J Appl Physiol 107: 1736–1742, 2009.
First published October 1, 2009; doi:10.1152/japplphysiol.00753.2009.
Mechanisms of the inspiratory action of the diaphragm during isolated
contraction
André De Troyer,1,2 Dimitri Leduc,1,2 Matteo Cappello,1,2 Benjamin Mine,3 Pierre Alain Gevenois,3
and Theodore A. Wilson4
1
Laboratory of Cardiorespiratory Physiology, Brussels School of Medicine; 2Chest Service and 3Department of Radiology,
Erasme University Hospital, Brussels, Belgium; and 4Department of Aerospace Engineering and Mechanics, University
of Minnesota, Minneapolis, Minnesota
Submitted 14 July 2009; accepted in final form 30 September 2009
respiratory muscles; chest wall mechanics; action of diaphragm
of the diaphragm is to lower pleural
pressure (Ppl) and to inflate the lung, and a number of studies,
beginning with the work of Marshall (18) in 1962, have clearly
established that this function is altered by changes in lung
volume. Specifically, when the airways in animals (6, 12, 14,
15, 18 –21) and in humans (4, 23) are occluded and the
diaphragm is selectively activated by stimulation of the phrenic
nerves, the change in pleural (⌬Ppl) or airway opening pressure (⌬Pao) that occurs during stimulation decreases progressively as lung volume prior to stimulation increases. Near total
lung capacity (TLC), the lung-expanding action of the diaphragm is, in fact, almost zero.
To the extent that the diaphragm is conventionally pictured as a piston, the lung-expanding action of the muscle is
THE PRIMARY FUNCTION
Address for reprint requests and other correspondence: A. De Troyer, Chest
Service, Erasme Univ. Hospital, 808, Route de Lennik, 1070 Brussels, Belgium (e-mail: [email protected]).
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considered to be the result of the shortening of the muscle
fibers. Thus, as the muscle fibers of the diaphragm contract
and shorten, the dome of the muscle descends and Ppl falls.
Also, when lung volume increases above functional residual
capacity (FRC), the length of the muscle during relaxation
decreases (13, 14, 24). The length of the muscle during
phrenic nerve stimulation also decreases with increasing
lung volume, but the magnitude of this decrease is much
smaller than that during relaxation (14). As lung volume
increases, therefore, the amount of diaphragm shortening
produced by a given muscle activation decreases markedly,
in agreement with the large decrease in ⌬Ppl.
Recent studies of the effects of ascites on the canine diaphragm, however, have suggested that the ⌬Ppl generated by
diaphragm contraction may involve a mechanism other than
muscle shortening. Thus using computed tomography (CT) to
measure diaphragm length, Leduc et al. (16) showed that
isolated stimulation of the phrenic nerves at FRC produced not
only a large muscle shortening with a large descent of the
dome, but also a caudal displacement of the muscle insertions
into the lower ribs. Isolated, supramaximal phrenic nerve
stimulation in dogs with the airway open also displaces the
lower ribs in the caudal direction (9). As Leduc et al. (16)
pointed out, the change in diaphragm length is, as a first
approximation, proportional to the relative displacement of the
dome and the muscle insertions into the ribs. On this basis, one
would therefore expect that for a given muscle shortening, the
descent of the dome would be larger if the muscle insertions
into the ribs move caudally than it would if these insertions did
not move. In other words, the caudal displacement of the lower
ribs during isolated phrenic nerve stimulation would add to the
muscle shortening to enhance the caudal displacement of the
dome and, with it, ⌬Ppl.
The objective of the present study was to assess the role of
the lower rib displacement in determining the lung-expanding
action of the diaphragm and to evaluate the volume-dependence of this role. Radiopaque markers were attached along
muscle bundles in the midcostal region of the muscle in dogs,
the animals were placed in a CT scanner, and the phrenic
nerves were stimulated at different lung volumes. Consequently, accurate measurements of muscle length, dome displacement, and lower rib displacement were obtained, and the
pressure changes recorded during stimulation were analyzed as
functions of muscle length and displacement. From this analysis, the relative contributions of muscle shortening and rib
displacement to ⌬Ppl at different lung volumes could therefore
be estimated.
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De Troyer A, Leduc D, Cappello M, Mine B, Gevenois PA,
Wilson TA. Mechanisms of the inspiratory action of the diaphragm
during isolated contraction. J Appl Physiol 107: 1736 –1742, 2009. First
published October 1, 2009; doi:10.1152/japplphysiol.00753.2009.—
The lung-expanding action of the diaphragm is primarily related to the
descent of the dome produced by the shortening of the muscle fibers.
However, when the phrenic nerves in dogs are selectively stimulated
at functional residual capacity, the muscle insertions into the lower ribs also
move caudally. This rib motion should enhance the descent of the dome
and increase the fall in pleural pressure (⌬Ppl). To quantify the role of
this mechanism in determining ⌬Ppl during isolated diaphragm contraction and to evaluate the volume dependence of this role, radiopaque markers were attached to muscle bundles in the midcostal
region of the muscle in six animals, and the three-dimensional
location of the markers during relaxation at different lung volumes and
during phrenic nerve stimulation at the same lung volumes was measured
using computed tomography. From these data, accurate measurements of
muscle length, dome displacement, and lower rib displacement were
obtained. The values of dome displacement were then corrected for lower
rib displacement, and the values of ⌬Ppl corresponding to the corrected
dome displacements were obtained using the measured relationship
between ⌬Ppl and dome displacement. The measurements showed
that phrenic stimulation at all lung volumes causes a caudal displacement of the lower ribs and that this displacement, taken alone,
contributes ⬃25% of the ⌬Ppl produced by the diaphragm. To the
extent that this lower rib displacement is itself caused by ⌬Ppl, the
lung-expanding action of the diaphragm during isolated contraction
may therefore be viewed as a self-facilitating phenomenon.
MECHANISMS OF THE INSPIRATORY ACTION OF THE DIAPHRAGM
METHODS
J Appl Physiol • VOL
were studied to assess directly the effects of passive inflation and
phrenic nerve stimulation on the axial displacement of the ribs into
which the diaphragm inserts.
After the phrenic nerve roots were isolated in the neck, the rib cage
in each animal was exposed on the right side of the chest from the
second to eleventh rib by reflection of the skin and the superficial
muscle layers. A hook was screwed into the tenth rib in the anterior
axillary line, 3– 4 cm dorsal to the costo-chondral junction, and
connected to a linear displacement transducer (Schaevitz Engineering,
Pennsauken, NJ) to measure the craniocaudal (axial) rib displacement
(Xr), as previously described (7). Measurements of Xr, together with
Pao and Pab, were obtained first during a series of passive inflations
ranging from 0 to 30 cmH2O transrespiratory pressure, then during
phrenic nerve stimulation at FRC and at different lung volumes above
FRC. All stimulations were also performed while the endotracheal
tube was occluded.
The animals in both experiments were maintained at a constant,
rather deep level of anesthesia throughout the study. Thus, at no time
in the experiment, did they have a corneal reflex or movements of the
fore- or hindlimbs. Rectal temperature was maintained constant between 36 and 38°C with infrared lamps. At the conclusion of the
experiment, the animal was given an overdose of anesthetic (30 – 40
mg/kg iv). In three animals, careful postmortem examination of the
diaphragm insertions into the ribs was performed to define the nature
of the white band, and large samples of the area were taken. The
samples were fixed, embedded in paraffin, sliced in 10-␮m sections,
trichrome stained, and mounted for microscopic examination.
Data analysis. The CT data were analyzed as previously outlined
(16). Thus for each lung volume in each animal, 1.25-mm-thick
transverse CT sections during relaxation and during phrenic nerve
stimulation were reconstructed at 1.0-mm intervals by using a 360°
linear-interpolation algorithm and a standard kernel (AB 40f, Siemens
Medical Solutions). Sagittal and coronal images were also reconstructed, and these multiplanar reformations were then used in a
workstation (Leonardo, Siemens Medical Solutions) to define the
three-dimensional coordinates of each diaphragm marker in each
condition and to measure the length of each hemidiaphragm. By
convention, the coordinates of the different markers along the craniocaudal axis were expressed in millimeters relative to the position of
the lowest markers during relaxation at FRC; a positive sign indicates
a more cranial position, and a negative sign indicates a more caudal
position. The length of the muscle was also expressed in millimeters.
To allow comparison between the different animals, however, muscle
lengths during relaxation and during phrenic nerve stimulation at the
different lung volumes were then expressed as percentages of muscle
length during relaxation at FRC (LFRC).
The CT images were also used to measure the axial displacements
of the rib that was nearest the lower diaphragm markers at FRC and
to compare these displacements with those of the markers themselves.
Because no material point on the bony rib could be readily identified,
the analysis focused on the costo-chondral junction of rib 9. Thus the
(stationary) transverse plane going through the cranial edge of the
spinous process of T10 was defined, and for each hemidiaphragm in
each condition, the axial coordinates of both the lower diaphragm
marker and the cranial edge of the costo-chondral junction were
measured relative to that plane.
Statistical analysis. There were no consistent interhemidiaphragmatic differences in the positions of the markers situated near the
central tendon and of those situated near the muscle insertions into the
ribs (Expt. 1). Also there were no consistent differences in length
between the right and left hemidiaphragms and no differences between the positions of the right and left costo-chondral junctions of rib
9. For each condition, therefore, the values for the two sides were
averaged for each individual animal, and they were then averaged
across the animal group. The values of ⌬Pao and ⌬Pab recorded
during phrenic nerve stimulation at the different lung volumes were
also averaged across the animal group and they are presented as
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The studies were carried out on nine adult bred-for-research golden
retrievers (18 –22 kg) anesthetized with pentobarbital sodium (initial
dose, 30 mg/kg iv), as approved by the Animal Ethics and Welfare
Committee of the Brussels School of Medicine. The animals were
placed in the supine position, intubated with a cuffed endotracheal
tube, and connected to a mechanical ventilator (Harvard Pump,
Chicago, IL). A venous cannula was inserted in the forelimb to give
maintenance doses of anesthetic, after which the C5 and C6 phrenic
nerve roots were isolated bilaterally in the neck. Two experimental
protocols were then followed.
Experiment 1. Six animals were studied first to define the change in
diaphragm length, the displacement of the muscle, and the pressure
generated by the muscle during phrenic nerve stimulation at different
lung volumes. Thus, after the phrenic nerves were isolated, the
abdomen was opened by a midline incision from the xiphisternum to
the umbilicus and rows of five polyethylene spheres were stitched
superficially to a muscle bundle in the midcostal region of both the left
and the right hemidiaphragm. The details of the technique have been
previously reported (16), but it should be emphasized that placement
of the lowest marker in each row was made as described by Boriek et
al. (1, 2) and Wilson et al. (25), i.e., at the cranial edge of the band of
light-colored tissue situated at the junction between the caudal extremity of the diaphragmatic fibers and the fibers of the transversus
abdominis at their insertions into the ribs; this band of light-colored
tissue will be referred to as “the white band” throughout the manuscript. After the placement of the markers was completed, a ballooncatheter system filled with 1.0 ml of air was positioned between the
liver and the stomach to measure abdominal pressure (Pab), and the
abdomen was closely sutured in two layers.
The animal was given a 30-min recovery period, after which it was
transferred to a V-shaped board and placed in a four-channel multidetector CT scanner (Somatom Volume Zoom 4, Siemens Medical
Solutions, Forchheim, Germany). The C5 and C6 phrenic nerve roots
were laid over two pairs of insulated stainless steel stimulating
electrodes, and a differential pressure transducer (Validyne,
Northridge, CA) was connected to a side port of the endotracheal tube
to measure ⌬Pao. The animal was then made apneic by mechanical
hyperventilation, and a first helical data acquisition starting ⬃2 cm
caudal to the lower rib cage margin and extending to ⬃2 cm cranial
to the xiphoid process was performed during relaxation at FRC. The
scanning parameters were similar to those used in our previous study
(16): 120 kV, 120 effective mA, 0.5 s/revolution scanning time, 1-mm
collimation, and 6.9 mm feed/rotation. After the animal was hyperventilated again, the respiratory system was passively inflated to a
transrespiratory pressure of ⬃7.5 cmH2O (mean ⫾ SE: 7.8 ⫾ 0.3
cmH2O), the endotracheal tube was occluded, and a second CT data
acquisition was obtained. Lung volume was subsequently increased to
⬃15 (mean ⫾ SE: 14.9 ⫾ 0.2), 22 (22.1 ⫾ 0.3), and 30 (29.9 ⫾ 0.3)
cmH2O transrespiratory pressure, and a CT acquisition was obtained
at each lung volume. After completion of this procedure, the endotracheal tube was occluded at FRC, and square pulses of 0.1-ms
duration and supramaximal voltage were applied at a frequency of 20
impulses/s to the left and right phrenic nerve roots simultaneously. A
new CT data acquisition, together with the ⌬Pao and ⌬Pab generated
by the stimulation, was obtained at this time. Phrenic nerve stimulation was then repeated after lung volume was passively increased to
⬃7.5, 15, 22, and 30 cmH2O transrespiratory pressure. As was the
case at FRC, all stimulations were performed while the animal was
apneic and the endotracheal tube was occluded.
Experiment 2. Although the lowest diaphragm markers in Expt. 1
were placed in the vicinity of the muscle insertions into the ribs, their
displacement during passive inflation, as seen on CT, was inconsistent
with both earlier observations of rib motion in dogs (17) and the
known mechanical coupling between the lower ribs and the lung (8,
10) (see RESULTS). In a second experiment, therefore, three animals
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MECHANISMS OF THE INSPIRATORY ACTION OF THE DIAPHRAGM
means ⫾ SE. Statistical assessments of the effect of increasing lung
volume on pressure, marker position, muscle length, and costochondral junction position were made by ANOVA with repeated
measures, and multiple comparison testing of the mean values was
performed, when appropriate, using Student-Newman-Keuls tests.
The criterion for statistical significance was taken as P ⬍ 0.05.
As in Expt. 1, the axial position of rib 10 during passive inflation
and during phrenic nerve stimulation at each lung volume in each
animal of Expt. 2 was measured relative to the position of the rib
during relaxation at FRC, and the values obtained at the different lung
volumes were plotted against the value of Pao before phrenic stimulation (i.e., the precontractile transrespiratory pressure). The relationships were then fitted by quadratic equations, and rib positions at fixed
transrespiratory pressures at 7.5 cmH2O increments were determined
from these equations. The values were also averaged across the animal
group, and they are also presented as means ⫾ SE.
RESULTS
Fig. 1. Changes in airway opening pressure (⌬Pao) and abdominal pressure
(⌬Pab) during bilateral stimulation of the C5 and C6 phrenic nerve roots at
different lung volumes. Values are means ⫾ SE obtained from 6 animals.
J Appl Physiol • VOL
Fig. 2. Anterior-posterior view of marker locations in the right and left
hemidiaphragms obtained for a representative animal during relaxation at
functional residual capacity (FRC) (F) and 30 cmH2O transrespiratory pressure
(E), and during phrenic nerve stimulation at the same lung volumes (Œ and ‚,
respectively). The x-axis lies in the laterolateral direction, and the z-axis lies in
the craniocaudal direction. Note the caudal displacement of the relaxed
diaphragm dome at high lung volume and the caudal displacement of the
markers situated near the muscle insertions into the ribs. During phrenic nerve
stimulation, the muscle fibers shortened and the diaphragm dome moved caudally,
more markedly so at FRC than at 30 cmH2O transrespiratory pressure.
as lung volume increased (P ⬍ 0.001). The markers situated
near the muscle insertions into the ribs were also displaced in
the caudal direction (P ⬍ 0.001). This displacement, however,
was much smaller in magnitude than that of the central tendon.
Fig. 3. Axial position of the diaphragm markers situated near the central tendon
(squares) and those situated near the muscle insertions into the ribs (circles) during
relaxation (open symbols) and during phrenic nerve stimulation (filled symbols) at
different lung volumes. Values are means ⫾ SE obtained from 6 animals. The markers
positions are expressed relative to the position of the lower markers during relaxation
at FRC; positive values indicate cranial position.
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Pressure. The pressure changes measured during phrenic
nerve stimulation at different lung volumes in the six animals
of Expt. 1 are shown in Fig. 1. As lung volume increased, ⌬Pao
decreased markedly and progressively (P ⬍ 0.001), so that at
30.5 cmH2O transrespiratory pressure, it was only 8.8 ⫾ 1.0%
of the value at FRC. The rise in Pab during stimulation also
decreased progressively with increasing lung volume (P ⬍
0.001).
Position and length of the diaphragm. The anterior-posterior
view of the diaphragm markers during relaxation at FRC and at
30 cmH2O transrespiratory pressure and during phrenic nerve
stimulation at the same lung volumes is shown for a representative animal in Fig. 2, and the axial position of the markers
situated near the central tendon and near the muscle insertions
into the ribs in the six animals at all lung volumes is shown in
Fig. 3. With the animal relaxed, the markers situated near the
central tendon were gradually displaced in the caudal direction
MECHANISMS OF THE INSPIRATORY ACTION OF THE DIAPHRAGM
With increasing volume, therefore, the muscle fibers shortened
progressively (P ⬍ 0.001), and at 30 cmH2O transrespiratory
pressure, their length was 64.0 ⫾ 2.6% of LFRC (Fig. 4).
Phrenic nerve stimulation at FRC caused a large caudal
displacement of the central tendon and a smaller caudal displacement of the markers near the muscle insertions, so that the
muscle fibers shortened to 60.2 ⫾ 1.8% of LFRC. As lung
volume increased, however, the caudal displacement of the
central tendon during stimulation decreased gradually in magnitude (P ⬍ 0.001). The caudal displacement of the markers
near the muscle insertions also decreased, and during stimulation at high lung volumes, it was even reversed into a small
cranial displacement (Fig. 3). As a result, in agreement with the
previous observation of Hubmayr et al. (14), the amount of
muscle shortening decreased (P ⬍ 0.001) and muscle length
during stimulation decreased as well (P ⬍ 0.001). During
stimulation at 30.5 cmH2O transrespiratory pressure, muscle
length was only 51.4 ⫾ 2.1% of LFRC (Fig. 4).
Relationships between the pressure changes and dome displacement. The values of ⌬Pao obtained during phrenic stimulation at the different lung volumes are plotted against the
corresponding values of dome displacement in Fig. 5A. The
relationship between ⌬Pao and dome displacement was curvilinear, such that for a given displacement, ⌬Pao was greatest at
FRC and decreased gradually with increasing lung volume.
This result is fully consistent with the fact that in the dog, the
rib cage is stiffer at low lung volumes and becomes more
compliant as lung volume increases above FRC (3, 5). The
relationship between ⌬Pab and dome displacement was also
slightly curvilinear (Fig. 5B).
Displacement of the lower diaphragm markers vs. the costochondral junctions. The axial position of the costo-chondral
junction of rib 9 during passive inflation and during phrenic
nerve stimulation at the different lung volumes is compared
with the position of the lower diaphragm markers in Fig. 6.
There were marked differences between the two structures.
During passive inflation, whereas the lower diaphragm markers
moved gradually in the caudal direction with increasing lung
volume, the costo-chondral junctions moved in the cranial
direction in every animal (P ⬍ 0.001). Also, whereas the lower
markers moved cranially during stimulation at high lung volumes relative to their position during relaxation at the same
lung volumes, the costo-chondral junctions moved caudally
during stimulation at all lung volumes. The magnitude of this
caudal displacement, however, decreased gradually as lung
volume increased (P ⬍ 0.001).
Axial displacement of the lower ribs. During passive inflation, the three animals of Expt. 2 showed a progressive cranial
displacement of rib 10 as lung volume increased (Fig. 7). Also,
phrenic stimulation at all lung volumes caused the rib to move
caudally relative to its relaxed position, although the magnitude of this caudal displacement decreased with increasing
lung volume; this displacement was 7.0 ⫾ 2.7 mm at FRC, but
at 30 cmH2O transrespiratory pressure, it was only 2.2 ⫾ 1.0
mm. ⌬Pao during phrenic stimulation in these animals also
decreased progressively as lung volume increased, such that at
30 cmH2O transrespiratory pressure it was 8.7 ⫾ 1.5% of the
value at FRC.
Fig. 5. Relationships between ⌬Pao and the
displacement of the diaphragm dome (A) and
between ⌬Pab and the displacement of the
dome (B) during phrenic nerve stimulation at
different lung volumes. Values are mean ⫾
SE obtained from 6 animals. The relationship
in A is much steeper at low than at high lung
volumes.
J Appl Physiol • VOL
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Fig. 4. Diaphragm muscle length during relaxation (E) and during phrenic
nerve stimulation (F) at different lung volumes. Values are means ⫾ SE
obtained from 6 animals. All values are expressed as percentages of muscle
length during relaxation at FRC (LFRC). Note the decrease in passive and active
muscle length with increasing lung volume. Note also the gradual decrease in
muscle shortening.
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MECHANISMS OF THE INSPIRATORY ACTION OF THE DIAPHRAGM
Nature of the white band. Inspection of the diaphragm
insertions into the ribs indicated that the white band is essentially a thickening of the peritoneum covering both the caudal
extremity of the diaphragmatic muscle fibers and the costal
insertions of the transversus abdominis. The cranial edge of the
band, in fact, was 10 –15 mm cranial to the actual diaphragm
insertions into the ribs. On microscopic examination, the band
consisted only of adipose tissue.
DISCUSSION
In agreement with our recent observation (16), phrenic nerve
stimulation at FRC induced a large caudal displacement of the
lower diaphragm markers in every animal of the study (Figs. 2
and 3). In addition, the caudal displacement of the markers
during stimulation decreased progressively with increasing
lung volume and was eventually reversed into a cranial displacement as lung volume approached TLC (Fig. 3). As Leduc
et al. (16) pointed out, a given diaphragm shortening should
produce a larger descent of the dome if the muscle insertions
into the ribs move caudally than it would if these insertions did
not move. Consequently, a given muscle shortening should
produce a larger ⌬Ppl in the first instance than in the second.
On the basis of the observed displacement of the lower diaphragm markers at the different lung volumes, it was therefore
tempting to conclude that the displacement of the lower ribs
during isolated diaphragm contraction at low lung volumes
makes a significant contribution to the ⌬Ppl generated by the
muscle, and also that the adverse effect of increasing lung
volume on ⌬Ppl is, in part, the result of the change in lower rib
displacement.
J Appl Physiol • VOL
Fig. 7. Mean ⫾ SE values obtained from 3 animals of the axial position of rib
10 during relaxation (E) and during phrenic nerve stimulation (F) at different
lung volumes. These values were obtained from direct measurements of axial
rib motion, and they are expressed relative to the position of the rib during
relaxation at FRC.
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Fig. 6. Comparison between the axial position of the diaphragm marker
situated near the muscle insertions into the ribs (circles; same data as in Fig.
3) and the position of the costo-chondral junction of rib 9 (triangles) during
relaxation (open symbols) and during phrenic nerve stimulation (filled symbols) at different lung volumes. Values are means ⫾ SE obtained from 6
animals by using CT images. All values are expressed relative to the position
of the diaphragm marker during relaxation at FRC; positive values indicate
cranial position and negative values indicate caudal position.
Displacement of the lower ribs. As shown in Fig. 3, however, the lower diaphragm markers also moved caudally during
passive inflation, and although this finding was similar to
previous findings by Boriek et al. (1, 2) and Wilson et al. (25),
it was in opposition with the study of the kinematics of the ribs
in dogs by Margulies et al. (17). Thus, using the dynamic
spatial reconstructor (DSR), these investigators reported that in
supine animals, the ribs 3 to 8 move cranially during passive
inflation. Therefore, although the measurements in that study
did not extend caudally beyond the eighth rib, the possibility
that ribs 9 and 10 (i.e., the ribs into which the diaphragm
inserts) would concomitantly move in the caudal direction
appeared unlikely. Moreover, in our previous evaluation of the
mechanical coupling between the ribs and the lung in dogs (8,
10), we found that applying external loads to ribs 9 and 10 in
the cranial direction causes both a cranial rib displacement and
a fall in Pao; according to Maxwell’s reciprocity theorem,
therefore, the rise in Pao during passive inflation should cause
a cranial, rather than caudal motion of the lower ribs (25). On
the basis of these studies, we therefore suspected that the lower
diaphragm markers were, in fact, cranial relative to the muscle
insertions into the ribs and, hence, that the displacement of
these markers did not reflect the displacement of the ribs.
To define the displacement of the actual diaphragm insertions into the ribs, we reanalyzed the CT images and monitored
the costo-chondral junction of rib 9. The junction moved
cranially, rather than caudally during passive inflation in each
animal (Fig. 6), in agreement with the observations by Margulies et al. (17). Also, because this junction might not be
representative of the entire ring of insertion of the diaphragm
into the lower ribs, in a second set of experiments on three
animals, we measured directly the displacement of rib 10 in
the anterior axillary line (i.e., at a material point on the bony
rib), and these measurements confirmed that passive inflation
causes a cranial displacement of the ribs into which the
diaphragm inserts (Fig. 7). The confirmation was not only
qualitative but also quantitative; in both experiments, the
cranial rib displacement was ⬃10 mm as lung volume was
MECHANISMS OF THE INSPIRATORY ACTION OF THE DIAPHRAGM
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Fig. 8. A: computed effects of the caudal
displacement of the lower ribs on ⌬Pao. F
and continuous line, mean values of ⌬Pao
and dome displacement obtained from 6 animals during phrenic nerve stimulation at
different lung volumes (same data as Fig.
5A); E, computed values. B: comparison between the measured (F, shown in Fig. 1) and
the computed (E) values of ⌬Pao and ⌬Pab at
different lung volumes. The computed ⌬Pao
values are 20 –30% smaller than the measured values, and the computed ⌬Pab values
are 15–20% smaller.
J Appl Physiol • VOL
nearly the same at all lung volumes, including at TLC. In other
words, the caudal displacement of the lower ribs caused by
isolated diaphragm contraction would account for about a
quarter of the ⌬Pao generated by the muscle. The computed
values for dome displacement, combined with the measured
relationship between ⌬Pab and dome displacement (Fig. 5B),
similarly lead to the conclusion that the lower rib displacement
would also account for 15–20% of ⌬Pab (Fig. 8B). Thus, if the
Fig. 9. Graphical analysis of the compensatory effect on the diaphragm of a 25%
reduction in ⌬Pdi. F, mean values of Pdi (expressed as cmH2O) and muscle length
(expressed as percentages of muscle length during relaxation at FRC, LFRC) obtained
from the 6 animals of the study during relaxation at different lung volumes between
FRC and TLC and during phrenic nerve stimulation at the same lung volumes (SE not
shown for the sake of clarity). The thick continuous lines, therefore, are the passive and
active Pdi-length relationships. The thin continuous line is the load line describing the
load imposed by the lung and chest wall on the diaphragm during isolated contraction
at 7.5 cmH2O transrespiratory pressure; this load line intersects the passive and active
Pdi-length curves at the observed values of muscle length and Pdi. The dashed line is
the load line describing the load that would be imposed on the diaphragm at the same
lung volume if ⌬Pdi decreased by 25%, and 䊐 square corresponds to the equilibrium
position that the diaphragm would adopt in this condition. See Compensation for the
reduction in ⌬Pdi for further explanation.
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passively increased from 0 to 30 cmH2O. These results therefore implied that the lower diaphragm markers did not correspond to the muscle insertions into the ribs, and indeed anatomical and histological examination of the area showed that
the white band is simply a local, fatty thickening of the parietal
peritoneum that covers the caudal portion of the diaphragm
muscle fibers. As a corollary, the displacement of the lower
diaphragm markers during phrenic stimulation could not be
used to quantify the role played by the axial displacement of
the lower ribs in causing the descent of the dome and ⌬Pao.
Contribution of the lower rib displacement to ⌬Pao. As
shown by both the CT-based measurements of the position of
the costo-chondral junction (Fig. 6) and the direct measurements of rib motion (Fig. 7), phrenic stimulation at FRC
produced a large caudal displacement of the diaphragm insertions into the ribs. Indeed, such stimulation causes large shortening of the diaphragm muscle fibers so that the zone of
apposition of the diaphragm to the lower rib cage (19) decreases markedly. As a result, most of the lower rib cage is
exposed to the expiratory effect of Ppl, rather than the inspiratory effect of Pab. Also, both the CT-based measurements (Fig.
6) and the direct measurements of rib motion (Fig. 7) showed
that the caudal displacement of the diaphragm insertions into
the ribs decreased, together with ⌬Ppl, with increasing lung
volume. To compute the contribution of the lower rib displacement to ⌬Pao, therefore, we first subtracted, for each lung
volume, the displacement of the costo-chondral junction during
stimulation from the observed displacement of the dome. In so
doing, we thus obtained the displacement of the dome that
would be produced by muscle shortening if the lower ribs did
not move. Then, in a second step, we used the relationship
between ⌬Pao and dome displacement (shown in Fig. 5A) to
determine the values of ⌬Pao corresponding to the calculated
dome displacements.
This analysis is illustrated in Fig. 8A, and the ⌬Pao values
computed for the different lung volumes (open circles) are
compared with the measured values (closed circles) in Fig. 8B.
The computed ⌬Pao value at FRC was 27% smaller than the
measured value. Furthermore, the relative pressure loss was
1742
MECHANISMS OF THE INSPIRATORY ACTION OF THE DIAPHRAGM
J Appl Physiol • VOL
may therefore be viewed as a self-facilitating phenomenon. That
is, shortening of the diaphragm during contraction generates a fall
in Ppl through the descent of the dome, and this pressure fall, by
displacing the lower ribs caudally, enhances the descent of the
dome and accentuates ⌬Ppl.
ACKNOWLEDGMENTS
The authors are grateful to M. Rooze (Laboratory of Functional Anatomy,
Brussels School of Medicine) for performing the microscopic examination of
the “white band.”
GRANTS
This work was supported by the Fonds National de la Recherche Scientifique (FNRS, Belgium) Grant 3.4558.06F.
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lower ribs were stationary, ⌬Pdi would be reduced by 20 –
25%. With such a reduction in ⌬Pdi, however, it would be
expected that some compensation would take place.
Compensation for the reduction in ⌬Pdi. As the muscle
fibers of the diaphragm contract and shorten, the dome descends, Ppl falls and Pab rises. At equilibrium, the force
generated by the muscle must balance the load imposed on the
muscle by the pressure difference across it. Consequently, if
the suppression of the lower rib displacement caused a 25%
reduction in ⌬Pdi, the amount of diaphragm shortening that
would occur in response to a given muscle activation would be
greater, and this greater shortening would compensate, at least
in part, for the reduction in Pdi.
The quantitative effect of a 25% reduction in ⌬Pdi on
muscle shortening and pressure can be evaluated by using the
Pdi-length diagram shown in Fig. 9. The closed circles in the
figure are the values of Pdi plotted against the corresponding
values of muscle length (shown in Fig. 4) obtained in our
animals during relaxation at the different lung volumes and
during phrenic nerve stimulation at the same lung volumes.
The thick continuous lines connecting these data points, therefore, represent the passive and active Pdi-length curves, respectively. When the diaphragm contracts at a particular lung
volume, it thus “moves” from its relaxed, passive state to its
active state by following a line that corresponds to the load
imposed on the muscle by Ppl and Pab. This line has been
called the “load line” (6, 11), and it intersects the active
Pdi-length curve at the observed values of muscle length and
Pdi. The thin continuous line in Fig. 9 is, as an example, the
load line corresponding to a volume of 7.5 cmH2O transrespiratory pressure; when the phrenic nerves in our animals were
stimulated at this lung volume, muscle length at equilibrium
was 57.6% of LFRC and Pdi was 39.0 cmH2O.
The effect of a 25% reduction in ⌬Pdi at this particular lung
volume can now be obtained by the following two-step procedure. First, active diaphragm length is imagined to be fixed as
⌬Pdi is reduced by 25% relative to the measured value; the
new Pdi (30.5 cmH2O) is shown by the open circle in Fig. 9.
In the second step, diaphragm length is imagined to be released
from this state to reach its equilibrium position. This is given
by the intersection of the new load line (dashed line) with the
active Pdi-length curve. The intersection, represented by the
open square, thus corresponds to the equilibrium position that
the diaphragm would adopt if the load imposed on the muscle
was reduced by 25%. It can be seen that the muscle in this
position would be shorter than the measured value and that Pdi
would be larger. However, because the active Pdi-length curve,
as previously reported by Hubmayr et al. (14), is very steep in
this range of muscle length, the difference in Pdi would be only
1 cmH2O. Very small increases in pressure were also obtained
at the other lung volumes.
In conclusion, the primary result of the present study is the
demonstration that the lung-expanding action of the diaphragm
during isolated contraction results not only from the shortening of
the muscle fibers but also from the caudal displacement of the
lower ribs. This caudal rib displacement is accompanied by an
inward displacement, which may affect diaphragm action as well.
However, the caudal displacement, taken alone, contributes nearly
a quarter of the total ⌬Ppl generated by the diaphragm at all lung
volumes. To the extent that this rib displacement is itself produced
primarily by ⌬Ppl, the lung-expanding action of the diaphragm