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1 Department of Physiology3 Department of Anaesthesia, Medical Sciences Building, King's College Circle, University of Toronto, Canada2 Faculty of Medical Sciences, MWF-complex, A. Deusinglaan 1, University of Groningen, the Netherlands
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(Received 30 July 2004;
accepted after revision 19 January 2005; first published online 21 January 2005)
Corresponding author J. Duffin: Department of Physiology, University of Toronto, 1 King's College Circle, Toronto, Ontario, Canada M5S 1A8. Email: j.duffin{at}utoronto.ca
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Introduction |
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As well as the mechanisms of central motor command and afferent feedback, there is a third neural mechanism capable of providing a drive to breathe at the onset of exercise. The central neural drives to breathe that are most often collectively referred to as ‘wakefulness’ involve mechanisms of arousal or changes in behavioural state (Shea, 1996). Indeed, the mere neural process of imagining exercise under hypnosis will increase breathing in a manner similar to exercise itself (Thornton et al. 2001). It therefore seems likely that these behaviourally controlled drives to breathe could also contribute to the initial phase of exercise hyperpnoea.
Despite this possibility, the contribution of such behavioural drives to breathe during the initial phase of exercise hyperpnoea has received little attention, perhaps because of the methodological complications of isolating such a drive to breathe. Our present understanding of respiratory control suggests that if there were a simple summation of the neural drives to breathe that are concurrently activated at the onset of exercise, they would collectively provide for an increase in ventilation at the onset of exercise in excess of that observed (Waldrop et al. 1986). As such, there is likely to be an interaction between these neural mechanisms that determine the actual increase in ventilation observed at the start of exercise. Indeed, several sites in the central nervous system where central command and afferent feedback may interact or be integrated have been suggested (Waldrop et al. 1986; Richard et al. 1989; Degtyarenko & Kaufman, 2000).
Previously, we demonstrated that the rapid increase in ventilation at the onset of passive leg movement was effectively eliminated while performing a cognitive task (Bell & Duffin, 2004). We interpreted this finding to mean that there may be an interaction between behavioural drives to breathe and limb movement afferent feedback, such that wakefulness or arousal is capable of suppressing the afferent feedback respiratory drive. We speculate that behaviour-related drives to breathe may provide a means of rapidly regulating ventilatory drives from concurrently recruited sources at the onset of exercise. If this is true, then altering the level of background arousal should affect the ventilatory response to exercise.
Indeed, there is some evidence for a behavioural modification of the exercise response; Wasmund et al. (2002) found that the cardiovascular response to handgrip exercise is reduced during a mental task and Rousselle et al. (1995) discovered that the respiratory response to cycling exercise was less when combined with mental activity. However, these studies did not examine the fast increase in ventilation at the onset of exercise that is believed to reflect the combined operation of putative central command and afferent feedback mechanisms.
We therefore sought to determine whether the level of background wakefulness has an effect upon ventilatory dynamics at the onset of exercise, when neural drives to breathe in addition to afferent feedback are assumed to be present. We examined the respiratory response to 3 min of leg extension exercise, under two different conditions of background wakefulness; one in which subjects solved a computer-based puzzle and one in which they did not. We hypothesized that increasing wakefulness or arousal via a cognitive task would blunt the increase in ventilation at the onset of exercise, and report that the increase in ventilation at exercise onset was depressed by the cognitive task.
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Methods |
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General procedures
Subjects completed two exercise sessions that were identical except that during one session they solved the computer-based puzzle and in the other they did not. The common elements of the two sessions involved monitoring the subject during rest and active exercise on a tandem chair apparatus, previously described in detail (Bell & Duffin, 2003; Bell et al. 2003). An elastic load (Thera-BandTM, Hygenic Corporation, Akron, OH, USA) was placed between the frame of the chair apparatus and the most distal length of the leg extension arm on both sides of the chair, and adjusted such that at maximum extension there was 6.0 kg of resistance. The range of motion of the lower leg was an angle of approximately 70 deg and exercise was performed at a frequency of approximately 70 cycles min–1 per leg in an alternating fashion.
Subjects were monitored at rest to collect no less than 3 min of stable resting data, and once this interval of rest had passed, subjects were instructed to begin exercise using the simple word, ‘begin’. After 3 min of exercise the subjects were instructed to stop exercise using the simple word, ‘stop’, and monitoring continued for another 3 min. This common procedure was performed twice in a quiet, temperature-controlled laboratory, under two conditions whose order was pseudo-randomized, based upon the subject's order of entry into the study. (1) The subject was awake and relaxed, seated in the exercise chair. This condition will be referred to as the low wakefulness (LW) protocol. (2) The subject was awake and solving a computer-based puzzle called the ‘Tower of Hanoi’ on a notebook computer throughout this entire data collection interval, while seated in the tandem chair. This condition will be referred to as the high wakefulness (HW) protocol.
Cognitive task
Throughout the HW protocol, subjects solved a puzzle called The Tower of Hanoi, based upon the puzzle invented by French mathematician Edouard Lucas in 1883. This puzzle has been described in detail in a previous study (Bell & Duffin, 2004). This puzzle (software) was available as freeware on the internet during the time of completion of this study (http://www.mazeworks.com/hanoi/, Copyright © 2002 David Herzog).
Data collection
Subjects breathed through a facemask (model KM201/202/203, Vacu-Med, Ventura, CA, USA) directly coupled to a turbine (Universal Ventilation Meter, model 17125, Vacu-Med) measuring ventilation. The distal end of the turbine was coupled to a two-way non-rebreathing valve (model 2630, Hans Rudolph Inc., Kansas City, MO, USA) allowing the subject to breathe in room air while their expired air passed through a 7 l compliant mixing bag that was passively vented back into the room. The end-tidal partial pressure of carbon dioxide (PET,CO2) was determined using an anaesthetic gas monitor (Type 1304, Bruel and Kjaer, Naerum, Denmark) sampling gas from a port on the proximal end of the turbine. The mixed expired partial pressures of oxygen and carbon dioxide (PME,O2 and PME,CO2) were measured using gas analysers (models CD-3 A and S-3 A/1, respectively, Applied Electrochemistry, Pittsburg, PA, USA) sampling gas from within the mixing bag. Heart rate (fC) was measured using a pulse oximeter (model NPB-290, Nellcor Puritan Bennett Inc., Pleasanton, CA, USA).
The analog output from all monitoring devices was fed through a pulse code modulation recording adapter (model 4000 A, A. R. Vetter Co., Rebersburg, USA) for archiving data on VHS tape (JVC Hi-Fi Stereo VCR, model HR-D840U 500C, JVC Americas Corp., USA). Analog signals were directed in parallel to a 16-bit data acquisition card (DAQCard-AI-16XE-50, National Instruments, Austin, TX, USA) in the data acquisition computer (Inspiron 8100, Dell, USA). The data acquisition software was custom designed (LabVIEW 6.1, National Instruments, source code available on request). Signals were displayed continuously at a sampling rate of 20 Hz. Data were analysed and recorded on a breath-by-breath basis for ventilation, tidal volume and breathing frequency (
, VT and fB, respectively) and written to a file for further analysis. An exception to this breath-by-breath analysis was the collection of metabolic gas exchange data, which was performed by the software, based upon the average mixed-expired values for every 4 l of expired air to calculate oxygen uptake and carbon dioxide production (
and 
, respectively).
Data analysis
The breath-by-breath data collected during the experiment were analysed with specially written software (LabVIEW 6.1, National Instruments) that calculated a best-fit line for the data over each of the three discrete intervals of the test: (1) rest; (2) exercise; and (3) recovery. From these line equations, data points were then calculated for times corresponding to the start of the phase, and each 15 s thereafter, up to and including the 3 min mark (i.e. 180 s) for that interval. Data points were determined along the regression lines at times 0, 15, 30, 45 ... 180 s for the rest interval, at times 180, 195, 210 ... 360 s for the exercise interval, and at times 360, 375, 390 ... 540 s for the recovery interval.
To determine whether our method of altering wakefulness drive to breathe was effective, we compared resting values of 
, VT, fB, PET,CO2, fC, 
and 
between the two conditions (HW versus LW). Subjects were self-matched for comparison, and so all statistical testing involved repeated measures analysis. We used one-way repeated measures analysis of variance (RM-ANOVA) testing and Bonferroni post hoc analysis to test for any significant effects of the background cognitive state upon the resting measures. Tests were conducted using an a priori level of significance set at 0.05.
To examine the behaviour of the observed parameters during exercise in the two background conditions, we used two-way RM-ANOVA, again with Bonferroni post hoc testing. The two factors considered were condition (LW and HW) and time (rest, exercise start, exercise end and recovery start). Again, all analyses were performed using an a priori level of significance set at 0.05. Significant changes in 
, VT, fB and fC at the onset and cessation of exercise were interpreted to be an index of the fast exercise drive provided by the combined neural mechanisms of central command and afferent feedback. An interaction effect was interpreted to mean that the wakefulness condition affected the change in these ventilatory drive mechanisms at exercise transitions. PET,CO2, 
and 
were analysed in the same manner, to compare rest and ‘steady-state’ exercise in both LW and HW conditions.
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Results |
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Average 
values for all subjects in both HW and LW conditions at the four points of interest in the protocol are shown in Table 1. Mean 
at rest was higher (P < 0.001) during HW (12.38 ± 0.55 l min–1) than during LW (10.12 ± 0.51 l min–1); all subjects demonstrated greater 
at rest during HW compared to LW. There was an interaction effect between the factors of time and wakefulness condition present (P < 0.001); background wakefulness condition affected the size of the fast changes in 
elicited by active exercise. The mean fast changes in 
at the start and end of exercise during LW were 6.16 ± 1.12 (P < 0.001) and –4.53 ± 1.80 l min–1 (P < 0.001), respectively (see Figs 3A and 4A). During HW, these same fast changes in 
failed to reach significance (P= 0.170 and 0.174). Ventilation achieved at the start of exercise in absolute terms was also lower in the HW condition (14.6 ± 1.1 l min–1 in HW versus 16.3 ± 1.3 l min–1 in LW, P= 0.047). Despite differences in the rapid ventilatory response to exercise between LW and HW conditions, steady-state ventilation was not different (P= 0.401).
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Average fB for all subjects during both HW and LW at the four times of interest in the protocol are shown in Table 1. fB at rest during HW (17.1 ± 0.93 breaths min–1) was significantly higher (P < 0.001) than during LW (13.6 ± 0.59 breaths min–1). Both time (P < 0.001) and wakefulness condition (P= 0.013) were found to be significant factors in determining fB. There was also an interaction effect between these two factors (P= 0.043; see Figs 3B and 4B). The increase in fB at the start of exercise was significant during both LW (5.5 ± 1.07 breaths min–1, P < 0.001) and HW (2.9 ± 0.94 breaths min–1, P= 0.015), and significantly larger during LW (P= 0.015). The fast decrease in fB at the end of exercise was also significant during LW (–4.2 ± 1.02 breaths min–1, P < 0.001) and HW (–3.4 ± 0.73 breaths min–1, P= 0.003), but these decreases were not significantly different between wakefulness conditions (P= 0.399).
Tidal volume
The average values for VT across all subjects during both HW and LW at the four times of interest in the protocol are shown in Table 1. There were no apparent differences in resting VT between LW (0.76 ± 0.04) and HW (0.73 ± 0.04), P= 0.469. While time was found to be a significant factor (P < 0.001), wakefulness condition was not (P= 0.146), and no interaction effect was found (P= 0.610; see Figs 3C and 4C).
Heart rate
Average fC for all subjects during both HW and LW conditions at the four times of interest in the protocol are shown in Table 1. Resting fC was significantly higher (P= 0.016) during HW (73.7 ± 2.5 beats min–1) than during LW (69.8 ± 2.3 beats min–1). There was a significant effect of time (P < 0.001), but wakefulness condition exerted no independent effect (P= 0.133), and there was lack of significant interaction (P= 0.467).
End-tidal carbon dioxide tensions
The behaviour of PET,CO2 is illustrated in Fig. 3D. Resting PET,CO2 was found to be significantly lower (P= 0.003) during HW (37.6 ± 0.94 mmHg) than during LW (39.4 ± 1.02 mmHg). There was a significant effect of time (P= 0.002), with PET,CO2 being 2.0 mmHg higher on average after 3 min of exercise than it was at rest, independent of wakefulness condition. Wakefulness condition also exerted a significant independent effect (P= 0.002), with PET,CO2 being 1.7 mmHg lower on average in the HW condition. There was no significant interaction (P= 0.581) between time and wakefulness condition.
Metabolic gas exchange
Metabolic gas exchange data are summarized in Fig. 5. At rest, no significant difference was found for 
between LW and HW conditions (P= 0.071). However, mean resting 
was found to be slightly higher (P= 0.045) during HW (0.32 ± 0.01 l min–1) than during LW (0.29 ± 0.02 l min–1). Exercise caused a significant increase in both 
and 
(P < 0.001), and there was a significant interaction effect between wakefulness condition and time for both 
and 
(P < 0.001 and P= 0.006, respectively). At the end of 3 min of active exercise, 
was significantly higher in LW than HW (P= 0.017), and the same result was found for 
(P= 0.010).
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There was no effect of condition (i.e. LW versus HW) upon leg movement frequency (fLM, P= 0.874). The only observed change in leg movement frequency was a slight reduction that occurred over the 3 min of exercise (P < 0.001). This was a combined effect, observed in both conditions. Indeed, across the exercise interval in both conditions, leg movement frequency was nearly identical. The average fLM at the onset of exercise was 74.0 ± 0.6 s–1 per leg during LW and 74.0 ± 0.9 s–1 per leg during HW. By the end of the 3 min of exercise, movement frequency was 71.0 ± 1.0 s–1 per leg during LW and 71.1 ± 1.2 s–1 per leg during HW.
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Discussion |
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At rest, the HW condition produced a change in respiratory control such that subjects had increased ventilation due to an elevated breathing frequency. Heart rate was also significantly higher at rest in HW, and there was a small but significant increase in carbon dioxide elimination. The onset of leg extension exercise caused a rapid increase in ventilation and its components of breathing frequency and tidal volume, with the fast increases in ventilation and breathing frequency, but not tidal volume, larger in LW than in HW. There was also a rapid increase in heart rate at the onset of exercise, but no evidence for an effect of wakefulness condition on this increase. By the end of 3 min of active exercise there was no difference in either ventilation or breathing frequency between the HW and LW conditions, but both oxygen consumption and carbon dioxide elimination were significantly higher in LW. Exercise leg movement frequency was not different during LW and HW.
The cognitive task
We used a puzzle, the Tower of Hanoi, to increase wakefulness during the HW condition. We have previously used this puzzle to provide a cognitive task (Bell & Duffin, 2004) and found a similar effect upon respiratory control at rest; ventilation was augmented at rest because of an increase in breathing frequency. While this is not a novel finding (Rigg et al. 1977; Bechbache et al. 1979; Shea et al. 1988; Chin et al. 1996), this observation does provide support for our contention that wakefulness was increased by the cognitive task. We also found that while solving the puzzle at rest subjects had a higher fc (by 5 beats min–1), in agreement with other studies (Rousselle et al. 1995; Wasmund et al. 2002). The higher resting ventilation might have been due to an increased metabolism, since resting 
was higher in HW; it would be expected that increased mental activity and increased respiratory muscle activity would elevate resting 
. However, PET,CO2 at rest was significantly lower in HW, and this suggests that there was ventilation in excess of metabolic demand. We suggest that the higher 
(0.03 l min–1) probably resulted from the washout of CO2 from body stores, as a result of the increased ventilation in HW. We therefore attribute the increased resting ventilation in HW to a wakefulness drive to breathe increased by the cognitive task.
Interaction between exercise and wakefulness
The onset of exercise caused a rapid increase in 
, fB and VT in both conditions, but the increase in 
and fB was smaller in HW; an observation made in nine of the ten subjects tested. The absolute ventilation achieved at the first point of exercise was also smaller in the HW condition; an observation made in seven of ten subjects. This is a novel finding, but receives corroborative support from previous studies indicating that mental activity reduces the physiological response to exercise (Rousselle et al. 1995; Wasmund et al. 2002). Despite the differences in the phase-one exercise ventilatory responses, by the end of 3 min of exercise there were no differences in 
, fB and VT between LW and HW conditions. However, both 
and 
were slightly larger in LW than in HW, and we suggest that this difference can be attributed to the smaller body stores of CO2 present at the onset of exercise in HW because of the increased resting ventilation. PET,CO2 remained higher at the end of 3 min of exercise in LW than in HW (41.3 ± 1.3 versus 39.8 ± 1.1 mmHg), although this difference was not statistically significant. Since 
after 3 min of exercise was the same in LW and HW, the larger CO2 stores in LW led to the differences in 
and 
that we observed.
Mechanism of interaction
PET,CO2 was lower in HW at rest, and so it is possible that this mild hypocapnia could have attenuated the initial increase in ventilation at the onset of exercise. Indeed, such an effect is supported by the data of Ward et al. (1983). In their study, a 9 min voluntary hyperventilation was used to reduce PET,CO2 towards the range of 25 mmHg prior to exercise. However, this effect has not been observed in mild to moderate hypocapnia. When exercise is started abruptly in a background of mild hypocapnia, ventilatory changes are the same as when observed in the normocapnic range (Dejours et al. 1960; Lefrancois & Dejours, 1964; Casey et al. 1987; McConnell & Gardener, 1996). Granted, there may be some threshold between normocapnia and more ‘severe’ (< 25 mmHg) hypocapnia, below which there is an effect of CO2 stores upon ventilatory control at the onset of exercise. In fact, PET,CO2 during the high wakefulness condition at rest, though lower than in the low wakefulness condition at rest, remained in the lower normocapnic range (37.6 mmHg). It is therefore unlikely that the difference we observed was due to differences in background PET,CO2.
In one study, posture was shown to affect the initial ventilatory response to exercise (Weiler-Ravell et al. 1983). During cycling exercise performed in the supine position, the initial increase in ventilation was markedly attenuated compared to exercise performed in the upright position. The authors speculated that this effect was related to a reduction in cardiac output in the supine condition. In our study, posture was the same in both conditions and heart rate changes (as an index of cardiac output) were not significantly different at exercise onset between LW and HW conditions. Therefore, any mechanistic link between observations by Weiler-Ravell et al. (1983) and ours remains unclear.
Our results indicate that the amplitude of the change in ventilation at the onset of exercise was smaller in the high wakefulness condition, and the absolute ventilation achieved at the onset of exercise was also reduced in the high wakefulness condition (14.6 ± 1.1 l min–1 in HW versus 16.3 ± 1.3 l min–1 in LW, P= 0.047, observed in 7 out of 10 subjects). Had the absolute ventilation achieved at the very start of exercise been the same in the HW and LW conditions, it could be argued that the change in ventilation was smaller at exercise onset in the HW condition only because resting ventilation was higher, and so the respiratory controller needed to make a smaller adjustment to match ventilation to CO2 production in the tissues during exercise.
It has been suggested that the flow of CO2 from the tissues to the lung and heart regulates ventilation during exercise (Wasserman et al. 1977). Since workload during exercise in the HW and LW conditions was the same, such a mechanism coupling ventilation to CO2 production would indeed predict equivalent absolute ventilation at the start of exercise regardless of resting ventilation. Though the precise nature of a mechanism linking ventilation to CO2 production remains to be established, this possibility must be considered in respiratory control. Evidence that implicates a link between ventilation and the status of the vasculature provides one such possibility (Haouzi et al. 2004). Given the differences in both the change in ventilation and the absolute ventilation at the onset of exercise between the conditions, we can say with reasonable certainty that during the performance of a cognitive task the initial ventilatory response to exercise was blunted.
One interpretation of our results is that increased arousal interacts with the fast neural drives to breathe believed to be concurrently activated at the start of exercise, such that they are effectively suppressed. Support for this interpretation comes from previous studies, where we found that a cognitive task reduced the respiratory response to passive limb movement that activated afferent feedback (Bell & Duffin, 2004), and others found that the fast ventilatory response to passive limb movement tended towards being greater during sleep than while awake (Ishida et al. 1993). However, both putative mechanisms related to afferent feedback and central motor command were presumed to be concurrently activated in the present study and it is not possible to attribute the effect we observed to either mechanism specifically.
In both this and our previous study (Bell & Duffin, 2004), the rapid increase in ventilation at the onset of movement or exercise while solving the puzzle were non-significant. Therefore, comparison of the magnitude of these changes between the two studies would, strictly speaking, not be statistically valid. Nonetheless, an examination of the fast increase in ventilation at the onset of passive movement shows that that the cognitive task suppressed the increase to 19% of that observed in the control condition (Bell & Duffin, 2004). In the present study, the fast change in ventilation at the onset of active exercise during the cognitive task was suppressed to 37% of that observed in the control situation. Ignoring the fact that there were non-significant increases while solving the puzzle, one might suggest that the fast increase in ventilation at the onset of active exercise was not as effectively suppressed as it was during passive movement. This further suggests that central motor command, or some other fast onset drive to breathe related to the exercise, is not appreciably affected by the level of background wakefulness.
Differences in the efficacy of cognitive activity to suppress afferent feedback versus other rapid onset neural drives to breathe provide an interesting topic for future investigation; however, we need to keep in mind that in this case we are comparing non-significant changes, and any such interpretation is therefore problematic.
If the central neural arousal related to cognitive processes actively suppresses rapid-onset feedback and/or feedforward exercise drives to breathe, it may act at a level where central motor command and afferent feedback are believed to interact and form an integrated fast neural drive to breathe (Waldrop et al. 1986; Richard et al. 1989; Degtyarenko & Kaufman, 2000); several brain regions have been suggested in this regard (Craig, 1995; Sequeira et al. 2000; Nattie, 2001; Potts, 2001; Shintani et al. 2003).
Limitations
Our study design cannot provide a description of the mechanisms involved in the interaction of wakefulness and fast exercise drives to breathe; we made no measures of cortical activity and so cannot say what brain regions were activated by the cognitive task. Nor can we specify whether wakefulness interacts with central motor command, afferent feedback or both. Throughout the past century many potential drives to breathe at the onset of physical activity have been identified, but the fact remains that little is known about their interaction or their efficacy within the integrated central nervous system. Our use of mixed expired CO2 and O2 to calculate gas exchange data over a period corresponding to the collection of 4 l of expired breath means that we could not measure breath-by-breath gas exchange and examine the transient responses. Therefore, we cannot say whether there were differences in the initial oxygen uptake and/or carbon dioxide production kinetics at the start of exercise in the two conditions.
Significance
If wakefulness or arousal does suppress drives to breathe from other neural sources during exercise, what would be the purpose? If the increased wakefulness or arousal related to exercise is able to abruptly drive breathing and yield an initial ventilatory response, then perhaps a suppression of other neural mechanisms prevents superfluous respiratory stimulation from those sources. The behaviour of performing exercise may have evolved to include the act of increasing breathing. Fink et al. (1995) demonstrated that the superolateral primary motor cortex in areas known to be associated with volitional breathing is active both during and while recovering from exercise. Jack et al. (2003, 2004) have studied patients with idiopathic hyperventilation. This poorly understood condition involves chronically elevated ventilation with reduced body CO2 stores accompanied by full metabolic compensation. These patients have been shown to hyperventilate even during exercise (Jack et al. 2003, 2004). Since this disorder may have behavioural (psychological) origins (Jack et al. 2003), it suggests that a pathology in the behavioural component of the control of breathing leads to an inappropriate respiratory response to exercise.
We believe that exercise represents a state of increased neural arousal in the integrated human system, and therefore rapidly augments the drive to breathe from wakefulness. Our present observation that the increase in ventilation at the start of exercise is decreased by a cognitive task may be related to the concept of division of attention used in the psychology of behaviour and cognitive processing (Hopfinger et al. 2001). The increase in ventilation at the start of exercise that normally results from an increased arousal/wakefulness can be blunted by a cognitive task that diverts conscious attention away from the exercise task. If, as we speculate, wakefulness also has an inhibitory influence over exercise-related feedforward and/or feedback drives to breathe, then those putative drives should be rendered ineffective. Thus, our intervention of a cognitive task may have diverted attention away from the exercise task, altering the behavioural response that is perhaps important to the initial respiratory response to exercise. We hope that these speculations regarding the nature of the interaction we observed and the significance of behavioural state will stimulate research that will aid in our understanding of the stimulus to breathe at the onset of exercise in humans.
Conclusion
In humans, a background cognitive task decreases the fast exercise drive to breathe, expressed as either the rapid change in ventilation or the absolute level of ventilation achieved, at exercise onset. This observation suggests there may be an important role for mechanisms related to behaviour in the control of breathing during exercise, in particular during the initial transient phase of the response. There was a trend towards the cognitive task providing less potent suppression over the initial ventilatory response to active exercise compared to that during passive movement, as we previously demonstrated (Bell & Duffin, 2004). Rapid onset drives to breathe related to the motor act and/or metabolic components of exercise may be more robust to suppression from wakefulness. Further experiments will be required to determine the nature and presence of such an effect.
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References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Bell
HJ
&
Duffin
J (2003). CO2 does not affect passive exercise ventilatory decline. J Appl Physiol
95, 322–329.
Bell
HJ
&
Duffin
J (2004). The respiratory response to passive limb movement is suppressed by a cognitive task. J Appl Physiol
97, 2112–2120.
Bell HJ, Ramsaroop DM & Duffin J (2003). The respiratory effects of two modes of passive exercise. Eur J Appl Physiol 88, 544–552.[Medline]
Casey
K, Duffin
J
&
McAvoy
GV (1987). The effect of exercise on the central-chemoreceptor threshold in man. J Physiol
383, 9–18.
Chin
K, Ohi
M, Fukui
M, Kita
H, Tsuboi
T, Noguchi
T
et al. (1996). Inhibitory effect of an intellectual task on breathing after voluntary hyperventilation. J Appl Physiol
81, 1379–1387.
Craig AD (1995). Distribution of brainstem projections from spinal lamina I neurons in the cat and the monkey. J Comp Neurol 361, 225–248.[CrossRef][Medline]
Degtyarenko AM & Kaufman MP (2000). Fictive locomotion and scratching inhibit dorsal horn neurons receiving thin fiber afferent input. Am J Physiol 279, R394–R403.
Dejours P, Lefrancois R, Flandrois R & Teillac A (1960). Autonomie des stimulus ventilatoires oxygene, gaz carbonique et neurogenique de l'exerice musculaire. J Physiol (Paris) 52, 63.[Medline]
Eldridge FL (1994). Central integration of mechanisms in exercise hyperpnea. Med Sci Sports Exerc 26, 319–327.[Medline]
Fink GR, Adams L, Watson JD, Innes JA, Wuyam B, Kobayashi I et al. (1995). Hyperpnoea during and immediately after exercise in man: evidence of motor cortical involvement. J Physiol 489, 663–675.[Medline]
Haouzi
P, Chenuel
B
&
Huszczuk
A (2004). Sensing vascular distension in skeletal muscle by slow conducting afferent fibers: neurophysiological basis and implication for respiratory control. J Appl Physiol
96, 407–418. 10.1152/japplphysiol.00597.2003
Hopfinger JB, Woldorff MG, Fletcher EM & Mangun GR (2001). Dissociating top-down attentional control from selective perception and action. Neuropsychologia 39, 1277–1291. 10.1016/S0028-3932(01)00117-8[CrossRef][Medline]
Ishida K, Yasuda Y & Miyamura M (1993). Cardiorespiratory response at the onset of passive leg movements during sleep in humans. Eur J Appl Physiol 66, 507–513. 10.1007/BF00634300[CrossRef]
Jack
S, Rossiter
HB, Pearson
MG, Ward
SA, Warburton
CJ
&
Whipp
BJ (2004). Ventilatory responses to inhaled carbon dioxide, hypoxia, and exercise in idiopathic hyperventilation. Am J Respir Crit Care Med
170, 118–125. 10.1164/rccm.200207-720OC
Jack S, Rossiter HB, Warburton CJ & Whipp BJ (2003). Behavioral influences and physiological indices of ventilatory control in subjects with idiopathic hyperventilation. Behav Modif 27, 637–652. 10.1177/0145445503256318[Abstract]
Kaufman MP & Forster HV (1996). Reflexes controlling circulatory, ventilatory and airway responses to exercise. In Handbook of Physiology, section 12, chap. 10, Exercise, ed. Rowell LB & Shepherd JT, pp. 381–447. Oxford University Press, Oxford.
Lefrancois R & Dejours P (1964). Etude des relation entre stimulus ventilatoire gaz carbonique et stimulus ventilatoire neurogenique de l'exercice musculaire chez l'homme. Rev Franc Etud Clin Biol 9, 498.
Matell G (1963). Time-courses of changes in ventilation and arterial gas tensions in man induced by moderate exercise. Acta Physiol Scand 58, 1–53.
McConnell A & Gardener WN (1996). The ventilatory response to moderate hypocapnic exercise in human beings. Respir Physiol 103, 147–156. 10.1016/0034-5687(95)00087-9[CrossRef][Medline]
Nattie EE (2001). Central chemosensitivity, sleep, and wakefulness. Respir Physiol 129, 257–268. 10.1016/S0034-5687(01)00295-X[CrossRef][Medline]
Potts
JT (2001). Exercise and sensory integration. Role of the nucleus tractus solitarius. Ann N Y Acad Sci
940, 221–236.
Richard CA, Waldrop TG, Bauer RM, Mitchell JH & Stremel RW (1989). The nucleus reticularis gigantocellularis modulates the cardiopulmonary responses to central and peripheral drives related to exercise. Brain Res 482, 49–56. 10.1016/0006-8993(89)90541-6[CrossRef][Medline]
Rigg JR, Inman EM, Saunders NA, Leeder SR & Jones NL (1977). Interaction of mental factors with hypercapnic ventilatory drive in man. Clin Sci Mol Med 52, 269–275.[Medline]
Rousselle JG, Blascovich J & Kelsey RM (1995). Cardiorespiratory response under combined psychological and exercise stress. Int J Psychophysiol 20, 49–58. 10.1016/0167-8760(95)00026-O[CrossRef][Medline]
Sequeira H, Viltart O, Ba-M'Hamed S & Poulain P (2000). Cortical control of somato-cardiovascular integration: neuroanatomical studies. Brain Res Bull 53, 87–93. 10.1016/S0361-9230(00)00312-9[CrossRef][Medline]
Shea SA (1996). Behavioural and arousal-related influences on breathing in humans. Exp Physiol 81, 1–26.[Abstract]
Shea SA, Murphy K, Hamilton L, Benchetrit G & Guz A (1988). Do changes in respiratory pattern and ventilation seen with different behavioural situations reflect metabolic demands? In Wenner-Green International Symposium Series, vol. 50, ed. Von Euler C & Katz-Salamon M, pp. 21–28. MacMillan Press, Basingstoke, UK.
Shintani T, Mori RL & Yates BJ (2003). Locations of neurons with respiratory-related activity in the ferret brainstem. Brain Res 974, 236–242. 10.1016/S0006-8993(03)02592-7[CrossRef][Medline]
Thornton
JM, Guz
A, Murphy
K, Griffith
AR, Pedersen
DL, Kardos
A
et al. (2001). Identification of higher brain centres that may encode the cardiorespiratory response to exercise in humans. J Physiol
533, 823–836. 10.1111/j.1469-7793.2001.00823.x
Waldrop TG, Mullins DC & Millhorn DE (1986). Control of respiration by the hypothalamus and by feedback from contracting muscles in cats. Respir Physiol 64, 317–328. 10.1016/0034-5687(86)90125-8[CrossRef][Medline]
Ward SA (2000). Control of the exercise hyperpnoea in humans: a modeling perspective. Respir Physiol 122, 149–166. 10.1016/S0034-5687(00)00156-0[CrossRef][Medline]
Ward
SA, Whipp
BJ, Koyal
S
&
Wasserman
K (1983). Influence of body CO2 stores on ventilatory dynamics during exercise. J Appl Physiol
55, 742–749.
Wasmund
WL, Westerholm
EC, Watenpaugh
DE, Wasmund
SL
&
Smith
ML (2002). Interactive effects of mental and physical stress on cardiovascular control. J Appl Physiol
92, 1828–1834.
Wasserman K, Whipp BJ, Casaburi R & Beaver WL (1977). Carbon dioxide flow and exercise hyperpnea. Cause and effect. Am Rev Respir Dis 115, 225–237.[Medline]
Weiler-Ravell
D, Cooper
DM, Whipp
BJ
&
Wasserman
K (1983). Control of breathing at the start of exercise as influenced by posture. J Appl Physiol
55, 1460–1466.
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) and HW (•) averaged across all subjects 
