization in exercise. J Appl Physiol 35:522–525
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Concu, A. Contribution of central and reflex nervous activity to the rapid increase in pulmonary ventilation at the start of muscular exercise in man. Europ. J. Appl. Physiol. 59, 10–15 (1989). https://doi.org/10.1007/BF02396573
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DOI: https://doi.org/10.1007/BF02396573