|
NO INFLUENCE OF HYPOXIA ON COORDINATION BETWEEN RESPIRATORY AND
LOCOMOTOR RHYTHMS DURING ROWING AT MODERATE INTENSITY
|
1Laboratoire des Sciences du Sport, Besançon, France
2EA 2991 Efficience et Déficience Motrices, UFR STAPS, Montpellier, France
3Laboratoire d'Analyse de la Performance Sportive, Université de Pau, Département
STAPS, Tarbes, France.
| Received |
|
02 August 2007 |
| Accepted |
|
20
September 2007 |
| Published |
|
01
December 2007 |
©
Journal of Sports Science and Medicine (2007) 6, 526- 531
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| ABSTRACT |
| Besides neuro-mechanical constraints, chemical or metabolic stimuli
have also been proposed to interfere with the coordination between
respiratory and locomotor rhythms. In the light of the conflicting
data observed in the literature, this study aimed to assess whether
acute hypoxia modifies the degree of coordination between respiratory
and locomotor rhythms during rowing exercises in order to investigate
competitive interactions between neuro-mechanical (movement) and chemical
(hypoxia) respiratory drives. Nine male healthy subjects performed
one submaximal 6-min rowing exercise on a rowing ergometer in both
normoxia (altitude: 304 m) and acute hypoxia (altitude: 2877 m). The
exercise intensity was about 40 % and 35 % (for normoxia and hypoxia
conditions, respectively) of the individual maximal power output measured
during an incremental rowing test to volitional exhaustion carried
out in normoxia. Metabolic rate and minute ventilation were continuously
collected throughout exercise. Locomotor movement and breathing rhythms
were continuously recorded and synchronized cycle-by-cycle. The degree
of coordination was expressed as a percentage of breaths starting
during the same phase of the locomotor cycle. For a same and a constant
metabolic rate, acute hypoxia did not influence significantly the
degree of coordination (mean ± SEM, normoxia: 20.0 ± 6.2 %, hypoxia:
21.3 ± 11.1 %, p > 0.05) while ventilation and breathing frequency
were significantly greater in hypoxia. Our results may suggest that
during rowing exercise at a moderate metabolic load, neuro-mechanical
locomotion-linked respiratory stimuli appear "stronger"
than peripheral chemoreceptors- linked respiratory stimuli induced
by hypoxia, in the context of our study.
KEY
WORDS: Control
of breathing, locomotor-respiratory coupling, neuro-mechanical entrainment,
chemical drive.
|
| INTRODUCTION |
|
Interactions between locomotion and ventilation have now been
studied in several species of mammals, from a variety of perspectives.
Among the mechanisms for this interaction are neural and mechanical
interactions of separate controllers. Viala and Freton, 1983
and Viala, 1986
observed that direct central (subcortical and spinal areas) interactions
do exist between the respiratory and the locomotor rhythms in decorticate
rabbits. Iscoe and Polosa, 1976
showed entrainment of the respiratory rate by repetitive somatic
afferent stimulation of the hamstring nerve in cats. Moreover, in
instrumented dogs and horses, Ainsworth et al., 1997
provided evidence that the exercise hyperpnea is neurally mediated.
Further, it is now well established that locomotion entrains breathing
rhythm, that is that the locomotor cycle contributes to the respiratory
flow (Bernasconi et al., 1995;
Bramble and Carrier, 1983;
Hill et al., 1988;
Rassler and Kohl, 1996)
by mechanical linkage mechanisms. Locomotor muscles can cause airflow
by acting directly on the chest wall (diaphragm, rib cage) or by
generating inertial forces that accelerate tissue masses.
Interactions between rhythmic locomotor and respiratory patterns
may lead to coordination, which can occur as an integer ratio of
both frequencies and as a significant coincidence of certain phases
of both cycles. When the nature of the locomotion involves a greater
role for the forelimbs in humans as well as spinal flexion and extension,
as occurs during rowing, then an entrainment of ventilation is reported
to occur at integral multiples of stroke rate (1:1, 2:1 or 3:1).
In rowing, periodic contraction of muscles and movement elevate
pleural pressure (Siegmund et al., 1999).
Also the increased intra-abdominal pressure impairs ventilation
(VE) at stroke catch (Cunningham et al., 1975)
or stroke finish (Siegmund et al., 1999).
Furthermore, during the drive phase the knees and hips extend and
VE is assisted (Siegmund et al., 1999).
In rowing, entrainment with various frequency ratios of 1:1, 2:1
or 3:1 (Maclennan et al., 1994;
Mahler et al., 1991;
Siegmund et al., 1999)
appears to lead adequate VE (Siegmund et al., 1999).
Besides neuro-mechanical constraints, chemical or metabolic stimuli
have also been proposed to interfere with coordination between respiratory
and locomotor rhythms (Paterson et al., 1987).
For instance, an increase in chemical drive to breathe can occur
under hypoxic conditions. To date, two independent studies (Paterson
et al., 1987;
Seebauer et al., 2003b)
have tested the hypothesis that entrainment of breathing frequency
(Bf) by exercise rhythm may be affected during conditions of an
enhanced peripheral chemoreceptor activity in hypoxia. However,
these two studies showed opposite findings. In running, Paterson
et al., 1987
observed a decrease in degree of coordination with increasing hypoxia
but more recently Seebauer et al., 2003b
observed no influence of hypoxia on coordination between breathing
and cycling rhythms. Paterson et al., 1987
discussed their results in terms of an increased Bf in hypoxia beyond
the fundamental frequencies that were locked to exercise rhythm
in normoxia. It would seem that increased peripheral chemoreceptor
activity during exercise in hypoxia decreases the degree of coordination
as a consequence of hypoxic-induced increases in VE (as seen in
Bf), suggesting that the respiratory system is possibly no longer
optimized.
Rowing presents a well established respiratory entrainment by limb
movements during normoxia due to neuro-mechanical interactions especially
with active upper-body limbs (Cunningham et al., 1975;
Maclennan et al., 1994;
Mahler et al., 1991;
Siegmund et al., 1999).
Considering the two previous contradictory findings of Paterson
et al., 1987
and Seebauer et al., 2003b,
we were interested to study whether chemical and neuro-mechanical
respiratory drives competitively interact during submaximal rowing
exercise. Therefore, the present study aimed to assess whether acute
hypoxia (chemical respiratory drive) modifies the degree of coordination
between respiratory and locomotor rhythms during rowing exercise.
| METHODS |
|
Subjects
Nine male healthy students (age 25 ± 1.0 years, height 1.77
± 0.02 m, and body weight 78.0 ± 3.6 kg) volunteered to participate
to this study. Participants were not specialists in rowing
activity but were regularly accustomed to rowing during the
last three months before the testing period, twice a week.
They were asked to refrain from ingesting caffeine and/or
alcohol for at least 12 hours prior to testing. They were
asked to eat a light meal 2 hours before testing. All participants
were blind to the purpose of the experiment. The study protocol
complies with the Helsinki declaration for human experimentation
and was approved by the local Ethics Committee. Possible risks
and benefits were explained and written informed consent was
obtained from each subject prior to all testing.
Environmental
conditions
Tests under normoxic conditions were undertaken at an altitude
of 304 m and tests under hypoxic conditions were realized
at an altitude of 2877 m (laboratory of the Pic du Midi de
Bigorre, observatory, France). Subjects were transported by
a cable-car and were tested immediately after their arrival.
So, they were acutely exposed to hypoxia in order to induce
marked alterations in Bf during exercise.
Determination
of working intensity
Each subject underwent an incremental rowing test to volitional
exhaustion on a rowing ergometer (Concept II, Morrisville,
Vermont, USA) in normoxic conditions. The initial power output
was set at 50 W, and each minute, the target intensity was
increased by 25 W. Each subject continued to exercise until
exhaustion or the inability to maintain the target level of
power output. From this incremental test, a submaximal intensity
corresponding to ~ 40 % of the individual maximal power output
in normoxia was determined, that is with a negligible contribution
of the anaerobic metabolism in total energy expenditure and
allowing a large degree of freedom in the breathing regulation
(Seebauer et al., 2003b).
Due to the decrease in aerobic power output with the increase
in altitude (Fulco et al., 1998),
the submaximal intensity in hypoxia was adjusted in order
to obtain the same metabolic rate (i.e., VO2) than
during normoxic conditions. A decrease of about 13 % of the
submaximal exercise power output in normoxia was necessary
to reach the same absolute VO2 in both normoxia
and hypoxia (that is for an equivalent absolute submaximal
metabolic load).
Experimental
protocol
During a second visit, subjects were asked to perform one
submaximal 6-min rowing exercise in normoxia, and on a separate
day, the same submaximal test with an adjusted exercise intensity
(see above) was carried out in hypoxia. These tests were randomized.
Mechanical
measurements
Upper-body movements were recorded with a custom-made load
cell inserted between the ergometer handle and chain, and
connected to a dedicated acquisition system (MP30, Biopac
Systems Inc., Santa Barbara, CA, USA). Then, stroke rate (SR)
values were calculated off-line.
Physiological
measurements
Values of VE, tidal volume (VT) and VO2 were continuously
determined breath-by-breath during all exercise testing (Cosmed
K4b², Rome, Italy). Gas analyzers were calibrated before each
test with ambient air (O2: 20.93 % and CO2:
0.03 %) and a gas mixture of known composition (O2:
16.00 % and CO2: 5.00 %). An O2 analyzer
with a polarographic electrode and a CO2 analyzer
with an infrared electrode sampled expired gases at the mouth.
The facemask, that had a low dead space (70 mL) was equipped
with a low-resistance, bidirectional digital turbine (28 mm
diameter). This turbine was calibrated before each test with
a 3 L syringe (Hans Rudolph Inc., Dallas, USA). Face masks
allowed subjects to simultaneously breath with mouth and nose,
for more comfort. It has been demonstrated that the use of
a mouthpiece and nose clip may affect VT, VE, inspiratory
flow and respiratory frequency (Weissman et al., 1984).
Heart rate (HR) was continuously measured via a wireless Polar-monitoring
system (Polar Electro Oy, Kempele, Finland), and mean HR over
each breath was recorded.
Breathing frequency (Bf) was recorded using a thermocouple
sensor (SS6L Temperature Transducer BSL, Biopac Systems Inc,
Santa Barbara, USA) which determines nasal airflow by detecting
the difference in air temperature. The temperature transducer
was attached just under the nostril of the subject and connected
to the Biopac MP100 acquisition unit. The respiratory flow
and upper-body movement signals were continuously recorded
and synchronized at 200 Hz during all exercises.
Data
analysis
All values were recorded during metabolic steady state (after
the initial 2 min of each constant-load submaximal exercise)
and averaged during the last 4 min. Given the various inputs
that may influence the central nervous system pattern generators
for breathing and rowing, some cycle-to-cycle variability
in the "tightness" of rhythm coordination is to
be expected during entrainment. The onset
of the movement cycle and that of the expiration phase were
determined cycle-by-cycle during the last 4 min of all submaximal
exercise tests (Figure 1).
Then, to estimate the degree of coordination, we used the
rigorous method proposed by Seebauer et al., 2003a.
We determined the time between the peak force during stroke
and the onset of expiration during each cycle; this time is
called phase interval. When the phase interval value is maintained
constant ± 0. 0725 sec for at least four consecutive breaths,
coordination is considered to be present (Hill et al., 1988).
The degree of coordination (%) corresponded to the percentage
of breaths meeting this criteria compared with the total number
of breaths recorded in the last 4 min of the respective test.
This method takes into account the natural variability in
coordination precision and is sensitive to changing patterns
of coordination but also addresses the issue of how often
apparent entrainment may arise by chance.
We also determined the mean integer ratio of frequencies (stroke
frequency / breathing frequency) over the last 4 min of all
exercise tests.
Statistical
analysis
Data are reported as means ± SEM. Differences between environmental
conditions (normoxia vs. hypxoxia) were assessed by using
paired t-tests (SigmaStat, V2.03, SPSS Inc., USA). The level
of significance was set at p < 0.05 for all tests.
|
| RESULTS |
|
Mechanical
power values during submaximal and incremental rowing exercises
are given in Table 1. Physiological and mechanical variables during submaximal
exercises are summarized in Table
2.
Ventilatory
and metabolic variables
During the rowing incremental test to volitional exhaustion,
average peak VO2 value was about 53.3 ± 2.8 mL.min-1.kg-1.
During submaximal exercises, VE was significantly increased
with altitude (p < 0.01) due to an increase in Bf (p <
0.01). An increase in HR was also observed with altitude (p
< 0.05). Absolute VO2 values were not significantly
different between normoxia and hypoxia conditions, and corresponded
to 56.6 ± 1.4 % of peak VO2 measured in normoxia.
Mechanical
variable
A significant effect of hypoxia was observed on the SR values:
SR was significantly higher in hypoxia than in normoxia (Table
2, p < 0.05).
Degree
of coordination and mean integer ratio
No effect of hypoxia was observed on the degree of coordination
(p = 0.9) as on the mean integer ratio of both frequencies
(p = 0.1, Table 2). The
average degree of coordination was of 20.0 ± 6.2 % and of
21.3 ± 11.1 % in normoxia and in hypoxia, respectively.
|
| DISCUSSION |
The degree of coordination observed during rowing exercise may
be judged low. However, this value is completely dependent on
the method of determination used. Different methods are proposed
in the analysis of coordination between respiratory and locomotor
rhythms but with variable results. Spectral analysis (MacDonald
et al., 1992),
nonlinear mathematical models like the Farey tree (Gonzalez
and Piro, 1985)
or the HKB model, a dynamical model first developed by Haken,
Kelso and Bunz (Haken et al., 1985),
or the percentage of recorded breaths in one phase of propulsion
(Bernasconi and Kohl, 1993)
have all been used. An integer frequency ratio is characteristic
of coordination. It implies a tight phase locking during consecutive
breaths. The base of any method for detecting coordination is
to establish how often apparent phase locking may arise randomly.
Previous studies suggest that coordination may often be intermittent;
thus a detection method capable of discriminating short- term
rhythm interactions is necessary to establish physiological
interactions between breathing and moving limb patterns. We
chose the method described by Hill et al., 1988,
a rather well-identified method in the literature (Seebauer
et al., 2003a;
2003b)
allowing us to detect coordination even when it occurs sporadically,
with varying coupling patterns, and in a not randomly fashion.
However, since this method imposes strict criteria (see Methods)
for coordination between two rhythms generators, it appears
as a restrictive method and this may explain the low values
of degree of coordination reported (about 20 %) in the present
study and in the literature using the same method (Fabre et
al., 2007;
Seebauer et al., 2003a;
2003b).
The main goal of this study was to assess whether acute hypoxia
modifies the degree of coordination between respiratory and
locomotor rhythms during constant workload rowing exercise in
order to investigate possible competitive interactions between
neuro-mechanical (movement) and chemical (hypoxia) respiratory
drives. The few studies (Paterson et al., 1987;
Seebauer et al., 2003b)
which have investigated this issue gave conflicting results.
Paterson et al., 1987
observed a decrease in degree of coordination during running
with hypoxia whereas Seebauer et al., 2003b
showed no influence of hypoxia on the coordination between breathing
and cycling rhythms at three submaximal workloads. Rowing appears
like a very different form of locomotion than running or cycling.
Upper-body locomotor muscles implicated in rowing are in part
the same as respiratory muscles and are acting directly on the
chest wall (diaphragm, rib cage) in contrast to running or cycling
activities. This type of mechanical links between respiratory
and locomotory systems is further strengthened by the succession
of cramped and extended body positions during rowing (Siegmund
et al., 1999).
Such an activity (with an important contribution of the upper-body
limbs in propulsion) had never been investigated in this way.
When two rhythmic components of a system interact in a way so
that one (locomotor rhythm) imposes its rhythm on the other
(breathing), the first is said to have entrained the other (Bramble
and Carrier, 1983;
Hill et al., 1988;
Rassler and Kohl, 1996;
Seebauer et al., 2003a).
So, coordination is determined by the relationships between
the strength of attraction of the locomotor rhythm and the strength
of the breathing rhythm in maintaining its intrinsic rate. Based
on the control of breathing during exercise involving interactions
between neuro-mechanical and chemical respiratory drives, it
is possible that the hypoxic stimulus would decrease the degree
of coordination between upper-body movement and breathing rhythms
during rowing at a moderate metabolic load. But, our results
suggest that the degree of coordination was not influenced by
the increase in metabolic stimuli induced by the hypoxic-induced
stress although we observed, as expected, a significant increase
in both Bf and VE in hypoxia for a same moderate
metabolic load. Such an increase in Bf has been proposed by
Paterson et al., 1987
as the main responsible factor of the hypoxic-induced decrease
in degree of coordination. But, in the present study and contrary
to Paterson's study (Paterson et al., 1987),
the frequency of the second rhythm involved in the occurrence
of coordination was also significantly affected by hypoxia,
so that the mean integer ratio of both frequencies remained
unchanged and close to a 1:1 coordination pattern whatever the
condition (Table 2). However
the impact of movement rate on the coordination is still a matter
of debate. During rowing and contrary to running (Paterson et
al., 1987),
the respiratory and locomotor rhythms seem to be strongly locked
in order to maintain homeostasis even when hypoxia induces an
increase in chemical respiratory drive. This linkage between
these two rhythms may have permitted to avoid a decrease of
the degree of coordination. Nevertheless, our result is in agreement
with a recent study (Seebauer et al., 2003b)
involving different cycling exercise intensities where the authors
proposed that the effect of hypoxia on the degree of coordination
is in part dependent on the exercise intensity. In fact, Paterson
et al., 1987
chose an exercise intensity at about 40 % of maximal VO2
whereas the lowest intensity used in Seebauer's study (Seebauer
et al., 2003b)
was of 56.1 6.7 % of maximal VO2 and of 56.6 1.4
% of peak VO2 in the present study. According to
Seebauer et al., 2003b,
lower intensities would permit higher degree of freedom in the
breathing regulation and therefore, the breathing rhythm would
be more vulnerable to other stimuli.
In our study, the absolute VO2 was deliberately the
same in normoxia and hypoxia conditions. In the two previous
studies concerning the influence of hypoxia on the degree of
coordination (Paterson et al., 1987;
Seebauer et al., 2003b),
the subjects ran or cycled with the same relative VO2.
So, the absolute VO2 in hypoxia was reduced (e.g.
~15 % in Seebauer et al., 2003b).
The principle in the experimental design of these previous studies
was to increase chemical stimuli with hypoxic condition in order
to perturb the accepted concept of entrainment of the breathing
rhythm by the movement rhythm. However, by reducing absolute
VO2 in hypoxia, the metabolic demand and therefore
the chemical stimuli are equally reduced. So, chemical stimuli
are not necessarily increased by hypoxic conditions when the
absolute VO2 is considerably reduced compared to
normoxic condition. This is the reason why we chose to adjust
the rowing ergometer workload in order to obtain the same absolute
VO2 in hypoxia than in normoxia while keeping submaximal
moderate intensities.
More than the metabolic load, it is likely that the neuro-mechanical-linked
respiratory stimuli induced by the cramped position in rowing
can exert more influence on breathing compared to the peripheral
chemoreceptors-linked respiratory stimuli; this was likely less
in cycling (Seebauer et al., 2003b)
and running (Paterson et al., 1987)
tasks. In rowing, Cunningham et al., 1975
speculated that, at catch, the body is in a cramped position
with both knees and hips flexed. Increased intra-abdominal pressure
in this position may impair downward excursion of the diaphragm
and therefore inspiration. Conversely, during the drive phase
of the rowing stroke, the knees and hips extend and inspiration
may be assisted (Siegmund et al., 1999).
Moreover, the respiratory muscles are used to perform a valsalva-like
manoeuvre at the onset of each stroke in order to increase back
strength. Very tight coordination between limb and breathing
rhythms due to mechanical constraints in the thoracic region
may account for our findings in rowing. Another explicative
hypothesis could be that the hypoxic stimulus induced by altitude
(i.e., 2877 m) was not important enough to alter the degree
of coordination. We are fully conscious that we should have
measured the arterial O2 saturation and / or the
arterial O2 pressure in order to verify the direct
effect of the hypoxic stimulus. But, in Paterson's study (Paterson
et al., 1987),
an effect of hypoxic stimulus on the degree of coordination
was already observed as soon as subjects reached the altitude
of 2135 m.
However, we need to emphasize that these results could be distorted
by an important inter-individual difference in ventilatory response
to hypoxia (VRH) (Weil et al., 1970;
Reeves et al., 1993).
But, in a previous study no correlation was found between individual
VRH and the degree of coordination (Seebauer et al., 2003b).
Finally, the degree of coordination is known to show large interindividual
differences. Combined with the low number of subjects in our
study (n = 9) this might have masked real effects (i.e., type
II error) and so have induced failure to detect significant
differences (i.e., too low experimental power). |
|
| CONCLUSION |
| In conclusion, this study demonstrated that acute hypoxia did
not influence the degree of coordination between breathing and locomotor
rhythm during rowing at a moderate metabolic load. Neuro-mechanical
locomotion-linked respiratory stimuli appear stronger than peripheral
chemoreceptors-linked respiratory stimuli induced by hypoxia during
rowing in the context of our study. It might be quite different during
activities such as cycling or running, where the coupling between
movement and ventilation is less required. |
| ACKNOWLEDGMENTS |
| The authors gratefully acknowledge the assistance of all those
who took part in this study, Nicolas Peluhet (Engineer) for technical
help on determination of the degree of coordination, Catherine Capitan
for her contribution and Jean-Marc Abbadie, Technical Department Director
of the Pic du Midi de Bigorre observatory (France). |
| KEY
POINTS |
- Changes in breathing frequency and ventilation induced by altitude
have no effect on the degree of coordination between locomotor
and breathing rhythms during moderate rowing exercise.
- During moderate rowing exercise in hypoxia, the neuro-mechanical
drives still dominate over chemoreceptive stimuli.
- These above statements have to be taken carefully because it might
be quite different during activities where the coupling between
locomotor and breathing rhythms is less constrained (e.g., running,
cycling).
|
| AUTHORS
BIOGRAPHY |
Nicolas FABRE
Employment: Prof. at the Department of Sport Sciences, University
of Pau, France.
Degree: PhD.
Research interests: Exercise physiology, locomotor-respiratory
coupling in human, training.
E-mail: fabre.nicolas@tiscali.fr |
|
Stéphane
PERREY
Employment: Prof. at the Department of Physical Training
& Sports Engineering, Faculty of Sport Sciences, University
of Montpellier I, France.
Degree: PhD.
Research interests: Exercise physiology, acute and chronic
cardiorespiratory and muscle responses of human to physical
activity, physiological responses of endurance and power athletes,
and neuromuscular fatigue.
E-mail: stephane.perrey@univ-montp1.fr |
|
Philippe
PASSELERGUE
Employment: Prof. at the Department of Sport Sciences, University
of Pau, France.
Degree: PhD.
Research interests: Exercise physiology, acute and chronic
hormonal responses of human to physical activity, neuromuscular
adaptations to resistance training.
E-mail: philippe.passelergue@univ-pau.fr |
|
Jean-Denis
ROUILLON
Employment: Prof. at the Faculty of Sport Sciences, University
of Franche-Comté, France.
Degree: Full Professor and MD.
Research interests: Exercise physiology : Energy, Nutrition
and Human Performance.
E-mail: jean-denis.rouillon@univ-fcomte.fr |
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