The control of ventilation is dissociated from locomotion during walking in sheep

Abstract

This study was designed to test the hypothesis that the frequency response of the systems controlling the motor activity of breathing and walking in quadrupeds is compatible with the idea that supra-spinal locomotor centres could proportionally drive locomotion and ventilation. The locomotor and the breath-by-breath ventilatory and gas exchange (CO2 output (VCO2) and O2 uptake (VO2)) responses were studied in five sheep spontaneously walking on a treadmill. The speed of the treadmill was changed in a sinusoidal pattern of various periods (from 10 to 1 minute) and in a step-like manner. The frequency and amplitude of the limb movements, oscillating at the same period as the treadmill speed changes, had a constant gain with no phase lag (determined by Fourier analysis) regardless the periods of oscillations. In marked contrast, when the periods of speed oscillations decreased, the amplitude (peak-to-mean) of minute ventilation (VE) oscillations decreased sharply and significantly (from 6.1 +/- 0.4 l min(-1) to 1.9 +/- 0.2 l min(-1)) and the phase lag between ventilation and treadmill speed oscillations increased (to 105 +/- 25 degrees during the 1 min oscillation periods). VE response followed VCO2 very closely. The drop in VE amplitude ratio was proportional to that in VCO2 (from 149 +/- 48 ml min(-1) to 38 +/- 5 ml min(-1)) with a slightly longer phase lag for ventilation than for VCO2. These results show that beyond the onset period of a locomotor activity, the amplitude and phase lag of the VE response depends on the period of the walking speed oscillations, tracking the gas exchange rate, regardless of the amplitude of the motor act of walking. Locomotion thus appears unlikely to cause a simple parallel and proportional increase in ventilation in walking sheep.

Figure 1. Example of end tidal P_CO2 and ventilatory responses during a walking test (4.5 km h⁻¹ from rest) 12 h (right panels) and 30 h (left panels) after food ingestion in one sheep

Note that within the first 18 h, a large number of episodes of eructation (rise in P_ETCO2) and swallowing related to rumination provoked rhythmic hypoventilation and hyperventilation. After 30 h, ventilation was stable allowing reproducible measurements.

Figure 2. Temporal profile of the averaged pulmonary gas exchange (V̇_O2, open symbols V̇_CO2 filled symbols) and ventilatory response to a walking test (4.5 km h⁻¹) of the five sheep (10 tests)

Exercise starts at the vertical line. Note that ventilation reached a steady state within less than 2 min

Figure 3. Example in one sheep of the locomotor response during walking with the fastest speed oscillations used in the study, i.e. 1 min period (from 3 to 6 km h⁻¹)

From top to bottom: speed imposed by the treadmill, signal from the goniometers, frequency and amplitude of movement (in arbitrary units) obtained from the goniometric raw data. Note that (1) the increase in walking speed consists mostly of a sinusoidal change in the frequency of walking and (2) both the changes in the frequency and the amplitude of movement are in perfect phase with the treadmill speed oscillations.

Figure 4. Example in one sheep of the locomotor (frequency of movement), V̇_O2, V̇_CO2, ventilation and P_ETCO2 responses to three different treadmill speed oscillation periods

The fundamental component of the responses computed by Fourier analysis is superimposed on the raw data and the residuals for ventilation (after suppression of the fundamental component of the response) are shown in the lower panel. Note that the change in walking frequency is in phase with the sinusoidal changes in the speed of the treadmill with a constant amplitude. There is a clear reduction in amplitude of both pulmonary gas exchange and ventilation when the oscillation period decreases whereas the phase lag between walking frequency and the respiratory parameters increases. Finally, note that (1) P_ETCO2 oscillates with a small amplitude in phase with ventilation and (2) the residual data for ventilation are not influenced by the locomotor activity.

Figure 5. Amplitude of the respiratory and locomotor responses as a function of the frequency of the sinusoidal changes in treadmill speed

A, amplitude of the ventilatory and of the locomotor responses (mean ±s.e.m.) at each frequency of treadmill speed oscillation. Zero frequency corresponds to the steady-state response. Note the dissociation between the lack of change in the oscillations of the frequency of movement and the progressive reduction in V̇_E amplitude when the frequency of treadmill speed oscillations increases. B, amplitude of the V̇_O2 and V̇_CO2 responses at each frequency of treadmill speed oscillation. Note that V̇_O2 amplitude starts to decrease at a higher frequency than V̇_CO2 (and V̇_E), reflecting faster V̇_O2 than V̇_CO2 kinetics. C–E, relationship between the gain ratio (steady-state response–amplitude response ratio at each frequency) of ventilation and V̇_CO2 (C) V̇_O2 (D) and the locomotor response (E). Note that the change in amplitude ratio of the locomotor response has no relationship with the ventilatory response, which appears to follow the pulmonary gas exchange amplitude ratio.

Figure 6. Phase lag between treadmill speed oscillations and CO₂ output (open squares), ventilation (filled circles), V̇_O2 (filled squares) and the locomotor response (frequency of walking, open circles) at each frequency of treadmill speed oscillation

Note that the phase lag of ventilation follows that of CO₂ output very closely. The increase in V̇_O2 phase lag is less pronounced than V̇_CO2 and V̇_E. The frequency response of locomotor response is flat.

Figure 7. Amplitude and phase of P_ETCO2 response as a function of the frequency of the sinusoidal changes in treadmill speed

Note that the amplitude of P_ETCO2 oscillations is small and is not affected by the frequency of the input.

Figure 8. Phase lag between CO₂ output, ventilation, oxygen uptake and treadmill speed sinusoidal oscillations in sheep (left panel) work rate sinusoidal oscillations in humans (humans WR, middle panel) and pedalling frequency oscillations in humans (humans freq, right panel) at three different periods of oscillations

Data in humans were computed from the studies of Casaburi et al. (1977, . The shorter ventilatory phase lag in sheep than in humans (middle panel) was always associated with faster V̇_CO2 kinetics in the former. Oxygen uptake phase lags were always much shorter than V̇_CO2 in both species. Note the fast dynamics in pulmonary gas exchange and ventilation when fluctuating changes in pedal frequency are applied (see text for comments).