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J Appl Physiol 96: 2187-2193, 2004. First published February 6, 2004; doi:10.1152/japplphysiol.00998.2003
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Ventilatory dynamics and control of blood gases after maximal exercise in the Thoroughbred horse

Danielle J. Padilla,1 Paul McDonough,1 Casey A. Kindig,2 Howard H. Erickson,1 and David C. Poole1,3

1Departments of Anatomy and Physiology, 3Kinesiology, Kansas State University, Manhattan, Kansas 66506; and 2Department of Medicine, University of California, San Diego, La Jolla, California 92093

Submitted 15 September 2003 ; accepted in final form 4 February 2004


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Despite enormous rates of minute ventilation (E) in the galloping Thoroughbred (TB) horse, the energetic demands of exercise conspire to raise arterial PCO2 (i.e., induce hypercapnia). If locomotory-respiratory coupling (LRC) is an obligatory facilitator of high E in the horse such as those found during galloping (Bramble and Carrier. Science 219: 251–256, 1983), E should drop precipitously when LRC ceases at the galloptrot transition, thus exacerbating the hypercapnia. TB horses (n = 5) were run to volitional fatigue on a motor-driven treadmill (1 m/s increments; 14–15 m/s) to study the dynamic control of breath-by-breath E, O2 uptake, and CO2 output at the transition from maximal exercise to active recovery (i.e., trotting at 3 m/s for 800 m). At the transition from the gallop to the trot, E did not drop instantaneously. Rather, E remained at the peak exercising levels (1,391 ± 88 l/min) for ~13 s via the combination of an increased tidal volume (12.6 ± 1.2 liters at gallop; 13.9 ± 1.6 liters over 13 s of trotting recovery; P < 0.05) and a reduced breathing frequency [113.8 ± 5.2 breaths/min (at gallop); 97.7 ± 5.9 breaths/min over 13 s of trotting recovery (P < 0.05)]. Subsequently, E declined in a biphasic fashion with a slower mean response time (85.4 ± 9.0 s) than that of the monoexponential decline of CO2 output (39.9 ± 4.7 s; P < 0.05), which rapidly reversed the postexercise arterial hypercapnia (arterial PCO2 at gallop: 52.8 ± 3.2 Torr; at 2 min of recovery: 25.0 ± 1.4 Torr; P < 0.05). We conclude that LRC is not a prerequisite for achievement of E commensurate with maximal exercise or the pronounced hyperventilation during recovery.

exercise recovery; locomotory-respiratory coupling; blood acid-base; equid

THE CONTROL OF MINUTE VENTILATION (E) differs between Thoroughbred (TB) horses and humans during maximal exercise. For example, the horse displays a strict 1:1 coupling of breathing to stride frequency [i.e., locomotory-respiratory coupling (LRC)] while cantering and galloping (8), whereas humans are not limited to a particular coupling ratio (7). Notwithstanding this constraint, the exercising TB horse can achieve prodigious values for pulmonary E (>1,800 l/min in extremely fit horses) and rates of gas exchange [i.e., O2 uptake (O2) of >70 l/min; CO2 output (CO2) of >80 l/min during maximal exercise] (35, 36). The relative E are similar in humans and horses but much less than those seen in dogs (a species of similar aerobic scope to the TB horse; Refs. 45, 48), which indicates that E during exercise may be limited as suggested by very low ventilatory equivalents for O2 (E/O2) and CO2 (E/CO2) resulting in pronounced hypercapnia (35). In this regard, it may be that LRC may actually limit E during brief, maximal exercise (26, 32).

In contrast to the above, LRC has been considered the key facilitator of E in TB horses, with high ventilatory volumes being achieved with supposedly little respiratory muscle contribution to exercise hyperpnea (8). However, electromyographic studies demonstrate that the diaphragm is highly active in running horses (2). Other indicators of the increased diaphragmatic activity include substantial transdiaphragmatic pressures (43) and high diaphragm muscle blood flows (31). In addition, the horse diaphragm is highly oxidative and, therefore, suited to sustained high-intensity respiratory efforts (38). It has also been shown recently that rib cage expansion is very limited and out of phase with inspiration in the galloping horse, which will serve to place a greater reliance on diaphragmatic vs. intercostal or accessory muscle breathing (32).

Whereas humans usually hyperventilate during intense exercise [e.g., arterial PCO2 (PaCO2) typically falls to values of <30 Torr; Refs. 10, 27] and defend arterial PO2 (PaO2) close to resting values, horses routinely become markedly hypercapnic and hypoxemic (6, 25, 35, 36) during brief, incremental exercise (PaCO2 of ~55–65 Torr; PaO2 of ~60–80 Torr). This hypercapnic response is a direct consequence of the extraordinarily high metabolic rate coupled with an inadequate ventilatory response in the TB (6, 35).

Horses and other quadrupeds (8) are considered to rely on LRC primarily during the canter and gallop to facilitate E, which would act to reduce the energetic cost of E. This would be advantageous because it would serve to minimize the redistribution of cardiac output from the exercising limbs to the respiratory muscles (3, 20). Indeed, in humans, reducing respiratory muscle work elevates the proportion of cardiac output available to the working limb muscles (21, 22).

The purpose of the present investigation was to explore the notion that, if LRC is an obligatory requirement for achieving very high E such as those present in the galloping horse, when LRC is removed abruptly at the onset of trotting, E should drop immediately and precipitously. Specifically, we tested the hypothesis that, at the onset of recovery from galloping [i.e., across the transition from the gallop (LRC present) to the trot at 3 m/s (no LRC)], E would fall precipitously and PaCO2 would increase transiently above end-exercise levels. By resolving, for the first time, the breath-by-breath responses of E and gas exchange (O2 and CO2) across the gallop-trot transition, we sought to gain novel insights into the control of breathing in the horse.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Animals. Five TB geldings (4–10 yr; 470–600 kg) were used in this investigation. Horses were housed in enclosed dry lots with a shaded area and fed alfalfa, grass hay, and concentrate twice daily, with water and salt available ad libitum. Deworming and vaccinations were administered at regular intervals. A high-speed treadmill (SATO, Uppsala, Sweden) was utilized to exercise horses at least twice weekly to maintain fitness and condition. All procedures were approved by the Kansas State University Institutional Animal Care and Use Committee.

Instrumentation. Before each trial, with the use of aseptic techniques, each horse was instrumented with a 7-Fr introducer catheter inserted into the right jugular vein, and an 18-gauge, 2.0-in. catheter was placed in a previously elevated carotid artery or transverse facial artery (20 gauge, 1.5 in. in 2 TB horses). Lidocaine (2%, i.e., 2 ml) was utilized subcutaneously for the insertion of the catheter in the carotid artery and jugular vein but not in the transverse facial artery (2 horses). To determine mean pulmonary artery temperature (for correction of arterial blood gases), a thermistor catheter was inserted through the 7-Fr introducer catheter and advanced into the pulmonary artery 8 cm past the pulmonary valve. Calibration of the thermistor catheter was conducted with the use of a Physitemp thermocouple thermometer (BAT-10, Physitemp, Clifton, NJ). To withdraw arterial blood, a cannula (1.6-mm inner diameter, 3.2-mm outer diameter) was attached to the arterial catheter.

Measurement of breath-by-breath gas exchange. To measure expired E, an ultrasonic phase-shift flowmeter (model FR-41eq; Flow-metrics-BDRL, Birmingham, UK) was used as described previously (52). Briefly, horses were outfitted with a lightweight fiberglass facemask (<1 kg). This mask was fitted internally with silicone rubber and foam gaskets to maintain an airtight seal. The flow tubes were then placed in the openings of the facemask opposite each nostril to allow measurement of airflow for each nostril. Each flow tube contained two ultrasonic transducers that quantified velocity of airflow at a resonant frequency of 40 kHz. Each ultrasonic phase-shift flowmeter (i.e., left and right) underwent a three-point calibration at -20, 0, and +20 l/s using a rotameter (KDG Flowmeters, Burgess Hill, UK) certified by the National Board of Standards. Because the system responded linearly to changes in airflow and the design characteristics of the flow probes negate the effects of temperature and humidity (52), the above calibration allowed for the measurement of the full extent of the exercise and recovery E response.

Right and left airway flows, as well as inspired and expired O2 and CO2, were collected with a commercial data analysis system (DATAQ, Akron, OH) and stored for later analysis. The conversion of E to STPD was conducted using standard equations, whereas O2 and CO2 were calculated using the principle of mass balance [i.e., O2 STPD = (I STPD x FIO2) - (E STPD x FEO2 STPD); and CO2 STPD = E STPD x (FE STPDCO2 - FI STPDCO2)]. Inspired and expired gas fractions (FI and FE, respecively) were measured using a mass spectrometer (Perkin-Elmer, model 1100, Pomona, CA), which was calibrated using gravimetrically determined gas concentrations that spanned the range of O2 and CO2 concentrations between the inspired air and that expired by the horse. Gas was sampled continuously via a sampling port attached between the two nostril openings of the fiberglass mask (i.e., between the nares of the horse).

Experimental protocol. An incremental exercise test was conducted with each TB horse on a level treadmill. The horses trotted (i.e., warmed up) at 3 m/s for 800 m, and the speed of the treadmill was rapidly increased to 7 m/s for 1 min, and then the speed was increased in 1 m/s increments until fatigue (i.e., the horse could no longer keep up with the speed of the treadmill despite humane encouragement). The treadmill was immediately slowed to 3 m/s for 800 m, and cardiovascular, E, and gas-exchange measurements (O2 and CO2) were continuously recorded from the immediate offset of maximal exercise and throughout the 4-min recovery period. Arterial blood samples were collected, and pulmonary arterial temperature was recorded during the last 10 s of the final stage of exercise and at 2 and 4 min of the recovery period.

Blood analysis. Arterial blood samples were placed immediately on ice after anaerobic withdrawal (~5 ml) into plastic, heparinized syringes. Blood gases (PaO2 and PaCO2), pH, and plasma lactate concentrations were quantified after the exercise test (within 1–2 h) with a blood-gas analyzer (Nova Stat Profile, Waltham, MA). Blood gases and pH were then corrected to the individual horse's pulmonary arterial temperature (16). To ensure technical and internal consistency, one person conducted all blood analyses. Equipment was calibrated before and after each exercise test in accordance with manufacturers' standards.

Modeling of O2, CO2, and E. Four-breath rolling averages for O2, CO2, and E were used for modeling data. Curve fitting was accomplished with KaleidaGraph software (Synergy software, Reading, PA) and was performed on the gallop-trot transition data using a one-component model

and a more complex, two-component model

where indicates the gas-exchange variable of interest (i.e., O2, CO2, or E), t is a given time point, b is baseline (end-exercise), A1 and A2 are the response amplitudes, TD1 and TD2 are the independent time delays, and {tau}1 and {tau}2 are the time constants.

Goodness of model fit was determined via three criteria: 1) the coefficient of determination (i.e., r2), 2) the sum of the squared residuals term (i.e., {chi}2), and 3) visual inspection of the model. The time delay from end exercise until the beginning of the response for E was determined independent of model estimates because the response varied considerably between horses [i.e., in some, E increased before falling (n = 3), whereas E remained stable in others (n = 2)]. Mean response times (MRTs) were calculated from the model parameters using the following equation for the one-component model

and for the two-component model (see Ref. 30)

Statistics. A repeated-measures ANOVA was used for each variable compared over time. If significance was revealed, a Student-Newman-Keuls post hoc test was utilized to determine the point of significance. Paired t-tests were used to determine whether the two-component model provided a statistically better fit to the data than the one-component model. Between-variable comparisons were made by unpaired t-tests. Where a directional hypothesis was tested, a one-tailed test was utilized. Statistical significance was accepted at a P value of <=0.05.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
E. In the absence of overt pathology, the flow profiles for the left and right nostrils are almost superimposable. For the horses studied in the present investigation, the flow profiles from each nostril were remarkably similar throughout both exercise and recovery. Determination of inspired and expired volumes and E were made using the total flow through both the left and right nostrils.

After the gallop-trot transition, E remained elevated at or above end-exercise values for ~13 s, after which E fell biphasically (Fig. 1). Quantitatively, E was best characterized by a dual-exponential model with a fast and slow phase (Table 1; Fig. 1) and a MRT of 85.4 ± 9.0 s (Table 1; Fig. 1), which was significantly longer than the MRT of either CO2 or O2 (Table 1; Figs. 1 and 2). The two-component nature of the response was confirmed via a significantly higher correlation coefficient [0.96 (two-component) vs. 0.93 (one-component); P < 0.05] and a lower sum of squares residual term [1.0 x 105 (two-component) vs. 1.78 x 105 (one-component); P < 0.05]. The prolongation of the exercise E into recovery and the biphasic nature of the subsequent E decrease in trotting recovery were due, in part, to a radical change in breathing strategy (Table 2; Fig. 3). Specifically, over the first 7–13 s of recovery, tidal volume (VT) rose and breathing frequency (f) fell significantly (Table 2). After this period, f and VT remained at end-exercise levels for 30 s. After 30 s, VT fell progressively with time, but f did not differ from end-exercise values (Fig. 3; Table 2). At the end of the 4-min recovery period, E was still 44.5 ± 18.5% (e.g., Figs. 1 and 3) above trotting baseline values.



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  		Fig. 1. Minute ventilation (E) and CO2 output (CO2) responses at the gallop-trot transition (~14 m/s to 3 m/s) and throughout trotting recovery (4 min) in a representative horse. Data are fit with a time delay plus 2-component exponential (E, top) and 1-component exponential (CO2, bottom) model. Trotting baseline (BL) values are shown for this horse. Note the markedly different temporal responses between E and CO2.

 

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  		Table 1. Model parameters of E, CO2, and O2 responses during the trotting recovery period from maximal exercise

 


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  		Fig. 2. O2 uptake (O2) response at the gallop-trot transition (~14 m/s to 3 m/s) and throughout trotting recovery (4 min) for the same representative horse as in Fig. 1. Data are fit with a time delay plus 1-component exponential model. Trotting BL value is shown for this horse.

 

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  		Table 2. Recovery values at specified times for f, VT, and E

 


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  		Fig. 3. E, breathing frequency (f), and tidal volume (VT) for the same representative horse as in Figs. 1 and 2 at rest and during the incremental exercise test and trotting recovery. Arrows denote beginning of trotting recovery period. Time Axis

 

O2 and CO2. VCO2 and VO2 both fell with a monoexponential profile after the gallop-trot transition (Figs. 1 and 2, respectively; Table 1) with MRTs of 39.9 ± 4.7 and 28.9 ± 3.2 s, respectively (P < 0.05). Both O2 and CO2 apparently resolved to an elevated baseline (9.8 ± 36.0 and 17.5 ± 30.9% above the pregallop, trotting baseline for O2 and CO2, respectively; e.g., Figs. 2 and 1, respectively). However, compared with E, CO2 and O2 were relatively closer to trotting baseline values after the 4-min recovery period (Table 1; Figs. 1 and 2, respectively).

Blood gas response across the gallop-trot transition. The hypercapnia found during exercise was completely reversed within 2 min after the gallop-trot transition, and the ensuing hypocapnia was maintained through 4 min of trotting (Fig. 4; PaCO2 at gallop: 52.8 ± 3.2 Torr; 2 min of trot: 25.0 ± 1.4 Torr; 4 min of trot: 24.6 ± 1.5 Torr; both P < 0.05 vs. gallop). This hyperventilation is further evidenced by the pronounced increase in the ratio of E to CO2 (from ~20 at the gallop to ~60 within 1–2 min of trotting recovery; e.g., Fig. 4). Plasma lactate was elevated to 25.5 ± 4.0 mM at the gallop and remained unchanged throughout the recovery period (2 min of trot: 24.9 ± 3.6 mM; 4 min of trot: 24.5 ± 3.7 mM). Arterial pH increased from the gallop (7.217 ± 0.107) to 2 min of trot (7.301 ± 0.093; P < 0.05) but did not differ between 2 and 4 min (7.307 ± 0.098) of the recovery period.



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  		Fig. 4. Ventilatory equivalents for O2 (E/O2) and CO2 (E/CO2), and arterial PO2 (PaO2) and arterial PCO2 (PaCO2) for the same representative horse as in Figs. 1 and 2 at rest and during the incremental exercise test and trotting recovery. Arrows denote beginning of trotting recovery period.

 

Core temperature changes across the gallop-trot transition. Pulmonary arterial temperature decreased (P < 0.05) from the gallop (41.6 ± 0.9°C) to 2 min of trot (40.6 ± 0.7°C) but did not change subsequently between 2 and 4 min (40.4 ± 0.7°C) of the recovery period.


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
ACKNOWLEDGMENTS
 REFERENCES
 
To the best of our knowledge, this is the first study to provide a breath-by-breath analysis of E, gas exchange (i.e., O2 and CO2), and related metabolic and blood-gas measurements across the gallop-trot transition at the cessation of maximal exercise in the TB horse. The finding that E did not decrease abruptly at the gallop-trot transition suggests that any mechanical link between locomotion and respiration (i.e., LRC) does not constitute an obligatory component of extraordinary E commensurate with those found during exercise. Specifically, an abrupt reduction in stride length and frequency, as seen at the transition from galloping to trotting (i.e., 3 m/s), and the removal of the synchrony between stride and breathing frequency (LRC) did not reduce E instantaneously. Furthermore, given the finite CO2 dynamics, had a precipitous fall in E occurred, it would be expected to sustain or even exacerbate the exercise-induced hypercapnia (i.e., elevate PaCO2 further). In contrast to this notion, our results show that the hypercapnia and hypoxemia of exercise are quickly reversed (at least within 2 min) because E remained at peak galloping levels for ~13 s of the postgallop trot (due to an altered breathing strategy) before decreasing relatively slowly in the presence of more rapid reductions of O2 and CO2 (i.e., ratios of both E/O2 and E/CO2 increased). Thus, after the transition of gallop to trot, compensatory hyperventilation was evident. One putative interpretation of this behavior is that LRC at the gallop may have restricted the full magnitude of the exercise hyperpnea. When this constraint was removed, the E/CO2 ratio rose to a level that ensured a respiratory compensation for metabolic acidosis (PaCO2 of <20 Torr) and restored PaO2 to preexercise levels. Although the possibility remains that LRC may contribute to exercise hyperpnea, data from the present investigation demonstrate that the TB horse can attain E values equivalent to those during galloping in the absence of LRC during postmaximal exercise trotting recovery.

Role of LRC in the horse. LRC has been presented as a "general requirement for sustained aerobic activity among endothermic vertebrates" (8). Some researchers maintain that LRC functions to enhance pulmonary airflow during the gallop in the horse (5, 26). However, it is also clear that racing breeds, in contrast to their more pedestrian counterparts (see Ref. 11), become considerably hypoxemic and hypercapnic (6, 9, 15, 36, 47) during brief, maximal exercise, suggestive of some sort of "functional" ventilatory restraint. That this restraint is not the result of an absolute limitation to ventilation per se is supported by studies using heliox inspirates (14) and hypoxia (37). In addition, the results of the present study, where E remained at or rose above (3 of 5 horses) end-exercise values for the first 7–13 s of recovery also argues against any purely mechanical limitation to airflow generation.

Marlin et al. (via respiratory inductance plethysmography; Ref. 32) have shown that (during the canter and gallop) VT is increased by abdominal elongation and expansion consistent with a major diaphragmatic contribution to inspiration, whereas Ainsworth et al. (2) determined (via electromyogram analysis) that diaphragmatic contractions are always in phase with esophageal pressure changes and inspiratory flow generation as exercise intensity increases. These results suggest that inspiratory tidal airflow generation during running in the horse may be the sole province of the diaphragm, a contention that is supported by the extraordinary thickness, oxidative capacity, and blood flow capacity of the equine diaphragm (31, 38).

Although LRC may limit airflow generation during running in the horse, one potential benefit of a LRC-derived constraint on exercise ventilation can be gleaned from the work of Harms et al. (21, 22). These authors reported that the work of breathing can affect performance and time to fatigue in humans by redistributing flow away from the locomotory and toward the respiratory muscles. As the work of breathing increases to a much greater degree in the horse than the human (cf. Refs. 1 and 3), this mechanism has perhaps an even greater fatigue-generation potential in the horse. This is particularly true because the TB horse is thought to rely primarily on diaphragmatic breathing (2, 32) during the gallop; thus any attempt to overcome the constraint resulting from LRC could well lead to both diaphragmatic and locomotory muscle fatigue.

Unlike TB horses, Standardbred horses can achieve their maximum O2 while trotting or pacing when the breathing and stride frequencies are not coupled. The maximum O2 in competitive Standardbred horses (i.e., ~165 ml · kg-1 · min-1; see Refs. 4 and 18) is close to that found in the TB horse. However, VT is far higher (20–26 vs. 12–14 l/breath) and f is lower (70–80 vs. 130 breaths/min) in the Standardbred vs. the TB horse. Therefore, for Standardbred horses at the transition from the maximum speed to either resting or a lower speed, one would not expect the same response as is found in the TB horse (i.e., increasing VT, lowering of f). Indeed, Standardbred horses increase f and decrease VT across this transition. Thus, although the strategy is different, one common feature across these two breeds is that both hypoventilate during intense exercise (i.e., E/O2, E/CO2, and PaO2 fall, and PaCO2 rises) and hyperventilate in recovery (4, 35).

Mechanistic basis for slow E recovery in TB horse. In the TB horse, the presence of hypoventilation during maximal exercise and noticeable hyperventilation (see Fig. 4) during recovery suggests strongly that, in considerable contrast to humans (51), PaCO2 is not a precisely controlled variable in equids (35, 39). In addition, the observation that E remains at or above end-exercise values during the early recovery period (Figs. 1 and 3) constitutes strong evidence that LRC may actually provide an impedance to E during exercise, whereas the slow, prolonged recovery profile for E suggests multiple sources of ventilatory control during recovery from maximal exercise.

Initial ("fast") component of E. Throughout high-intensity exercise, PaCO2 is markedly elevated in the TB horse (35, 36). As TB horses exhibit a normal ventilatory response to CO2 at rest (in contrast to the situation during exercise; Ref. 28), it is likely that CO2 is providing at least some of the initial stimulus responsible for the elevation of E noted in the present study. Indeed, VT increased rapidly, whereas f fell (Fig. 3 and Table 2), indicative of increased alveolar ventilation and enhanced CO2 elimination (51). However, by 2 min of recovery, PaCO2 had fallen to hypocapnic levels (Fig. 4), whereas E was still elevated, which strongly suggests that the ventilatory response was being maintained at this point by other stimuli.

Secondary ("slow") component of E. The secondary component of E during recovery started at ~90 s of recovery, likely at a time point when PaCO2 was already well below 40 Torr (see E/CO2 profile in Fig. 4). Although pH at end exercise (7.217 ± 0.107) and during recovery (2 min: 7.301 ± 0.093; 4 min: 7.307 ± 0.098) is reduced below trotting baseline, these values are not different from those reported in humans (46) or in the pony (39), which, unlike its more fit relative, exhibits a more rapid E recovery-response profile. In addition, the changes in pH and E were not correlated.

It is also generally acknowledged that there is an extensive array of ventilatory stimuli present during and after intense exercise. Thus the control of the exercise (and postexercise) hyperpnea is complex and demonstrates considerable redundancy (for review, see Ref. 50). In early recovery after the gallop-trot transition, potential sources of ventilatory stimulation include arterial acidosis (lactic acidosis and hypercapnia), elevated catecholamines, temperature, potassium ions (K+), osmolality, venous distension, and/or some form of short-term potentiation (STP). This STP was originally termed "respiratory afterdischarge" by Gesell and White (19) and has subsequently been described as an exponential ventilatory response that decays relatively slowly after removal of the stimulus. Specifically, STP decays with a time constant ranging from 36 to 101 s after carotid sinus nerve stimulation in cats (12, 13) and 18 to 39 s after hypoxic exercise in humans (17). Thus, if present in the TB horse, STP may have potentially played a role in the prolonged ventilatory response that was found during trotting recovery described herein.

The present investigation was not designed to determine which of these above mediators induced the postgalloping elevated ventilatory response. However, the temporal profile of some of these mediators decreases the likelihood that they played a major role in the extended hyperventilation seen in the trotting recovery. For example, the exercise-induced hypercapnia was resolved at least by 2 min, at which time the PaCO2 had been driven substantially below resting values. Whereas catecholamines were not measured in the present investigation, Snow et al. (44) observed that blood catecholamine levels returned close to resting levels within 60 s postexercise, which is much faster that the E response. In addition, K+ recovers to baseline values within ~2 min of recovery (23).

How are ventilation and hyperthermia linked? Respiratory heat exchange occurs in many mammalian species that primarily employ nasal breathing (42). In large mammals such as the camel (41) and the horse (24, 34), ventilation during heat stress serves to maintain brain temperature as much as several degrees Celsius below core body temperature (34, 49). Although horses employ a robust sweating response (rates of >30 l/h) that works in concert with the respiratory system to dissipate heat during exercise (24), these responses are not adequate to prevent heat storage during exercise, in part due to a relatively low surface area-to-body mass ratio in the racing horse. Thus, during exercise, the TB horse routinely achieves core body temperatures up to ~42–43°C (24, 34, 49). During trotting recovery, with the locomotory muscles operating at a much reduced metabolic rate compared with the gallop, evaporative heat loss from the respiratory tract will augment heat dissipation and provides one possible explanation for the prolonged elevation in E seen postgalloping. This strategy may be affected, in part, by the adoption of an altered breathing pattern during the recovery from high-intensity exercise.

Core temperature follows a slow recovery time course after incremental exercise (33). In this investigation, core temperature was markedly elevated throughout recovery (~40.5°C at 4-min postgallop), and the rate of change in E during the secondary recovery component was highly correlated with that of core temperature (r2 = 0.998; P < 0.05). Given that hyperthermia does constitute a powerful E stimulus in the horse (33) and that the temporal profile of other potential E stimuli (i.e., K+, catecholamines, PaCO2) during recovery from exercise in the horse does not cohere with that of E, the possibility must be acknowledged that the hyperthermia, which attends maximal exercise and recovery in TB horses, may potentially contribute to the prolonged hyperventilatory response found during recovery.

In conclusion, rather than exhibiting the precipitous fall in E such as that observed in humans after intense exercise (29, 40, 46), horses sustain the full magnitude of the exercise hyperpnea for several seconds into recovery followed by a prolonged biphasic decrease in E. This sustained hyperpnea is the product of an immediate increase in VT combined with a fall in f (Table 2 and Fig. 3). Because an immediate fall in E was not found during the off-transition from the gallop (LRC present) to the trot (no LRC), we conclude that LRC does not appear requisite to achieve a prodigiously high E equivalent to that seen during maximal exercise.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
REFERENCES
 
The authors thank Dr. Casey Ramsel, Dr. Melissa Finley, Angie Dick, Ann Otto, Leslie Mikos, Joanna Thomas, and Dani Goodband.

GRANTS

This work was supported by the National Heart, Lung, and Blood Institute Grants HL-69739 and HL-50306 and the American Quarter Horse Association. C. A. Kindig is a Parker B. Francis pulmonary fellow.


   FOOTNOTES
 

Address for reprint requests and other correspondence: D. C. Poole, Dept. of Anatomy and Physiology, 228 Coles Hall, Kansas State Univ., Manhattan, KS 66506 (E-mail: poole{at}vet.k-state.edu).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 

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