Observations of consistent integer relationships
between breathing and stride cycles in
exercising birds and mammals date from Marey's
observations in the last century. The tight
temporal correlation between locomotor and
respiratory cycles in animals such as hopping
wallabies, galloping dogs and horses, and flying
bats has led investigators to propose that
during locomotion, muscles of exercising limbs
provide some or all of the work of breathing. In
this paper, we discuss the possible advantages
and disadvantages of mechanical linkages between
locomotion and breathing, consider mechanical
mechanisms that could link these two activities,
and describe experiments showing that the total
effect of such linkages provide a fraction of
tidal volume.
Kinds of linkages
Locomotion and breathing may be linked
neurally or mechanically. Neural linkages exist:
activity in limb motor nerves is coordinated
with activity in respiratory motor nerves even
during fictive locomotion in paralyzed
decerebrated animals. In contrast, the extent of
mechanical linkages is less certain. The
observation that breathing and locomotion are
coordinated does not necessarily imply a
mechanical link. However, if mechanical
interactions exist, proper neural coordination
may be necessary for the animal to benefit from
the interaction.
Mechanical interactions between breathing and
locomotion may occur in either direction:
respiratory muscle contraction could affect the
locomotor cycle, or conversely, the locomotor
cycle (stride or wingbeat) could contribute to
respiratory flow, the focus of this review.
Although mechanical interactions have been
proposed in a range of animals, including fish,
lizards, birds and mammals, and during various
forms of locomotion, from hopping in wallabies
to rowing in humans, we limit our review to
flying, hopping, walking, and running in birds
and mammals.
Advantages and disadvantages of mechanical
links
One possible advantage of a mechanical link
between breathing and locomotion is reduction of
the energetic cost of breathing. The best
estimates of the oxygen cost of breathing during
exercise have been made by asking human subjects
to voluntarily mimic their respiratory patterns
during exercise. These studies show that, during
exercise at maximal aerobic capacity (VO2 max),
the cost of breathing averages 10% of total
oxygen consumption; during moderate exercise
(70% of maximal aerobic capacity), the cost of
breathing is a smaller fraction of total oxygen
consumption, +/-5% (1). Transferring energy from
limb muscles to breathing saves energy only if
this energy would have otherwise been lost. In
running (but probably not in flying), much
energy is stored from cycle to cycle by
alternating among gravitational potential,
elastic, and kinetic forms. In breathing, a
large part of the energy is expended to overcome
airway and tissue resistance and dissipates as
heat; little or none is available for the next
cycle. Thus transfer of energy from locomotor
activity to breathing might reduce the work of
respiratory muscles but increase the work of the
legs.
A second possible advantage is that breathing
performance (maximum ventilation) may be
increased with the assistance of limb muscle
activity. Even in the absence of energy savings,
this could be advantageous in cases when the
power or endurance of respiratory muscles limits
alveolar ventilation, causing a drop in alveolar
PO2 during very heavy exercise. Such a limit to
breathing performance has been observed in
thoroughbred horses and elite human athletes but
bas not yet been reported in other cases.
A third possible advantage, neglected in many
treatments of this subject, is that gas mixing
from locomotor-induced volume changes may reduce
effective dead space, thus increasing the
effective alveolar ventilation for a given total
ventilation. Smail, high-frequency volume
displacements can reduce effective airway dead
space to zero. Such mixing will be most
important at low tidal volumes where the ratio
of dead space ventilation to alveolar
ventilation is high. High-frequency mixing, in
contrast to tidal volume assistance, would not
depend on coordination of breath-stride phase
relationships.
A fourth possible advantage is that synchrony
may feel more comfortable, a phenomenon reported
by many human runners.
If the mechanical link is strong, a possible
disadvantage is reduced flexibility in changing
ventilation to meet metabolic and thermal
demands. If stride were to produce all or most
of tidal volume, the animal would be obligated
to breathe at stride frequency to take advantage
of constructive interference and to avoid
destructive interference. The metabolic and
thermal demands on ventilation are not tightly
linked to stride frequency or length, and, thus,
an inability to uncouple breathing from
locomotion could result in ventilation that is
inappropriate for the control of gas or heat
exchange. For example, during climbing
(terrestrial or aerial), energetic costs
increase, whereas the frequency and amplitude of
the locornotor cycle may stay constant or even
decrease. Similarly, the ventilatory requirement
for heat loss is a function both of exercise
heat production and of ambient temperature and
humidity and is thus not simply related to
stride frequency and amplitude.
Another possible disadvantage of strong
mechanical linkage is that animals may be forced
to breathe at energetically unfavorable
frequency tidal volume combinations. The
frequency of the locomotor cycle is high
compared with the frequency of breathing at rest
or during hypercapnia. A given alveolar
ventilation requires more work at high frequency
and low tidal volume combinations because dead
space contribution is proportionately greater
and because a significant amount of energy may
be necessary to accelerate gas in the airways.
Thus far, no published models have incorporated
the more recently developed concept of
high-frequency mixing that would change the
determination of optimal frequencies nor have
these models been applied to the problem of
breathing at stride frequency.
Proposed rnechanical 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. Several mechanical linkage
mechanisms have been proposed.
Inertial displacement of the diaphragm or
visceral piston mechanism. As an animal
accelerates and decelerates with each stride,
the abdominal viscera move relative to the spine
(and thoracic cage) because they are not a
rigidly attached mass. When the viscera
underlying the diaphragm move along the
cranial-caudal axis, they change the volume of
the thoracic cavity and can cause airflow:
inspiration when the diaphragm is displaced
caudally by cranial acceleration of the trunk
and expiration when the diaphragm is displaced
cranially by trunk deceleration. ln this way,
the viscera may act like a piston and drive
changes in lung volume (8).
Inertial displacement of the rib cage.
When the spine accelerates in the cranial
direction, ribs can move caudally about their
articulation with the spine to decrease thoracic
dorsoventral diameter ("pump handle" motion,
which is limportant during resting breathing in
humans) or they can move both caudally and
medially about their articulations with the
spine and sternum to decrease the lateral
diameter of the thorax ("bucket handle" motion,
which is important in quadrupeds). Both of these
motions produce expiratory flows. Conversely,
when the spine decelerates, ribs move cranially
or laterally to increase thoracic volume and
produce inspiratory flows. For a given direction
of acceleration, therefore, resultant rib cage
displacements generate flows in the opposite
direction relative to abdominal visceral mass
displacements (5, 13).
Spinal flexion. Flexion of the lumbar
spine tends to shorten the trunk, displacing the
abdominal viscera and diaphragm cranially, and
causes expiratory flows. Extension tends to
displace abdominal contents caudally and causes
inspiratory flows (8). This mechanism assumes
that the trunk cross-sectional area remains
relatively constant during spinal flexion and
extension, which may not be true.
Rib cage loading by foretimb.
Onimpactwith the ground, the forelimb of
quadrupeds transmits compressive forces to the
rib cage (8). The direction of respiratory flow
depends on the angle of forces relative to hinge
axes of the ribs, but it seems likely that limb
impact forces cause expiralory flow.
Common muscle link. Chest wall muscles
that function in locomotion may link breathing
to locomotor cycles. These include pectoral,
intercostal, and abdominal muscles. The pectoral
muscles are especially powerful in birds, and
their contraction might be expected to compress
the thorax and lead to expiratory flows during
wing downstroke. Activation of intercostal and
abdominal muscles in quadrupeds during
locomotion may not only stabilize the trunk or
flex the lumbosacral joint but may also cause
respiratory flows. Whether flow actually occurs,
however, will depend on what other muscles are
simultaneously activated.
Phrasing the question
Although it is evident even to the casual
observer that some respiratory flow occurs with
stride, we want to know whether the volume
displaced is large enough to be important for
breathing. We consider here quantifiable effects
that relate directly to gas-exchange parameters
(e.g., alveolar ventilation, ticial volume) and
ask, How much air does a stride (or win-beat)
move?
What volume of air is significant? Whether a
stride-induced volume change significantly
assists the respiratory muscles is most easily
assessed by comparing it with tidal volume. Much
smaller volumes at high frequencies might
significantly improve gas exchange by mixing;
the effectiveness of this action depends on the
product of volume and frequency.
Studies
Investigators disagree on how much air a
stride or wingbeat moves. Several investigators
have proposed that locornotor activity could
drive all or a substantial part of ventilation
in exercising animals (e.g., Ref. 8).
Mathematical models suggest that this is
possible in hopping or galloping animals (4).
However, actual measurements of volume change
provided by stride in trotting or galloping
animals range from 1 to 20%, of tidal volume.
Most of the measured variation is likely due to
species differences. We discuss the approaches,
techniques, and findings of various studies.
Mathematical models. Alexander (4) examined
the plausibility of three mechanical mechanisms
(visceral piston, spinal flexion, and forelimb
loading) by generatino "best case scenario"
models for a horse and wallaby. Using these
mathernatical models to calculate the maximum
ventilation that could result from various
mechanisnis, he concluded that if the natural
frequency of a visceral piston \vere tuned to
stride frequency, this mechanism could provide
the entire tidal volume in a hopping wallaby and
that spinal flexion could provide the entire
tidal volume in a galloping horse. These models
did not account for 1) acceleration of the rib
cage that would produce volume changes that tend
to negate those produced by accelerating
abdominal viscera (13) and 2) trunk
cross-sectional expansion that can accompany
spinal flexion, which would tend to negate
shortening of the trunk caused by flexion. This
latter occurs in humans (14) but has not been
examined in other animals.
Experimental techniques. To determine the
volume of air moved by stride, we desire a
measure of respiratory flow during exercise, as
well as the means to determine what part of the
respiratory signal is stride related. Although
temperature and sound variation at the nostril
or mouth can be used to infer the timing of
flow, they cannot be used to quantify volume
changes because their amplitude is not uniquely
related to flow.
Respiratory flow can be measured with a
pneumotachometer (e.g., in which flow through a
fixed-diameter tube is inferred from the
pressure drop across a known resistance or from
the cooling of a heated element). One can then
integrate the flow signal over time to determine
volume. The timing of locomotor events is
typically inferred from an accelerometer, a foot
switch, or a phototransistor that alternates
between light and dark over wingbeat or stride.
Animals have generally been studied while
running on a treadmill or flying in a wind
tunnel, but there have also been a few studies
of breathing in free running and flying
animals.
It is not always easy to entice animals to
run on treadmills or fly in wind tunnels with
natural gaits or to breathe normally through
respiratory equipment. Measuring respiration in
exercising animals also presents several
problems: for example, it is difficult to
connect measuring devices (e.g., a mask with a
pneumotachometer) to an animal; motion artifacts
may be misinterpreted as a locomotor
contribution to breathing (e.g., motion of a
mask on the face may displace air through the
pneumotachometer; many pressure transducers used
with pneumotachometers respond to acceleration,
etc.). To measure flow accurately, the mask
holding the pneumotachometer must form a good
seal. A tight-fitting mask, however, may
interfere with breathing or locomotion by
increasing the dead space and resistanceor by
impeding head motion orvision. Masks may cause
animals to breathe at slower frequencies (3) or
higher tidal volumes, Chronic tracheostomies can
provide an excellent seal without disturbing the
face and head but may also interfere with normal
breathing. Thus techniques that have been used
to measure flow may themselves affect flow.
Skill and patience are needed to find acceptable
techniques for each species.
One can infer respiratory flow and volume
with less encumbrance to the animal, but these
measures are less direct and are subject to
other artifacts. Changes in lung volume in
stationary subjects have been inferred from
changes in chest wall dimensions (via
magnetorneters, respitrace, and radiographic
reconstruction) or from changes in radiographic
densities and transmission impedance.
Stride-related artifacts, however, are likely
with these techniques, confounding any estimate
of stride-related volume change. Magnetometers
detect changes in length via the strength in
magnetic field between sender and receiver coils
on opposite sides of the trunk. Respitrace
measures changes in cross-sectional area via
changes in inductance in wire loops surrounding
the trunk. Impedance pneumography measures
changes in electrical characteristics of lung
tissue by means of external electrodes. Because
all these devices are fastened to the skin, skin
motion artifacts are problematic during
locomotion. In radiographic density
determinations of volume change, artifacts may
arise from soft tissue moving in and out of the
field of measurement. Radiographic
reconstruction of lung volume entails sometimes
difficult judgment of lung boundaries. Estimates
based on single-plane images do not account for
possible opposing changes of the third
dimension; simultaneous two- or three-plane
images have not been done in running animals,
presumably because of the difficulty and
expense.
Pleural pressure records provide information
on breathing frequency but require significant
analytic effort to extract flow or volume
estimates. Pleural pressure changes are due to
elastic, inertial, and resistive impedances; an
appropriate model incorporating A of these
impedances is required to inter volume changes
from pleural pressure.
After flow or volume records have been
acquired, how does one distinguish
locomotorrelated signals from those that are
driven by breathing muscles? When step and
breathing are not synchronous, one can estimate
the locomotor contribution from fluctuations in
the flow signal that correspond in time to step.
In some cases, these fluctuations are visible by
eye. For example, Fig. 1 shows a record of
airflow in an exercising dog; the flow
fluctuation associated with one step of the trot
is easily distinguished.
Step-related flow can be quantified more
rigorously by ensemble averaging the flow
signals recorded during many steps. A trigger
point is selected from each cycle of the
locomotor signal. The trigger points of many
step cycles are then aligned on the same time
axis, superimposing their corresponding flow
records. When the flow records are averaged,
they produce a trace that represents flow during
an average step cycle. if steps are uniformly
distributed throughout breathing cycles, then
flows due to the act of breathing will average
zero. If we assume that the mechanical effects
of stride events add linearly to the effects of
respiratory muscles, we may regard the residual
ensemble-averaged flow as an estimate of
step-related flow. if steps are not uniformly
distributed, the resulting average flow record
is biased and may overestimate stride
contribution. If the effects do not add linearly
(e.g., if stride systematically changes
respiratory muscle activation), the resulting
average flow record may either overestimate or
underestimate stride contribution.
Experimental results. Locomotor contribution
to tidal volume. Several studies have reported
flow measured at the airway opening during
locomotion. Ensemble averaging shows that the
locomotor-related contribution is <20% of the
tidal volume. In starlings, although strong
coupling might be expected because the
pectoralis muscles insert on the sternum and
exert force during wing downstrokes, wingbeat
accounted for 3-11 % of the tidal volume (6).
Similar results were also found in quadrupeds.
ln galloping horses, the step-related volume
change \vas <20% of tidal Volume (12). In
trotting dogs, it was 3-16% (7), consistent with
data of Ainsworth and co-workers shown in Fig.
1. In hunians, whose bipedal posture and gait
are expected to be associated with a greater
mechanical independence (8), the mechanical
contribution of stride to tidal volume during
walking and running was 1-2% (5). In addition to
these estimates of the total locomotor
contribution to tidal volume, the contributions
of various proposed mechanisms have been
evaluated qualitatively in several studies and
are summarized below.
Viscfral piston. Bramble and Jenkins (9)
compared flows measured with a pneumotachometer
in an intentionally loosely fitted mask with a
two-dimensional cineradiographic analysis of
diaphragm volume displacement and concluded that
inertial displacements of the visceral piston
appeared to be the primary driver of diaphragm
displacement in trotting dogs. Young et al. (15)
measured tidal volume with a
pneumotachometer-mask combination and trunk
accelerations from high-speed films and
concluded that the inertially driven visceral
piston could not be driving breathing because
the phase relationship between volume and
acceleration was not appropriate. Ainsworth and
co-workers found that during every breath cycle,
inspiratory swings in transdiaphragmatic
pressure corresponded with phasic diaphragmatic
electromyogram activity in trotting dogs (3), as
well as trotting and galloping horses (2), and
thus concluded that inspiratory motions of the
diaphragm resulted from muscle contraction
rather than from inertial forces.
Spinal flexion. Young and co-workers (15)
used a model that incorporated trunk shortening
(but not cross-sectional changes) to compare
lumbosacral flexion mesured from cinefilms with
tidal volume. They concluded that, at speeds of
9 m/s, spinal flexion in galloping horses was of
the proper magnitude and phase to drive i
substantiai part of tidal volume.
Forelimb Bramble and Jenkins (9) observed,
via two-dimensional cineradiography, that
loading by forelimbs produced prominent
unilateral inward deformation of the rib cage in
the region of limb articulation in trotting
dogs. Although they did not assess the effect of
this compression on lung volume, the deformation
appears large enough to cause an appreciable
expiratory effect.
Common muscle links. Several respiratory
muscles (e.g., interosseous intercostal and
abdominal muscles) also have locomotor
functions, inferred from correlation of their
phasic electromyogram activity with the
locomotor cycle when breathing and locomotion
were uncoupied in trotting dogs (3, 11). One
cannot deduce the mechanical effect of a muscle
on the respiratory system from measures of
electrical activity; therefore, the
effectiveness of this link has yet to be
assessed.
Perspectives
Because structures of the chest wall serve
both respiratory and locomotor functions,
opportunities exist for both conflict and
cooperation. These opportunities may constrain
both processes. Such functional constraints are
especially apparent in the lizardIguana iguana,
which actually reduces lung ventilation at high
locomotor speeds (10). The evolution of proper
neurological coordination was apparently
necessary to enable animals to breathe
effectively while running or flying. In
addition, mechanical linkages may have also
facilitated a recluced cost or a higher level of
performance of one or both of these
functions.
How much energy could be saved by mechanical
links between locomotion and breathing? During
sustainable levels of aerobic exercise (e.g.,
trot or slow gallop), ventilation consumes only
5% of the total energy budget, and the required
ventilation is well within the capacity of the
respiratory muscles. Measurements of respiratory
volume associated with stride suggest that less
than one-fifth of the work of breathing can be
provided by locomotor muscles, yielding <1%
net energy savings. On the other hand, a few
animals encounter limitation of ventilatory
capacity during heavy exercise, resulting in
arterial oxygen desaturation; in these animals,
a 20% increase in ventilatory capacity could be
quite important in increasing performance, even
if it bas little effect on overall
efficiency.
References
