Hypaxial muscle activity during running and breathing in dogs
Department of Biology, University of Utah, Salt Lake City, UT 84112, USA
* e-mail: deban{at}mac.com
Accepted 16 April 2002
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: hypaxial muscle, ventilation, locomotion, locomotorrespiratory coupling, mammal, dog, Canis familiaris
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The dual role of the hypaxial muscles poses a problem for sustained
locomotion because potentially conflicting demands placed on the hypaxial
muscles in a running tetrapod would be expected to compromise their locomotor
or ventilatory actions. Consistent with the possibility of conflicting demands
is the observation that the hypaxial muscles of lizards abandon their
ventilatory function during moderate-speed and rapid running (Carrier,
1989,
1990
,
1991
). The loss of ventilatory
function by the hypaxial muscles in running lizards is associated with reduced
costal ventilation (Carrier,
1987a
,
1991
;
Wang et al., 1997
;
Owerkowicz et al., 1999
) and
has been suggested to represent an evolutionary constraint on the aerobic
capacity and locomotor stamina of lizards (Carrier,
1987b
,
1991
). The intercostal muscles
of dogs have also been shown to abandon ventilatory function when ventilatory
and locomotor cycles become uncoupled during trotting
(Carrier, 1996
); however,
costal ventilation in dogs appears to be less affected by locomotion than in
lizards and is augmented by the ventilatory action of the diaphragm muscle
(Ainsworth et al., 1996
). In
contrast to that of the interosseus intercostals, the activity of the
parasternal portions of the internal intercostal muscles of dogs remains
entrained to ventilation, specifically inspiration, rather than locomotion
when breathing becomes uncoupled (Carrier,
1996
), and the activity of the transversus abdominis remains
entrained to both expiration and stride events
(Ainsworth et al., 1996
).
Nevertheless, the nature of the dual role of many of the hypaxial muscles and
the implications for locomotor behavior and performance remain poorly
understood.
The two groups of tetrapods that are capable of sustained vigorous
locomotion, mammals and birds, entrain their ventilatory and locomotor cycles
when they run. During running, birds and trotting mammals often couple at one
breath per step (2:1) or one breath per stride (1:1)
(Bramble and Carrier, 1983;
Bramble and Jenkins, 1989
;
Nassar et al., 2001
). Bounding
gaits, such as galloping, are associated with 1:1 coupling, in which
expiration occurs as the back flexes in the sagittal plane during forelimb
support and inspiration occurs as the back extends during hindlimb support.
Flying birds exhibit a wide variety of coupling patterns from one breath per
locomotor cycle (1:1) to one breath per five locomotor cycles (1:5)
(Berger et al., 1970
;
Boggs, 1997
). In all cases,
coupling represents strict phase locking of respiratory events to specific
locomotor events. Although the physiological significance of coupling is not
well understood (Lee and Banzett,
1997
), the hypothesis that it bestows some selective advantage is
supported by the observations that coupling appears to have evolved
independently in birds and mammals and that, in both mammals and running
birds, the natural frequency of the locomotor cycle and the resonant frequency
of the respiratory system are tuned to the same value
(Young et al., 1992
;
Nassar et al., 2001
). One
advantage of breathing in a coupled pattern is that it may minimize potential
conflict between locomotor and respiratory events such that those muscles that
effect both ventilation and locomotion can operate economically
(Funk et al., 1997
).
Evaluation of the hypothesis that coupling reduces locomotorventilatory
conflict is currently limited, in part, by our lack of understanding of the
dual function of the hypaxial musculature during running and breathing.
We undertook this study to differentiate the locomotor and ventilatory functions of the hypaxial muscles in running mammals, i.e. to identify those muscles that are primarily locomotor, those that are primarily ventilatory and those with a dual function. In particular, we were interested in the functions of the external and internal oblique muscles that had not been studied in mammals other than humans. We monitored ventilation and the activity of the major hypaxial muscles in dogs trotting on a motorized treadmill. We searched for associations between the timing of the activity of individual muscles and the locomotor or ventilatory cycle by taking advantage of fact that dogs sometimes uncouple their breathing and locomotor cycles such that the phase relationship of the two cycles changes over time.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Instrumentation
For surgery, subjects were initially anesthetized with an intravenous
injection of Pentethal. They were then intubated with an endotracheal tube and
maintained on a ventilator with oxygen to 1.3 MAC (minimal alveolar
concentration) and 1-2% isofluorane for the duration of the surgery. Incisions
were made through the skin above the site of electrode placement, and patch
(intercostal muscles) or sew-through (oblique and appendicular muscles)
electrodes were secured to the muscles of interest. Electrodes were
constructed from 0.3 mm diameter, multistranded Teflon-insulated
stainless-steel wire (Cooner Wire, Inc.; part AS636). Lead wires from the
electrodes were passed subcutaneously to a dorsal exit point just caudal to
the dorsal tips of the scapulae. Electromyographic (EMG) signals were passed
through a separate shielded, lightweight cable for each electrode (Cooner
Wire, Inc.; part NMUF2/30-404b SJ), filtered above 1000 Hz and below 100 Hz,
and amplified approximately 2000 or 5000 times with Grass P511 AC amplifiers.
These signals were sampled at 4000 Hz and stored in digital form on an Apple
Macintosh computer.
Two sites in the intercostal musculature, the fourth and fifth intercostal
spaces, were monitored in all 4 dogs. Two sites were implanted to provide
redundancy in case of electrode failure. Patch electrodes were placed between
the external and internal intercostal muscle segments (as described in
Loeb and Gans, 1986;
Carrier, 1996
). Electrodes
were placed between the osseous portion of the ribs, at the level of the
insertion site of the serratus ventralis muscle. Two sew-through electrodes
were placed in the thoracic and abdominal external oblique, internal oblique,
transversus abdominis muscles (all 4 dogs), two in the longissimus dorsi
muscles (3 dogs) and in one appendicular muscle, the deep pectoralis muscle (2
dogs). Electrodes in the external oblique thoracic muscle were placed in the
slips that inserted on ribs four and five. Electrodes in the abdominal
external and internal oblique and transversus abdominis muscles were
positioned in the central abdominal region at a mid-lateral location. The
electrodes in the longissimus dorsi muscle were placed mid-trunk at
approximately the level of the eleventh thoracic vertebra. Patch electrodes
were constructed by sewing the wire through 1 cmx3 cm rectangles of 0.8
mm Silastic sheeting.
Locomotor events were recorded on video with a high-speed camera (Peak Performance Technologies, Inc.) at 120 fields s-1. An analog signal of the locomotor cycle was obtained by monitoring the vertical acceleration of the trunk with an accelerometer (Microtron, 7290A-10) mounted on the back in the lumbar region. The video recordings were synchronized with the EMG and accelerometer recordings using a synchronization circuit (Peak Performance Technologies, Inc.).
Ventilatory airflow was measured with a biased-flow mask pneumotachograph. To allow the dogs to breathe and pant as naturally as possible, the mask covered the entire face and was big enough to allow the mouth to open and the tongue to hang out of the mouth. The mask was held in place by a snug collar around the neck and was sealed around the head just in front of the ears with an inflatable rubber tube. The bias flow was supplied to the mask with two 1.83 m lengths of 35 mm (internal diameter) breathing tube (666120, Hans Rudolph, Inc.) glued to the top surface of the mask. The input tube from the mask was connected to a pneumotachograph (4813, Hans Rudolph, Inc.) with a linear capacity up to 800 l min-1. An additional 0.61 m length of breathing tube was connected to the upstream side of the pneumotachograph, making the total length of tubing on the upstream side of the mask 2.44 m. The output tube from the mask was connected to a constant-flow vacuum controlled by a rheostat that produced a bias flow that ranged from 2 to 41 s-1, depending on the dog. Pressure changes across the pneumotachograph were measured with an Omega 176 differential pressure transducer, with a range of ±1.75 kPa (±17.8 cmH2O).
Analysis of electromyographic data
To examine the relationships between EMG bursting pattern and ventilation
and locomotion, we generated ensemble averages (Banzett et al.,
1992a,
b
) of periodic muscle activity
for each muscle from 27-32 samples per muscle. Ensemble averages were
generated from rectified EMG signals using two different types of sampling
window: (i) extending from the time of peak expiratory airflow to the next
peak expiratory airflow, and (ii) extending from the time of peak vertical
acceleration of forelimb support contralateral to the electrodes to the next
peak vertical acceleration of contralateral forelimb support
(Fig. 1). Ensemble averages
were generated from trials in which the phase relationship between the
ventilatory and locomotor cycles drifted relative to one another (uncoupled)
and from trials in which ventilation and locomotion were phase-locked to one
another (coupled). Both types of sampling window were used for uncoupled
trials. For coupled trials, because ventilation and locomotion were locked in
phase, ensemble averages generated relative to the ventilatory cycle (type i,
above) and those generated relative to the stride (type ii, above) would be
identical. Therefore, we sampled only relative to stride. Three different
ensemble averages were thus generated for each muscle from each dog: (i)
coupled, sampled relative to stride, hereafter called the coupled average;
(ii) uncoupled, sampled relative to breath, called the uncoupled breath
average; and (iii) uncoupled, sampled relative to stride, called the uncoupled
stride average.
|
The distinction between coupled and uncoupled trials was based on
examination of the relative durations of the ventilatory and locomotor cycles
and their relative timing. When one looks at the ventilation and acceleration
traces, it is immediately obvious whether a dog's breathing is coupled or
uncoupled to locomotor events. In a sample of 15 steps of coupled locomotion
from one dog, for example, the timing of a ventilatory event, peak expiratory
airflow, relative to a locomotor event, mid-stance of the left forelimb,
showed a standard deviation of 6.7 ms. The steps had a mean duration of 240
ms. The ratio of these values reveals a 2.8 % drift in the relative timing of
locomotor and ventilatory events during coupled locomotion. In contrast,
during uncoupled locomotion, in which locomotor and ventilatory cycles have
different periods, ventilation can drift by 100 % in as few as four steps (for
examples of coupled and uncoupled trials, see
Fig. 3 in
Carrier, 1996). Even slight
differences in ventilatory and locomotor periods resulted in an obvious shift
of the two signals when examined over several strides, so periods of coupled
and uncoupled breathing were easily and reliably identified.
|
EMG signals within a sampling window varied in duration and consequently differed in the number of recorded points. To enable averaging across multiple samples of different durations, EMG signals were re-sampled by linear interpolation using a custom-built LabVIEW program to produce signals 800 points in length regardless of the original length. Ensemble averages were generated by averaging the value for each of the 800 points across multiple (27-32) samples for a given muscle EMG. The result was a series of 800 points that represented the average activity of the muscle during the period of interest (i.e. peak expiration to peak expiration or peak vertical acceleration to peak vertical acceleration) (Fig. 1). The ensemble averages also facilitated comparison among dogs and trials.
Ensemble averages generated relative to breathing (i.e. uncoupled breath averages) allowed us to examine the relationship between muscle activity and ventilation, i.e. to determine whether EMG activity was concentrated in or absent from particular periods of the breathing cycle. If EMG activity were correlated with the breathing cycle, we would expect the ensemble average of uncoupled breaths to show areas of increased activity and areas of little or no activity. If activity were to occur independently of the breathing cycle, we would expect a flat, noisy trace with no areas of concentrated high-amplitude activity. Similarly, ensemble averages of uncoupled trials generated relative to the stride (i.e. uncoupled stride averages) should show periodic increases in activity if the muscle activity was associated with locomotion, or flat, noisy traces if there was no association.
To prevent a biased representation in our ensemble averages of activity occurring during (or absent from) different regions of our sampling window, we `whitened' the data from uncoupled breathing trials by sampling equally from several locomotion/ventilation phase relationships for each ensemble average. Thus, all phase relationships of drifting bursts of activity were `captured' with equal frequency in each part of the sampling window. `Whitening' was not necessary for coupled breathing trials because locomotion and ventilation were locked to one another (i.e. no drifting of EMG activity occurred).
An average for each of the three different ensemble averages was generated across all dogs for each muscle to examine overall patterns. Prior to averaging across dogs, the ensemble averages for each dog were normalized to a percentage of maximum activity by dividing each value in each ensemble average by the maximum value obtained for that dog, whether that maximum be in the coupled average, uncoupled breath average or uncoupled stride average. By averaging normalized values, the pattern from one dog would not overwhelm the pattern from another (because of differences in EMG signal strength among electrodes, for example).
Interpretation of ensemble averages
Four combinations of phasic activity in the uncoupled ensemble averages are
possible: phasic activity in neither uncoupled breath average nor uncoupled
stride average, activity in uncoupled breath average, activity in uncoupled
stride average and activity in both uncoupled averages. In the simplest case,
the first possibility, a pattern of no bursting in either the uncoupled stride
average or the uncoupled breath average would indicate that the muscle
functions in neither locomotion nor ventilation. The second possibility, a
bursting pattern in the breath average, for example, and no bursting in the
corresponding stride average, would indicate that the muscle (i) has a
ventilatory function and is active periodically to power ventilation, and (ii)
has no consistent locomotor function. Alternatively, a bursting pattern in the
uncoupled stride average and no bursting in the corresponding breath average
would reveal that the muscle (i) has a locomotor function and is turned on to
power locomotion, and (ii) has no consistent ventilatory function. The third
possible pattern, bursting in both averages, would indicate that the muscle
has both functions and is active to contribute to both ventilation and
locomotion.
When the activities of the muscles during standing and panting (i.e. during only ventilatory function) and in coupled averages are considered together with these four patterns from running and breathing, muscles can be placed into four functional categories. (i) Pure locomotor function; no bursting during standing and panting, but bursting in the uncoupled stride average and no bursting in the uncoupled breath average. This pattern would indicate that the muscle is active at the appropriate time to perform a locomotor function and has no effect on ventilation. (ii) Primarily locomotor function; bursting during standing and panting and bursting in the uncoupled stride average and coupled average, and no bursting in the uncoupled breath average. This pattern would reveal that, although the muscle functions during ventilation when the dogs are not running, the muscle takes on a locomotor function and abandons its ventilatory function during trotting. (iii) Dual function; bursting during standing and panting, as well as in both uncoupled averages; this pattern would suggest that the muscle is active during trotting only when it can contribute to both ventilatory and locomotor functions. (iv) Ventilatory function; bursting during standing and panting, and in the uncoupled breath average and coupled average, but not in the uncoupled stride average. This pattern would show that the muscle is active when it needs to contribute to ventilation, regardless of its effect on locomotion.
These four categories illustrate the different potential responses of muscles to functional conflicts. If a muscle were to have a primarily locomotor function, it would have a ventilatory function during rest, but the locomotor function would override it during running. In other words, the bursts of activity would drift relative to the breath cycle, at times assisting in ventilation and at times hindering it. Activity would be independent of ventilation, which would presumably be effected by other muscles. Another possible response to functional conflict would be to adjust the timing or duration of bursts to reduce the conflict, as might occur in muscles with a dual function. Thus, we expect that a shift in timing of bursts relative to stride or ventilation from coupled to uncoupled running would indicate a functional conflict (i.e. a burst shifts in the uncoupled breath or stride average from its position in the coupled average to avoid conflict), but not one severe enough to necessitate complete abandonment of one function as in muscles with a primarily locomotor function.
The effects of coupled versus uncoupled breathing on the EMG
pattern of each muscle were examined quantitatively by a modification of the
methods of Farley and Koshland
(2000). For each muscle,
Pearson correlations (r) were determined for the uncoupled stride
average versus the coupled stride average and for the uncoupled
breath average versus the coupled breath average (coupled breath
averages were obtained by re-sampling coupled stride averages relative to
breath). Each correlation coefficient was then squared to yield the
coefficient of determination (r2), which indicates the
proportion of the point-to-point variation in the uncoupled ensemble average
that is explained by variation in the coupled ensemble average. A high
r2 indicates that the two ensemble averages are similar
and that uncoupled breathing has little effect on the pattern of muscle
activity. A low r2 indicates that the ensemble averages
are different, either because the temporal pattern of bursting is effected by
coupling or because the muscle shows no bursting in the uncoupled average.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
During panting while standing still, several muscles showed activity associated with ventilatory events (Fig. 2). The internal oblique abdominal, external oblique abdominal, external oblique thoracic, internal intercostal and transversus abdominis showed activity in the latter half of inspiration and the beginning of expiration; this pattern is consistent with an expiratory function for these muscles. Two muscles, the parasternal portion of the internal intercostal and the external intercostal, were active out of phase with the other muscles, showing bursts that extended from the second half of expiration to the beginning of inspiration. This pattern is appropriate for generating inspiratory airflow. These muscles were never all active simultaneously, however, and appeared to trade off from minute to minute as the dogs changed posture slightly. Fig. 2 shows the pattern of activity that each muscle showed when it was active, but this figure should not be interpreted to indicate that all the muscles shown were active at the same time. The longissimus dorsi and pectoralis showed no activity while the dogs were standing still.
|
During running, the transversus abdominis, external intercostal, internal intercostal, parasternal internal intercostal and external oblique thoracic muscles showed phasic activity in uncoupled ensemble averages sampled relative to both ventilation and locomotion. Only two hypaxial muscles showed phasic activity in uncoupled ensemble averages sampled only relative to locomotion during running: the internal oblique abdominal and the external oblique abdominal. The coefficients of determination (r2) that indicate the degree to which the locomotor and ventilatory activity of each muscle is influenced by the pattern of breathing (coupled versus uncoupled) are listed in Table 1. The pattern of activity of each muscle during running is described below.
|
External intercostal
The external intercostal muscle showed phasic activity in both uncoupled
breath and stride averages (Fig.
3). Among coupled averages, there was a great deal of variation
from dog to dog, with 1-4 bursts of activity. The largest burst was associated
with the flight phase and the first half of ipsilateral forelimb support and
occurred during the second half of expiration and the first half of
inspiration. The shorter, lower-amplitude bursts were associated with
mid-contralateral forelimb support and were centered on peak inspiratory
airflow. The coupled average of all dogs
(Fig. 3E) showed a large burst
associated with the first half of ipsilateral forelimb support and a much
smaller burst centered on mid-contralateral forelimb support. In uncoupled
stride averages, the bursts were more variable and dispersed in time than in
coupled averages. The greatest activity was generally associated with
mid-contralateral forelimb support, and smaller bursts were associated with
mid-ipsilateral forelimb support. The uncoupled stride average pattern from
all dogs (Fig. 3E) showed two
bursts per stride, the larger burst associated with mid-contralateral forelimb
support and the slightly smaller burst associated with the first half of
ipsilateral forelimb support. In uncoupled breath averages, increased activity
was evident extending from peak expiratory airflow to peak inspiratory airflow
in all dogs. This pattern is consistent with an inspiratory function. During
standing and panting (Fig. 2),
activity also occurred appropriately for inspiration.
Internal intercostal
The internal intercostal muscle showed phasic activity in both the
uncoupled breath averages and the uncoupled stride averages, but the stride
averages showed a much stronger pattern. The patterns of the EMGs in the
uncoupled stride averages were very similar to the coupled averages
(Fig. 4, first two columns).
There were typically two bursts of activity, both centered on peak expiratory
airflow during coupled breathing. The shorter, lower-amplitude burst occurred
at the transition from contralateral to ipsilateral forelimb support. The
larger burst was centered at the transition from ipsilateral to contralateral
forelimb support and extended from mid-ipsilateral support to
mid-contralateral support at its greatest extent. In the uncoupled breath
averages (Fig. 4, third
column), activity was not as concentrated into bursts as in coupled breathing,
but a low-amplitude single period of increased activity was evident extending
from peak inspiratory airflow to peak expiratory airflow, indicative of an
expiratory function. Activity appropriate for expiration also occurred during
this period when the dogs were standing
(Fig. 2).
|
Parasternal internal intercostal
The parasternal portion of the internal intercostal muscle showed bursting
in coupled averages, uncoupled breath averages and uncoupled stride averages
(Fig. 5). In coupled averages,
the largest burst was associated with the first half of contralateral forelimb
support and the smaller bursts were associated with the beginning of
ipsilateral support. In uncoupled stride averages, the bursts were not as
clean or as consistent among dogs as was the case in the coupled averages. The
largest burst was associated with the second half of contralateral forelimb
support in one dog, the second half of ipsilateral support in one dog and the
transition from ipsi- to contralateral support in one dog, and there were no
clear bursts in the fourth dog. The uncoupled stride average from all dogs
(Fig. 5E) showed little
bursting because of the high degree of variation among dogs. In uncoupled
breath averages, bursts were similar in all dogs: bursts extended from peak
expiratory airflow to peak inspiratory airflow, consistent with an inspiratory
function. The dog that showed no bursting in its stride average showed the
strongest, cleanest bursting in the breath average. Bursts were much clearer
during coupled than during uncoupled breathing, indicating that the
relationship between breathing and stepping during coupled breathing was
appropriate for both locomotor and ventilatory activity in this muscle, and
some interference occurred during uncoupled breathing. During standing and
panting (Fig. 2), activity was
also appropriate for inspiration.
|
External oblique thoracic
The external oblique thoracic muscle showed phasic activity in both
uncoupled stride averages and breath averages
(Fig. 6). A burst was present
centered on or near each forelimb support in coupled averages. In uncoupled
stride averages, the burst associated with ipsilateral forelimb support was
consistently larger. Uncoupled breath averages showed bursts extending from
peak inspiratory airflow to peak expiratory airflow, consistent with an
expiratory function. As in both the external oblique abdominal and internal
oblique abdominal muscles, activity during rest
(Fig. 2) indicates an
expiratory function for the external oblique thoracic muscle.
|
External oblique abdominal
The external oblique abdominal muscle showed phasic activity in uncoupled
stride averages and very little phasic activity in uncoupled breath averages
(Fig. 7). In coupled and
uncoupled stride averages, the largest spike was centered on mid-contralateral
forelimb support, and a secondary burst was associated with the start of
ipsilateral forelimb support. In one dog, the secondary burst was as large as
the primary burst and longer in duration. Uncoupled breath averages showed no
bursting and only a slight increase in activity during inspiration in one dog.
These patterns reveal that the external oblique abdominal muscle is primarily
a locomotor muscle and has little if any ventilatory function during running.
During rest (Fig. 2), activity
occurred during the latter half of inspiration, consistent with a role in
expiration.
|
Internal oblique abdominal
The internal oblique abdominal muscle showed phasic activity in uncoupled
stride averages and very little in uncoupled breath averages
(Fig. 8), a pattern similar to
that of the external oblique abdominal. The largest burst in the stride
averages was associated with the first half of contralateral forelimb support,
and a secondary burst was sometimes present in association with the first half
of ipsilateral forelimb support. This pattern was virtually identical to that
in the coupled averages. Uncoupled breath averages showed no clear bursts,
although a slight increase in activity was evident in one dog in association
with the latter half of inspiratory airflow. The ensemble averages considered
together indicate that the internal oblique abdominal muscle has primarily a
locomotor role during running. During standing and panting
(Fig. 2), activity occurred
during the second half of inspiration, appropriate for expiration.
|
Transversus abdominis
The transversus abdominis muscle showed bursting in both uncoupled stride
averages and breath averages. It was active during mid-forelimb support in
both the coupled averages and the uncoupled stride averages
(Fig. 9). Activity during
ipsilateral forelimb support was slightly greater than activity during
contralateral forelimb support, particularly in uncoupled stride averages. In
uncoupled breath averages, a burst extended from peak inspiratory airflow to
peak expiratory airflow, a pattern consistent with an expiratory function.
During panting at rest (Fig.
2), this muscle was active during the second half of inspiration,
also consistent with an expiratory function.
|
Deep pectoralis
The deep pectoralis muscle showed bursting in uncoupled stride averages and
coupled averages and almost none in uncoupled breath averages
(Fig. 10). Activity was
associated with the latter half of contralateral forelimb support and early
ipsilateral forelimb support. A very slight increase in activity was
associated with inspiration in one dog, but the absence of any pattern during
standing and panting (Fig. 2)
indicates no ventilatory function for the deep pectoralis.
|
Longissimus dorsi
The longissimus dorsi muscle showed phasic activity in coupled averages and
uncoupled stride averages (Fig.
11). A single burst occurred during the second half of
contralateral forelimb support. Uncoupled breath averages showed no bursting
or periodic increases in activity, indicating no ventilatory function for the
longissimus dorsi. No activity was present during standing and panting
(Fig. 2); thus, there is no
ventilatory role for this muscle during rest.
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The pectoralis and longissimus dorsi muscles appear to have a pure
locomotor function during running. The high correlations between uncoupled
versus coupled stride averages (r2=0.72 and
r2=0.96, respectively;
Table 1) indicate that the
locomotor functions of these muscles were relatively unaffected by whether
breathing was coupled. The low correlations between breath averages
(r2=0.02 and r2=0.003, respectively)
reflect the absence of a ventilatory function for these muscles. The
pectoralis and longissimus dorsi are appendicular and epaxial muscles,
respectively, and showed no ventilatory activity during standing and panting,
as expected for muscles in their positions. The longissimus dorsi muscle is in
a position to extend the back or resist flexion, and it has been suggested
that it helps to stabilize the trunk against inertial loading, which causes
the trunk to sag and rebound during each trotting step
(Ritter et al., 2001). The
activity of this muscle during forelimb support is consistent with this
hypothesized function. The pectoralis muscle is in a position to retract the
forelimb or resist protraction (Evans,
1993
), and its activity just prior to and during early ipsilateral
forelimb support suggests that it breaks the forward movement of the forelimb
and accelerates it backwards. The activity of the pectoralis ceases early in
support, indicating that it does not contribute to forward propulsion.
The internal oblique abdominal and external oblique abdominal muscles had
an expiratory function when the dogs were at rest, but abandoned this function
during running, and their activity remained associated with locomotor events.
The high correlations between uncoupled and coupled stride averages
(r2=0.88 for both;
Table 1) indicate that their
locomotor functions were relatively unaffected by whether breathing was
coupled. The low correlations between breath averages
(r2=0.07 and r2=0.14, respectively)
indicate that these muscles abandon ventilatory function during trotting. A
similar relationship has been observed in humans, in which these muscles
contribute to expiration at rest (De
Troyer and Loring, 1986) but adopt a postural function during
appendicular movements (Hodges and
Gandevia, 2000
). In running birds, these muscles have been found
to maintain a primarily locomotor function in some species and a ventilatory
function in others (Nassar,
1994
; Boggs et al.,
1999
).
The external intercostal, external oblique thoracic and transversus
abdominis muscles have a dual function during trotting, providing postural
support against the forces exerted on the trunk by the extrinsic appendicular
muscles and generating changes in thoracic volume that power ventilation.
These muscles also have a ventilatory function when the dogs are at rest
(Fig. 2). Of these muscles, the
external intercostal had the lowest correlation between stride ensemble
averages (r2=0.28;
Table 1), indicating that its
locomotor function is affected the most by uncoupled breathing. Conversely,
only the transversus abdominis showed high correlations both between breath
averages (r2=0.83) and between stride averages
(r2=0.79), indicating that this muscle is capable of
performing locomotor and ventilatory functions simultaneously, even if
breathing is uncoupled. This dual ventilatory and postural role of the
transversus abdominis has been observed previously in dogs
(Ainsworth et al., 1996) and
humans (Hodges and Gandevia,
2000
). In humans, the transversus abdominis has separate
populations of motor neurons for postural and ventilatory functions
(Puckree et al., 1998
). The
dual-function muscles in general showed a clean bursting pattern in the
coupled averages but a noisier bursting pattern in both uncoupled averages,
indicating slight shifts in timing of bursts and, hence, some level of
conflict between locomotor and ventilatory functions.
The internal intercostal muscle showed a similar pattern, but exhibited only slight bursting in the uncoupled breath average. Thus, it may be considered a muscle with a dual function, but with more of a locomotor role (or less of a ventilatory role) than the other dual-function muscles. Supporting this interpretation is the observation that the internal intercostal maintained the same clean bursting pattern in the coupled average and the uncoupled stride average, while the uncoupled breath average was much noisier, and the observation that the correlation between stride ensemble averages was high (r2=0.83; Table 1). The low correlation between breath averages (r2=0.06) is not due to an absence of bursting in the uncoupled breath average, as it is for the oblique abdominal muscles, but rather to a temporal redistribution of the bursts in the uncoupled breath average such that they do not match those in the coupled breath average.
The parasternal portion of the internal intercostal muscle showed the most
unusual EMG pattern of all the muscles examined. We place it in the category
of ventilatory muscles because it was active during inspiration while the dogs
stood panting, as has been shown previously
(DeTroyer and Loring, 1986),
stayed synchronized with inspiration during both coupled and uncoupled
breathing and had a higher correlation between breath averages
(r2=0.35; Table
1) than between stride averages (r2=0.001).
However, the relatively low correlation between breath averages reveals that
uncoupled breathing disrupted the ventilatory function of this muscle to some
extent. The average across all dogs (Fig.
5E) showed a noisy trace in the uncoupled stride average, but
relatively clean bursts in the coupled average and the uncoupled breath
average. Carrier (1996
) found
the same pattern in trotting dogs. The absence of a consistent pattern of
activity when averaged relative to locomotor events makes it impossible to
assign a locomotor role to this muscle that would be the same in all dogs.
Dual role of the interosseus intercostal muscles
Carrier (1996) examined the
EMG activity of the intercostal muscles of dogs during trotting and breathing
and obtained similar results, but with an interesting difference from the
results reported here: the internal and external intercostal muscles
(interosseus portions) at two positions on the trunk showed bursting in the
uncoupled stride average and no bursting in the uncoupled breath average
(compared with bursting in both uncoupled stride and uncoupled breath averages
in the present study). The results of Carrier
(1996
) led to the conclusion
that the intercostal muscles have a primarily locomotor function and abandon
their ventilatory role in running dogs. We do not doubt the veracity of these
results or conclusions, and think they can be reconciled with the current
study by considering the different loads placed on the ventilatory system in
the two different experiments. Carrier
(1996
) used a low-resistance
mask-mounted screen pneumotachograph with a bias flow of 2-41 s-1
to provide fresh air for respiration, which produced small negative pressures
in the mask (-29.4 to -61.8 Pa; -0.30 to -0.63 cmH2O). The current
study used a tube-mounted screen pneumotachograph with a higher resistance to
flow and consequently greater negative pressures (-55 to -164 Pa; -0.56 to
-1.67 cmH2O for 2-41 s-1 airflow) in the mask. We
suspect that this increased negative pressure in the current system (more than
double the pressure of the previous system at higher flows) loaded the
respiratory system and forced the dogs to work harder to breathe than in the
earlier study.
The differences in the methods used and data from these two studies suggest
that controlled studies in which respiratory load is changed would be
worthwhile. These studies suggest that dogs are capable of recruiting the
intercostal muscles, particularly the external intercostal, for both
ventilation and locomotion when necessary, but are also capable of using the
intercostal muscles solely for locomotion when the opportunity arises. In
nature, circumstances must arise when the ventilatory system experiences
differing locomotor loads, such as running uphill or carrying prey
versus running unencumbered on level ground, and the respiratory
system would need to make adjustments to muscular recruitment to counteract
the loads. Similarly, recent work in sheep and dogs indicates that, in species
that pant to thermoregulate and that couple their ventilation to the locomotor
cycle during galloping, regulation of body temperature during galloping
competes with control of pH balance (Entin et al.,
1998,
1999
;
Wagner et al., 1997
). Thus, an
ability to modulate the recruitment of the intercostals muscles for locomotor
or ventilatory function as the need arises during trotting would appear to be
beneficial.
Implications for integration and neural control
The observation that dogs can ventilate their lungs using various
combinations of hypaxial muscles while standing and panting
(Fig. 2) suggests that there is
functional overlap and even redundancy in the ventilatory musculature. This
interpretation is supported by the observation discussed above that muscles,
such as the intercostals, are recruited for breathing during trotting as
ventilatory load changes. We propose that the functional redundancy of the
ventilatory musculature may circumvent locomotorventilatory conflicts
in particular muscles and allow dogs to maintain steady breathing under
changing locomotor forces acting on the trunk and under changing ventilatory
loads. Hence, both the functional redundancy of the hypaxial musculature and
the dual role of some muscles in locomotion and ventilation indicate that the
neural control of ventilation during running in mammals is more complex than
is generally recognized.
A running mammal not only must adjust the activity of its ventilatory
muscles to accomplish gas exchange, thermoregulation
(Lee and Banzett, 1997) and to
regulate acidbase balance (Entin et
al., 1999
), it must also change the activity of its ventilatory
muscles in accordance with their locomotor functions. The examples mentioned
above of running uphill or carrying prey not only increase metabolic rate,
requiring greater rates of ventilation, but they also change the need for
locomotor recruitment of the hypaxial muscles responsible for ventilation.
Running uphill, for example, is associated with increased activity of the
internal oblique and internal intercostal muscles in dogs, but decreased
activity of the external oblique and external intercostal muscle
(Fife et al., 2001
). The
pattern is reversed when dogs run downhill: greater activity in the external
oblique and intercostal and less activity in the internal oblique and
intercostal muscles. These adjustments in recruitment appear to stabilize the
trunk against activity of the extrinsic appendicular muscles that place
shearing forces on the trunk in the sagittal plane
(Fife et al., 2001
).
Furthermore, in the variable terrain of the natural world, every step is
different in the forces applied to the trunk and in the period of force
application. Hence, every step would place variable and possibly unpredictable
demands on the activity and force production of the hypaxial muscles
responsible for lung ventilation. How the nervous system modifies the activity
of the axial muscles during running to maintain the mechanical integrity of
the trunk while at the same time adjusting ventilation in accordance with the
need for gas exchange and thermoregulation remains difficult to imagine and
largely unstudied.
The problem the nervous system faces in coordinating ventilation and
locomotion using shared muscles might conceivably be simplified by coupling
the two cycles in a limited number of possible phase relationships. The idea
that coupling reduces mechanical conflicts and may thus improve the economy of
ventilation is not new (Bramble and
Carrier, 1983; Young et al.,
1992
; Bramble and Jenkins,
1993
; Boggs et al.,
1997
; Boggs, 1997
;
Funk et al., 1997
;
Lee and Banzett, 1997
;
Entin et al., 1999
;
Nassar et al., 2001
). In
humans, although our locomotor and ventilatory functions are largely uncoupled
because of our bipedality, coupling is routine in most experienced runners
(Bramble and Carrier, 1983
;
Bramble, 1983
), and running
with coupled breathing appears to be slightly more economical than running
with uncoupled breathing (Bernasconi and
Kohl, 1993
). An even greater energetic benefit of coupled
breathing is expected in quadrupeds, in which the trunk plays a greater role
in locomotion (Carrier,
1984
).
Given the demands of locomotion on the trunk musculoskeletal system and the
dual function of the hypaxial muscles in quadrupeds, specific periods in a
trotting cycle may mechanically facilitate inspiration and other periods may
facilitate expiration. In addition, coupling locomotion and ventilation in
particular phase relationships (2:1 or 1:1) may simplify the pattern of
activation needed in the hypaxial musculature (Banzett et al.,
1992a,b
;
Lee and Banzett, 1997
) and may
help the muscles to perform both functions simultaneously. This line of
reasoning suggests that breathing in an uncoupled pattern would require
greater muscular recruitment and more complicated neural control.
Ventilatorylocomotor coupling is known to occur only in birds and
mammals and thus is likely to have evolved independently
(Carrier, 1987b
), and in both
mammals and running birds the resonant frequency of the respiratory system
matches the natural frequency of the locomotor cycle
(Young et al., 1992
;
Nassar et al., 2001
). This
convergent evolution suggests that coupling has a selective advantage.
Reducing functional conflicts in the trunk musculature and simplifying control
demands may have been selective forces contributing to the evolution of
coupling.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Ainsworth, D. M., Smith, C. A., Henderson, K. S. and Dempsey, J.
A. (1996). Breathing during exercise in dogs passive
or active? J. Appl. Physiol.
81,586
-595.
Banzett, R. B., Mead, J., Reid, M. B. and Topulos, G. P.
(1992a). Locomotion in men has no appreciable mechanical effect
on breathing. J. Appl. Physiol.
72,1922
-1926.
Banzett, R. B., Nations, C. S., Wang, N., Butler, J. P. and Lehr, J. L. (1992b). Mechanical independence of wingbeat and breathing in starlings. Respir. Physiol. 89, 27-36.[Medline]
Bennett, W. O., Simons, R. S. and Brainerd, E. L.
(2001). Twisting and bending: the functional role of salamander
lateral hypaxial musculature during locomotion. J. Exp.
Biol. 204,1979
-1989.
Berger, M., Roy, O. Z. and Hart, J. S. (1970). The co-ordination between respiration and wing beats in birds. Z. Vergl. Physiol. 66,190 -200.
Bernasconi, P. and Kohl, J. (1993). Analysis of co-ordination between breathing and exercise rhythms in man. J. Physiol., Lond. 471,693 -706.[Abstract]
Boggs, D. F. (1997). Coordinated control of respiratory pattern during locomotion in birds. Am. Zool. 37,41 -57.
Boggs, D. F., Butler, P. J., Baudinette, R. V. and Frappell, P. B. (1999). Relationship amongst air sac pressures, steps and abdominal muscle activity in waddling and running birds. FASEB J. 13,A495 .
Boggs, D. F., Jenkins, F. A. and Dial, K. P.
(1997). The effect of the wingbeat cycle on respiration in
black-billed magpies (Pica pica). J. Exp.
Biol. 200,1403
-1412.
Brainerd, E. L. (1998). Mechanics of lung ventilation in a larval salamander Ambystoma tigrinum. J. Exp. Biol. 201,2891 -2901.
Brainerd, E. L. (1999). New perspectives on the evolution of lung ventilation mechanisms in vertebrates. Exp. Biol. Online 4,11 -28.
Brainerd, E. L. and Monroy, J. A. (1998). Mechanics of lung ventilation in a large aquatic salamander, Siren lacertina. J. Exp. Biol. 201,673 -682.[Medline]
Bramble, D. M. (1983). Respiratory patterns and control during unrestrained human running. In Modeling and Control of Breathing (ed. B. J. Whipp and D. M. Wiberg), pp.213 -220. New York: Elsevier.
Bramble, D. M. and Carrier, D. R. (1983). Running and breathing in mammals. Science 219,251 -261.[Medline]
Bramble, D. M. and Jenkins, F. A. (1989). Structural and functional integration across the reptilemammal boundary: the locomotor system. In Complex Organismal Functions: Integration and Evolution in Vertebrates (ed. D. B. Wake and G. Roth), pp. 133-146. New York: John Wiley & Sons Ltd.
Bramble, D. M. and Jenkins, F. A. (1993). Mammalian locomotorrespiratory integration: implications for diaphragmatic and pulmonary design. Science 262,235 -240.[Medline]
Carrier, D. R. (1984). The energetic paradox of human running and hominid evolution. Curr. Anthropol. 25,483 -495.
Carrier, D. R. (1987a). Lung ventilation during walking and running in four species of lizards. J. Exp. Biol. 47,33 -42.
Carrier, D. R. (1987b). The evolution of locomotor stamina in tetrapods: circumventing a mechanical constraint. Paleobiology 13,326 -341.
Carrier, D. R. (1989). Ventilatory action of the hypaxial muscles of the lizard Iguana iguana: a function of slow muscle. J. Exp. Biol. 143,435 -457.[Abstract]
Carrier, D. R. (1990). Activity of the hypaxial muscles during walking in the lizard Iguana iguana. J. Exp. Biol. 152,453 -470.[Abstract]
Carrier, D. R. (1991). Conflict in the hypaxial musculo-skeletal system: documenting an evolutionary constraint. Am. Zool. 31,644 -654.
Carrier, D. R. (1993). Action of the hypaxial
muscles during walking and swimming in the salamander, Dicamptodon
ensatus. J. Exp. Biol. 180,75
-83.
Carrier, D. R. (1996). Function of the
intercostal muscles in trotting dogs: ventilation or locomotion? J.
Exp. Biol. 199,1455
-1465.
Davis, J. R. and Mirka, G. A. (2000). Transverse-contour modeling of trunk muscle-distributed forces and spinal loads during lifting and twisting. Spine 25,180 -189.[Medline]
De Troyer, A. and Loring, S. H. (1986). Action of the respiratory muscles. In Handbook of Physiology, The Respiratory System (ed. P. T. Macklem and J. Mead), pp.443 -561. Bethesda, MD: American Physiological Society.
Entin, P. L., Robertshaw, D. and Rawson, R. E.
(1998). Thermal drive contributes to hyperventilation during
exercise in sheep. J. Appl. Physiol.
85,318
-325.
Entin, P. L., Robertshaw, D. and Rawson, R. E.
(1999). Effect of locomotor respiratory coupling on respiratory
evaporative heat loss in the sheep. J. Appl. Physiol.
87,1887
-1893.
Evans, H. E. (1993). Miller's Anatomy of the Dog. Third edition. Philadelphia: W. B. Saunders Company.
Farley, B. G. and Koshland, G. F. (2000). Trunk muscle activity during the simultaneous performance of two motor tasks. Exp. Brain Res. 135,483 -496.[Medline]
Fife, M. M., Bailey, C., Lee, D. V. and Carrier, D. R.
(2001). Function of the oblique hypaxial muscles in trotting
dogs. J. Exp. Biol. 204,2371
-2381.
Funk, G. D., Valenzuela, I. J. and Milsom, W. K.
(1997). Energetic consequences of coordination wingbeat and
respiratory rhythms in birds. J. Exp. Biol.
200,915
-920.
Gardner-Morse, M. G. and Stokes, I. A. F. (1998). The effects of abdominal muscle coactivation on lumbar spine stability. Spine 23, 86-92.[Medline]
Hodges, P. W. and Gandevia, S. C. (2000).
Changes in intra-abdominal pressure during postural and respiratory activation
of the human diaphragm. J. Appl. Physiol.
89,967
-976.
Hodges, P. W., Gandevia, S. C. and Richardson, C. A.
(1997). Contractions of specific abdominal muscles in postural
tasks are affected by respiratory maneuvers. J. Appl.
Physiol. 83,753
-760.
Lee, H.-T. and Banzett, R. B. (1997).
Mechanical links between locomotion and breathing: can you breathe with your
legs? News Physiol. Sci.
12,273
-278.
Liem, K. F. (1985). Ventilation. In Functional Vertebrate Morphology (ed. M. Hildebrand, D. M. Bramble, K. F. Liem and D. B. Wake), pp.185 -209. Cambridge, MA: Harvard University Press.
Loeb, G. E. and Gans, C. (1986). Electromyography for Experimentalists. Chicago, IL: University of Chicago Press.
McGill, S. M. (1991). Electromyographic activity of the abdominal and low back musculature during the generation of isometric and dynamic axial trunk torque: implications for lumbar mechanics. J. Orthop. Res. 9,91 -103.[Medline]
Morris, J. M., Lucas, D. B. and Bresler, M. S. (1961). Role of the trunk in stability of the spine. J. Bone Joint Surg. 43,327 -351.
Nassar, P. N. (1994). A dual role for the abdominal muscles of running birds. Am. Zool. 34, 15A.
Nassar, P., Jackson, A. and Carrier, D. R.
(2001). Entraining the natural frequencies of running and
breathing in guinea fowl. J. Exp. Biol.
204,1641
-1651.
Owerkowicz, T., Farmer, C. G., Hicks, J. W. and Brainerd, E.
L. (1999). Contribution of gular pumping to lung ventilation
in monitor lizards. Science
284,1661
-1663.
Puckree, T., Cerny, F. and Bishop, B. (1998).
Abdominal motor unit activity during respiratory and nonrespiratory tasks.
J. Appl. Physiol. 84,1707
-1715.
Ritter, D. (1995). Epaxial muscle function
during locomotion in a lizard (Varanus salvator) and the proposal of
a key innovation in the vertebrate axial musculoskeletal system. J.
Exp. Biol. 198,2477
-2490.
Ritter, D. (1996). Axial muscle function during
lizard locomotion. J. Exp. Biol.
199,2499
-2510.
Ritter, D., Nassar, P., Fife, M. and Carrier, D. R.
(2001). Function of the epaxial muscles in trotting dogs.
J. Exp. Biol. 204,3053
-3064.
Simons, R. S., Bennett, W. O. and Brainerd, E. L.
(2000). Mechanics of lung ventilation in a post-metamorphic
salamander, Ambystoma tigrinum. J. Exp. Biol.
203,1081
-1092.
Wagner, J. A., Horvath, S. M. and Dahms, T. E. (1997). Cardiovascular, respiratory and metabolic adjustments to exercise in dogs. J. Appl. Physiol. 42,403 -407.
Wang, T., Carrier, D. R. and Hicks, J. W.
(1997). Ventilation and gas exchange in lizards during treadmill
exercise. J. Exp. Biol.
200,2629
-2639.
Young, I. S., Warren, R. D. and Altringham, J. D. (1992). Some properties of the mammalian locomotory and respiratory systems in relation to body mass. J. Exp. Biol. 164,283 -294.[Abstract]
Zetterberg, C., Andersson, G. B. J. and Schultz, A. B. (1987). The activity of individual trunk muscles during heavy physical loading. Spine 12,1035 -1040.[Medline]