J Appl Physiol 107: 741–748, 2009.
First published July 16, 2009; doi:10.1152/japplphysiol.91320.2008.
Neuromechanical matching of drive in the scalene muscle
of the anesthetized rabbit
Alexandre Legrand,1 Melanie Majcher,1 Emma Joly,1 Adeline Bonaert,1 and Pierre Alain Gevenois2
1
Department of Physiology and Pharmacology, University of Mons, Mons, Belgium; and 2Department of Radiology, Erasme
University Hospital, Université Libre de Bruxelles, Brussels, Belgium
Submitted 1 October 2008; accepted in final form 10 July 2009
electromyographic activity; neck muscle; mechanics of breathing
THE SCALENE MUSCLE IS GENERALLY considered a primary respiratory muscle in humans. EMG studies in normal subjects have
indeed shown that the scalene muscle is consistently active
during eupneic breathing, even when the tidal volume is trivial
(6, 8, 26, 39, 40), in the upright as well as in supine posture (22,
53). This phasic EMG activity increases with respiratory stress
such as resistive loading (54) or progressive hypercapnia (53)
or hypoxia (52) or non-rapid-eye-movement sleep (29). Respiratory drive to the scalene muscle is present during inspiration
but is not necessarily coupled with that of the diaphragm and
parasternal intercostal muscles (8), two well-known primary
inspiratory muscles. In pathological conditions such as chronic
obstructive pulmonary disease (15, 26) or scoliosis (23), however, the neural drive to the scalene muscle is increased in the
same way as to these muscles.
Address for reprint requests and other correspondence: A. Legrand, Dept. of
Physiology and Pharmacology, Univ. of Mons, Av. Du Champ de Mars 6,
7000 Mons, Belgium (e-mail: [email protected]).
http://www. jap.org
In quadrupeds, the contribution of the scalene muscle to
ventilation remains more controversial. Inspiratory activity has
been demonstrated in the medial scalene during quiet breathing
in awake and naturally sleeping rats (38, 42). In hamsters
awake or under anesthesia (24), the muscle is reported to be
silent at rest but rapidly recruited with increasing respiratory
drive. In anesthetized dogs, inspiratory activity is described at
rest (2), but some researchers have failed to demonstrate any
significant respiratory activity in the muscle at rest or under a
variety of respiratory conditions (5, 10, 12). Faced with this
discrepancy, the reality of the activation of the muscle has been
questioned and reassessed after section of the external intercostal nerve (7). In that condition, the muscle was silent.
Therefore, the activity recorded in the muscle was considered
as a contamination from underlying external intercostal muscles. The scalene muscle is now usually regarded as inactive in
the dog during breathing and as an accessory inspiratory
muscle in other species.
The scalene muscle originates from the transverse processes
of the cervical vertebrae and inserts caudally onto the ribs. Its
anatomy consists of three heads: ventral, medial or pars supracostalis, and dorsal. In humans, the muscle inserts onto the
upper surface of the first two ribs (34). In quadrupeds, the
medial portion predominates. It inserts on the lateral aspect of
the third to fifth ribs in the hamster (24) and down to the sixth
to eighth ribs in the dog (33). The respiratory effect of a muscle
depends, among other things, on its insertions and the shape of
the rib cage. This effect can be appreciated by the change in
airway pressure or in lung volume that the muscle can generate
during its maximal contraction in isolation. However, there is
no clinical setting that allows contraction of scalene muscle in
isolation. Therefore, its action on the respiratory system cannot
be precisely defined, particularly in humans. Theoretical studies (48, 49) have been conducted to evaluate the effect of a
particular muscle on the respiratory system by measuring its
fractional change length during passive inflation of the respiratory system. This last parameter is conventionally defined as
the mechanical advantage of the muscle. The validity of this
approach has been tested experimentally in different canine
muscles (17, 19, 33, 35, 36). Using this approach, we previously studied the effect of the scalene muscle in humans (34)
and dogs (33). In both species, the scalene muscle shortened
during passive inflation and therefore had an inspiratory effect.
In humans, the mean shortening averaged 11.8% of the length
at functional residual capacity (LFRC) per inspiratory capacity
(IC). In the dog, the fractional shortening was only 5.8%
LFRC/IC and decreased to 3.7% LFRC/IC when the neck was
extended to reach a more natural posture. In humans, the
scalene muscle is thus always active during breathing and has
a huge inspiratory mechanical advantage, whereas in anesthe-
8750-7587/09 $8.00 Copyright © 2009 the American Physiological Society
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Legrand A, Majcher M, Joly E, Bonaert A, Gevenois PA.
Neuromechanical matching of drive in the scalene muscle of the
anesthetized rabbit. J Appl Physiol 107: 741–748, 2009. First published July 16, 2009; doi:10.1152/japplphysiol.91320.2008.—The
scalene is a primary respiratory muscle in humans; however, in dogs,
EMG activity recorded from this muscle during inspiration was
reported to derive from underlying muscles. In the present studies,
origin of the activity in the medial scalene was tested in rabbits, and
its distribution was compared with the muscle mechanical advantage.
We assessed in anesthetized rabbits the presence of EMG activity in
the scalene, sternomastoid, and parasternal intercostal muscles during
quiet breathing and under resistive loading, before and after denervation of the scalene and after its additional insulation. At rest, activity
was always recorded in the parasternal muscle and in the scalene
bundle inserting on the third rib (medial scalene). The majority of this
activity disappeared after denervation. In the bundle inserting on the
fifth rib (lateral scalene), the activity was inconsistent, and a high
percentage of this activity persisted after denervation but disappeared
after insulation from underlying muscle layers. The sternomastoid was
always silent. The fractional change in muscle length during passive
inflation was then measured. The mean shortening obtained for medial
and lateral scalene and parasternal intercostal was 8.0 ⫾ 0.7%, 5.5 ⫾
0.5%, and 9.6 ⫾ 0.1%, respectively, of the length at functional
residual capacity. Sternomastoid muscle length did not change significantly with lung inflation. We conclude that, similar to that shown in
humans, respiratory activity arises from scalene muscles in rabbits.
This activity is however not uniformly distributed, and a neuromechanical matching of drive is observed, so that the most effective part
is also the most active.
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NEUROMECHANICAL MATCHING IN SCALENE
tized dogs the muscle has a small mechanical advantage and is
never active during breathing.
In rabbits, inspiratory activity has been reported in the
scalene muscle during quiet breathing (41) and under progressive stress (4). The purpose of the present studies was thus to
clarify the primary role of this muscle during breathing and
more specifically to determine whether the activity observed
during breathing in the rabbit is the result of a contamination
from underlying muscles. In addition, we evaluated the fractional shortening of the scalene muscle during passive inflation
of the thorax postulating that differences in activation could
reflect differences in mechanical advantage.
MATERIALS AND METHODS
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All procedures conformed to the American Physiological Society’s
“Guiding Principles in the Care and Use of Animals” and were
approved by our institutional Animal Ethics and Welfare Committee.
Studies were carried out on 10 New Zealand White rabbits (mean
body wt 2.9 ⫾ 0.1 kg).
Experiment 1. Because the shape and direction of ribs are determinants of the scalene respiratory effect, the form of the ribcage was
first defined in six animals. Animals were sedated with an intramuscular injection of ketamine (25 mg/kg) and xylazine (5 mg/kg),
intubated, and placed in supine posture in a computed tomographic
(CT) scanner (Somatom Plus 4, Siemens Medical Solutions, Forcheim, Germany). This position was chosen to allow comparison with
data from the literature. Once positioned, the animal was mechanically hyperventilated for 40 s to induce apnea, and the chest wall was
allowed to relax to equilibrium. A spiral data acquisition starting at the
last cervical vertebrae and extending to the lower edge of the ribcage
was performed during this apnea. The scanning parameters were as
follows: 120 kV, 50 mA, 0.75 s/revolution scanning time, 2 mm
collimation, and 2 mm/s table feed. Transverse CT scans at functional
residual capacity (FRC) were reconstructed at 1.6-mm intervals using
a 360-degree linear interpolation algorithm and a standard reconstruction algorithm. In each animal, the number of slices thus obtained
ranged from 60 to 80. The animal was then allowed to recover. On the
reconstructed images, points on the cranial edge of the ribs were
identified bilaterally. The x (anteroposterior) and y (lateral) coordinates of these points were obtained and, with the slice number of the
image, provided the three-dimensional coordinates of points along the
edges of the ribs. The orientation of planes that best fit the data for
each rib was assessed by using the method previously described (51).
Thus a plane of the form z ⫽ A ⫹ Bx ⫹ Cy was fitted to each rib, and
the coefficients A, B, and C were determined by a linear regression
analysis. The orientation of this plane with respect to a transverse (x-y)
plane was described by the angles ␣ and ␤, where ␣ was the
pump-handle angle and ␤ the bucket-handle angle of the rib. Angles
␣ and ␤ were derived from the relationships tan ␣ ⫽ B and tan ␤ ⫽
C cos␣ . By convention, angle ␣ was therefore negative when the
plane of the rib sloped ventrally and caudally. Shape of the rib cage
was also evaluated by measuring laterolateral and anteroposterior
diameters. The highest left and right y values were considered to
calculate laterolateral diameter, and the anteroposterior diameter was
measured along the x-axis at the level of the more posterior point on
the rib. These values were obtained for the third and sixth ribs and at
the level of the caudal edge of the sternum.
Experiment 2. Respiratory activity of the scalene muscle was
studied in eight animals. Five were anesthetized with urethane (1,300
mg/kg ip) and three with pentobarbital sodium (40 mg/kg ip). The
animal was placed in supine posture, and a venous cannula was
inserted to give maintenance doses of anesthetic agent adjusted to
maintain the abolition of response to nociceptive stimuli but to keep
the corneal reflex present throughout the measurements. A catheter
was inserted into the left femoral artery to monitor blood pressure, and
rectal temperature was maintained constant at 38 ⫾ 1°C with infrared
lamps. The animal was tracheotomized, and a cannula (length 3 cm,
inside diameter 3 mm, and outside diameter adapted to fit to the
animal’s trachea) was inserted in the airway. The medial scalene and
sternomastoid muscles, as well as the parasternal muscle of the second
interspace, were exposed on the left side of the chest. Its medial and
lateral portions (bundle inserting respectively on the third and fifth
ribs) were identified, and pairs of silver electrodes spaced 2 mm apart
were implanted in parallel fibers in each bundle. The electrodes were
made of insulated straight wire (30 gauge) finely hooked at the tip.
The insulation was removed at 4 mm. The volume of muscle sampled
with these electrodes was larger than with usual fine-wire electrodes.
We could thus obtain a better evaluation of the activity of the bundle
studied, since the recording of unrepresentative motor units was less
likely. In addition, the shape of the electrode allowed us to maintain
its position as superficial as possible in the muscle, limiting the
cross-contamination from the underlying external intercostal muscle.
An additional wire acting as common ground was also implanted
subcutaneously. Two additional pairs of electrodes were implanted:
one in the sternomastoid and the other in the medial part of the
parasternal muscle (2nd interspace). EMG signals were processed by
using amplifiers (BMA400, CWE, Ardmore, PA), band pass filtered
between 100 Hz and 3 kHz, and rectified before their passage through
leaky integrators (time constant ⫽ 100 ms; MA821, CWE). Raw and
integrated signals were then digitalized (NI-PCI 6034 E; National
Instrument, Austin, TX) with a sampling rate of 15 kHz. In addition,
changes in lung volume were measured by electronic integration of
flow signal derived from a heated Fleisch pneumotachograph and a
Validyne differential pressure transducer (PNT Digital, Medical Electronic Construction, Brussels, Belgium), and airway pressure was
measured with a second differential pressure transducer connected to
a side port of the endotracheal tube. Measurements were obtained
during resting room air breathing and against increased resistive loads
placed in the inspiratory line of a Hans-Rudolph valve (resistors of
1-cm-long through which holes of 2, 1, and 0.8 mm diameter had been
bored; valve series 2210 Hans Rudolph, Kansas City, MO). Three
periods of recording were obtained in each condition after an equilibration phase. The effect of scalene muscle denervation was then
studied. Branches of the second and third internal intercostal nerves
innervate the muscle. They were exposed and sectioned. Measurements were then repeated in the same way as in intact animals. To
appreciate incomplete denervation and to confirm the contamination
from underlying muscles, measurements were finally repeated when
the muscle was electrically insulated with a small rubber piece placed
between muscle layers. EMG activity was measured in arbitrary units.
The values obtained during respiratory stress in the intact animal were
expressed as a percentage of the value obtained during unimpeded
breathing. The values obtained after denervation and denervation plus
insulation were expressed as a percentage of the value obtained in the
intact animal with the same respiratory stress.
Experiment 3. The potential change in airway pressure produced by
a muscle contracting alone against a closed airway is related to the
mass of the muscle, the maximal active muscle tension per unit
cross-sectional area, and the fractional change in muscle length per
unit volume increase of the relaxed chest wall (48, 49). Using this
approach, we evaluated the mechanical advantage of the scalene
muscle in the rabbit and in hamsters. We first assessed the fractional
change in muscle length during passive inflation in seven rabbits. The
animal was deeply anesthetized so that the corneal reflex was abolished throughout the study. The tracheal cannula was connected to a
mechanical ventilator. The scalene muscle was exposed on the right
side from its upper insertion on the lateral part of the last cervical
vertebrae to its lower insertions on the ribs. Bundles inserting on the
third, fourth, and fifth ribs were clearly identified and referred to as the
medial, middle, and lateral portions, respectively. Markers were
implanted in the muscle 2–3 cm apart alongside each bundle. A digital
camera was positioned with an angle of incidence orthogonal to the
NEUROMECHANICAL MATCHING IN SCALENE
RESULTS
Shape of the upper rib cage and orientation of the ribs. The
laterolateral diameter of the chest increased from top to bottom. It grew from 36.4 ⫾ 1.0 mm at the level of the third rib
to 56.8 ⫾ 1.4 and 79.1 ⫾ 4.1 mm at the level of the sixth rib
and caudal edge of the sternum, respectively (P ⬍ 0.001).
Anteroposterior diameter also increased in the caudal direction,
from 33.2 ⫾ 1.3 to 47.5 ⫾ 1.35 and 51.9 ⫾ 1.3 mm at
corresponding levels (P ⬍ 0.001). The shape of the rib cage
was thus essentially circular at the top and became narrower in
the anteroposterior direction when going caudally to the base
(P ⬍ 0.001).
Values of ␣ angles at FRC are displayed in Fig. 1. Because
of its size, the number of slices obtained from the first rib
varied from two to five; therefore, it was not possible to
calculate its direction reliably. In each animal, the other ribs
were slanted caudally in the ventral direction and ␣ angle
increased gradually from the second (12.6 ⫾ 3.2 degrees) to
J Appl Physiol • VOL
Fig. 1. Direction of ribs at functional residual capacity. Mean ⫾ SE data
obtained from 6 animals in supine posture. Angle ␣ is formed by an individual
rib and the perpendicular to the spine. It represents the slope in ventral
direction (known as the pump-handle angle). The minus sign indicates the ribs
are slanted caudally.
the sixth rib (33.7 ⫾ 2.8 degrees; P ⬍ 0.001). Values of ␤
angle were more variable from one animal to another but
remained small. The lateral slope of ribs (known as the bucket
angle) was thus close to perpendicular to the sagittal midplane
at FRC.
EMG activity. Traces from a representative animal are
shown in Fig. 2. During quiet breathing, activity was always
recorded from the parasternal and medial scalene muscles. In
contrast, activity was present in only four of the eight lateral
scalene muscles studied. All the activity increased gradually
with progressive resistive loads. With the highest load (R3), the
mean parasternal EMG activity was increased to 929 ⫾ 251%
of basal activity (P ⬍ 0.05). The activity increased even more
significantly in the medial scalene (P ⬍ 0.05 vs. parasternal)
and reached 2,226 ⫾ 532% of basal activity (P ⬍ 0.05). With
resistive loading, activity appeared in each lateral scalene; with
R3, EMG activity reached 2,086 ⫾ 563% of basal activity in
the four animals in which the muscle was active during
unimpeded breathing (P ⬍ 0.05). The sternomastoid was never
active in any conditions.
After scalene denervation, changes in airway pressure and
parasternal activity did not vary significantly (Figs. 2B and 3).
Despite denervation, activity was always present in the medial
scalene, even if very limited in two. On average, this activity
lowered to 40.7 ⫾ 8.9% and 35.7 ⫾ 9.3% of predenervation
values during unimpeded breathing and with the highest resistive load, respectively (Fig. 3; P ⬍ 0.05 for both conditions).
Concerning the lateral scalene, activity was still detectable in
three muscles at rest. The mean activity recorded in the four
muscles active in intact condition was 24.1 ⫾ 4.8% of basal
activity. With the highest load, this percentage remained higher
(89.2 ⫾ 26.4% of the activity with R3 in intact animals; not
significant), essentially because of a higher persistence of
activity in the bundles silent at rest. The mean lateral EMG
activity with R3 was only 30.4 ⫾ 8.5% after denervation for
the four muscles active at rest (P ⬍ 0.05 vs. R3 in intact
animal). This percentage is not statistically different from the
one observed in the medial scalene. When the muscle was
insulated from underlying muscle layers in addition to the
denervation, the mean activity in the lateral bundle fell to 6.5 ⫾
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muscle plane. The animal was curarized (vecuronium 0.7 mg/kg), the
mechanical ventilation was stopped, and the chest wall was allowed to
relax to equilibrium. A gauge was placed next to the muscle bundles,
and pictures of the scalene were taken at FRC in close-up. The
tracheal cannula was then connected to a super syringe, lung volume
was either increased by 0.02, 0.04, 0.06, 0.08, or 0.1 liter above FRC,
and pictures were taken at each lung volume. The procedure was done
in triplicate. Markers were also implanted in the sternomastoid muscle
and in the parasternal muscle of the second interspace, and pictures
were taken after the same procedure. Finally, in five animals, heterogeneity in the mechanical advantage was then confirmed by applying
external forces on the ribcage. Hooks were implanted bilaterally at the
anterior extremity of the first, third, and sixth ribs and at the insertion
of the scalene bundles on the fourth and fifth ribs. After relaxation of
the chest, the change in occluded airway pressure was measured while
a load of 135 g was applied in the cranial direction to each individual
rib pair successively. The animal was then euthanized with an overdose of pentobarbital sodium.
In addition, we measured the scalene fractional change in muscle
length in four adult Syrian golden hamsters. The animal was sedated
with ketamine (200 mg/kg) and xylazine (10 mg/kg) by intraperitoneal injection, intubated (cannula length of 3 cm and inside diameter
of 1.3 mm), and placed in supine posture. The scalene was exposed,
and markers were implanted in the anterior part of the muscle
(inserting on the third rib). During apnea, pictures were taken at FRC
and after an inflation of the respiratory system by 20 cmH2O. The
animal was then euthanized with an overdose of pentobarbital sodium.
Data from the digital images were analyzed using a drawing
program (CorelDraw7). On each picture, the length of the gauge and
the distance between markers were measured in arbitrary units, and
the muscle length between markers was calculated. Changes in muscle
length during passive inflation were then expressed as a percentage of
the length at FRC. Changes in occluded airway pressure were expressed relative to the change measured during the loading of the third
rib pairs.
Statistical analysis. For each animal, measurements made in triplicate and values obtained on right and left sides of the chest were
averaged for each subject. The results were then averaged for the
group and expressed as means ⫾ SE. Statistical comparisons between
rib angles, changes in muscle length, EMG activities in basal condition, as well as after denervation or insulation, and changes in airway
pressure 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.
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as follows: after denervation ⫽ 36.0 ⫾ 8.3% and 31.7 ⫾ 9.1%
and after denervation plus isolation ⫽ 7.3 ⫾ 5.2% and 3.0 ⫾ 0.8%
of intact animal, with R0 and R3, respectively. Omitting this
animal did not affect the statistical significance of the results.
Mechanical advantage. The effect of passive inflation on
muscle length is shown in Fig. 4. With passive inflation, the
three bundles of scalene muscle invariably shortened. In addition, the amount of shortening was always smaller in the lateral
part than in the medial and middle parts. This amount of
shortening was linearly linked to the volume up to a 100-ml
insufflation. The relationship between lung volume inflation
over FRC and pressure in occluded airways was evaluated.
Over 80-ml inflation, the relationship became clearly exponential, indicating that lung volume was approaching total lung
capacity. A 100-ml inflation was used as IC for the evaluation
of the changes in muscle length. Shortening of the medial and
Fig. 2. Traces of EMG activity (in arbitrary units) recorded from parasternal
and scalene muscles in a representative animal. Each trace represents a
respiratory cycle. A: records were obtained during graded inspiratory resistance
(resistors R0 to R3 with an orifice of 4, 2, 1, and 0.8 mm in diameter,
respectively). B: records were obtained in an intact animal (left), after denervation of the scalene muscle (middle), and after additional insulation (right).
Bottom traces correspond to changes in airway pressure.
3.5% of the basal value with R3 (P ⬍ 0.01 vs. denervation). In
the medial scalene, the activity after insulation averaged
11.2 ⫾ 5.9% of basal activity at rest and 4.5 ⫾ 1.6% with the
highest resistive load (P ⬍ 0.02 vs. denervation). In one
animal, the denervation was actually partial. In this animal at
rest, the activity after denervation fell by 25% only and EMG
activity was still recorded (35% of basal) after insulation. The
mean values of medial scalene activity without this animal were
J Appl Physiol • VOL
Fig. 4. Fractional change in muscle length during passive inflation of the chest.
Values are means ⫾ SE data of 8 animals. The changes are expressed as
percent changes relative to the muscle length at functional residual capacity
(LFRC) and are reported for the parasternal intercostal (■) and sternomastoid
(䊐) muscles, as well as for the medial (E), middle (Œ), and lateral () scalene.
The minus sign indicates a shortening.
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Fig. 3. Inspiratory activity recorded from the parasternal intercostal and the
medial and lateral scalene after denervation of scalene muscle and after its
additional insulation. EMG activities are reported for unimpeded breathing
(R0) and for the highest inspiratory resistance (R3). Data are expressed in
percentage of the values obtained in the intact animals with the same resistance. Values are means ⫾ SE of 8 animals, except R0 values in the lateral
scalene (mean of the 4 active muscles, see text). *P ⬍ 0.05 compared with
intact animals; #P ⬍ 0.05 compared with denervation.
NEUROMECHANICAL MATCHING IN SCALENE
DISCUSSION
The scalene muscle is generally considered as either primary
or accessory, depending on the species. In the present studies,
activity was consistently recorded from the medial part of the
muscle in the rabbit, even during resting breathing. In the
lateral portion of this muscle, however, EMG activity was
observed only sporadically; under respiratory stress, the majority of the activity in that portion actually corresponded to a
contamination from underlying muscle layers. Depending on
which part of the muscle was studied, the scalene could thus be
considered as a primary inspiratory muscle or not. From a
mechanical point of view, the muscle had a significant inspiratory effect. Again, however, differences in the muscle did exist.
Therefore, this muscle can no longer be considered as a unique
entity. Interestingly, the portions active at rest are also the most
effective.
The effect of scalene contraction on the chest does not differ
fundamentally from one species to the other. Considering its
insertions in the neck and on the anterior rib cage, its primary
action is a cranial motion of the sternum and ribs. The displacement of the rib cage increases the anteroposterior diameter of the chest and causes lung inflation. This has been
observed in high tetraplegic patients (3, 9). In that condition, in
which the diaphragm and the intercostal muscles are paralyzed,
breathing induced a huge axial displacement of the sternum,
and the change in anteroposterior diameter was four times
greater than during a relaxed maneuver. Inversely, when a tidal
inspiration was performed mainly with the diaphragm and the
scalene EMG activity was suppressed in a normal subject, the
upper rib cage moved paradoxically and the anteroposterior
diameter was reduced (8). Finally, the action of the scalene has
been obtained in isolation in the dog (13). During its contraction, a displacement of the sternum in the cranial direction was
J Appl Physiol • VOL
induced and the increase of the anteroposterior diameter was
greater than expected on the basis of the relaxation curve. A
simple geometric model demonstrates the importance of the
slope of the ribs on the change in anteroposterior diameter
during an upward motion of the sternum. This is illustrated in
Fig. 5. From this model, we can predict that the respiratory
effect of a muscle producing an upward movement of the
sternum during its contraction would be maximal when ribs are
slanted caudally with an angle ␣ close to ⫺45° and would be
very limited when this angle is ⬃0°. In rabbits, ribs are directed
caudally and ventrally, and the slant increases with the rib
number. This contrasts with the results obtained in dogs (37),
in which direction of the rib varied around the perpendicular to
the spine, or in humans, in whom ribs are slanted caudally with
an angle close to ⫺45°. These values in humans (50) were
obtained with arms resting along the sides of the body. In other
studies, orientation of ribs three to seven was determined in
humans with the arms above the head (51). In that position, ␣
angles were decreased by 6 to 10 degrees, but ribs remained
largely slanted caudally. In the present studies, the forelegs
were left free during CT scan acquisitions, and our results have
disclosed an intermediate orientation, with a second rib only
slightly slanted but with the sixth and seventh rib slanted like
in humans. Based on these results, we could predict that, for a
given muscle shortening, the scalene has a higher respiratory
effect in the rabbit than in dogs but smaller effect than in
humans. This model is a convenient two-dimensional model
like Hamberger’s model (27). We circumvented the limitations
of this simple model by appreciating the effect of the muscle on
the respiratory system as a whole. The measurement of me-
Fig. 5. Schematic model illustrating the action of scalene muscle. The shortening of the distance (ac) rotates the lower bar (bc) upward (dotted lines),
increasing the angle ␸ between the left vertical bar and oblique bar. The
distance d between the 2 vertical bars is equal to [(bc) sin ␸] and increases by
⌬d during rotation. For a given change in ␸, ⌬d becomes smaller when the bar
is oriented in a direction closer to horizontal (top bar). Angle ␣, see text.
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middle bundles averaged 8.0 ⫾ 0.7% and 7.6 ⫾ 0.6% of
LFRC/IC, respectively (difference not significant). The lateral
bundle shortened only by 5.5 ⫾ 0.5% LFRC/IC (P ⬍ 0.05 vs.
medial and middle scalene shortening). Parasternal muscle
shortening was equal to or higher than the shortening of the
medial scalene with a mean value of 9.6 ⫾ 0.1% LFRC/IC (not
significant). The sternomastoid muscle behaved differently.
Changes in muscle length were small and not related to the
amount of lung inflation. In addition, the muscle was observed
to lengthen in one animal.
The four hamsters studied had a mean weight of 132 ⫾ 7 g,
and, on average, the scalene muscle shortened by 4.8 ⫾ 1.1%
LFRC/IC.
To mimic the effect of a muscle contraction, external loads
were applied bilaterally at the extremities of scalene bundles
(rib pairs 3, 4, or 5) in rabbits. The change in airway pressure
varied according to the rib on which the load was exerted.
Specifically, the change was highest when loads were applied
at the insertion of the medial bundle on the third rib. Relative
to this effect, the change measured when the load was applied
at the end of the middle and lateral bundles was respectively
79 ⫾ 10% and 51 ⫾ 7%. Considering the insertion of the
scalene muscle in dogs and humans, the loads were also
applied at the anterior extremity of the first and sixth rib, and
the mean relative change in occluded airway pressure was only
41 ⫾ 8% and 64 ⫾ 6%.
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NEUROMECHANICAL MATCHING IN SCALENE
J Appl Physiol • VOL
ity persisting after insulation. The scalene activity was
limited in amplitude during resting breathing. Indeed, when
the EMG value in that condition was expressed in percentage of the value measured with R3, the mean activity was
inferior to 5% in the medial scalene. In addition, the level of
activity recorded at rest and during stimulated breath was
probably affected by the anesthesia. In humans, scalene
activity is highly sensitive to some anesthetic agents. The
integrated EMG activity recorded at rest in the scalene
amounted to 7% of the maximal voluntary activity but
decreased to one-tenth of this value under thiopental anesthesia (20). During sedation with midazolam (21), the resting EMG activity measured with surface electrodes decreased to 33% of the value awake and activity was observed in only four of six patients studied under halothane
anesthesia (47). Here, the intensity of the activity is limited
under pentobarbital sodium or urethane anesthesia. However, its presence at rest clearly demonstrates that the
scalene muscle is a primary inspiratory muscle in the rabbit
like in humans. Interestingly, the scalene muscle is not
uniformly activated. When activity was always present in
the medial part, activity was only present in half the lateral
bundles at rest. With a higher respiratory stress, activity was
observed in all the lateral parts of the muscle; however, in
the muscle recruited with respiratory stress, the activity
largely persisted after denervation and was abolished by
insulation. The lateral scalene is thus inconsistently activated during breathing in the anesthetized rabbit. The action
of anesthetic agent on respiratory muscles and on the thorax
is known to vary with the depth of anesthesia, from muscle
to muscle and from species to species (45, 46). In the rabbit,
barbiturate anesthesia has a differential effect on the respiratory activities recorded from the diaphragm and intercostal muscles at rest and during rebreathing (1). Therefore, it
is possible that the difference observed between medial and
lateral scalene activity is related to the use of this anesthetic
agent. All anesthetics, however, do not modify respiratory
muscle activity in the same way. Ketamin, for instance, did
not alter the scalene activity (21). Our measurements were
obtained under barbiturate anesthesia but also with urethane
anesthesia. This drug is widely used in animal models
because it produces a long-lasting anesthesia with minimal
effects on the cardiovascular and respiratory systems (43).
Like ketamine, its molecular mechanism of action differs
from most anesthetics including barbiturates (28). With both
anesthetics, active and inactive lateral scalene muscles were
observed. In addition, in dogs (7) and in hamsters (24), the
presence or the absence of activity was not altered by
anesthesia. Therefore, we rather linked this observation to
our measurement of mechanical advantage. Portions with
the highest respiratory effect were activated more often than
the others. Similar to that shown in intercostal muscles (11,
16, 25, 31, 32), there is thus a parallel between activation
and mechanical advantage within the muscle. To further
evaluate this parallel, we have compared activation and
mechanical advantage from species to species. In humans,
the muscle is consistently active at rest (6, 8, 26, 39, 40) and
has a huge mechanical advantage (34). In the anesthetized
rabbit, activity is present at rest but limited in amplitude in
the medial portion of the muscle, which has a significant
mechanical advantage; and the activity is inconsistent in the
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chanical advantage allows this appreciation and has been
evaluated in humans (34), in dogs (33), and here in the rabbit.
The shortening of the scalene muscle during inflation confirms
its inspiratory potential in the three species. In the present
study, rabbit’s scalene shortened by 8% of the LFRC/IC, ranging between results observed in humans [11.8% LFRC/IC (34)]
and dogs [5.8% LFRC/IC (33)]. We evaluated the mechanical
advantage of the parasternal muscle in the second interspace
for comparison. This muscle is indeed considered as a primary
inspiratory muscle of the rib cage in mammals, and, like the
scalene, it moves the third rib upward. The mechanical advantage of the scalene was significantly smaller but amounted to
80% of the parasternal mechanical advantage. In humans,
parasternal changes in muscle length during passive inflation
were shown to be 7.7% LFRC/IC in the second interspace (18).
In the dog, the parasternal muscle’s fractional length change
was not different in the second and third interspace and
averaged 10% LFRC/IC (19). The ratio between scalene and
parasternal mechanical advantage varied thus in an opposite
direction in dogs (⫾60%) and in humans (⫾150%). Therefore,
the differences observed between species in scalene mechanical advantage do not reflect a global variation in efficacy of rib
cage muscles. On the contrary, it reflects a change specific to
each muscle depending on the chest wall mechanics. In addition, we investigated the heterogeneity of the fractional change
in muscle length among the muscle. During previous studies in
humans (34), we tried to differentiate the bundles inserting on
the first and second ribs. However, the method was not sufficiently accurate to reliably identify the lower insertion of the
scalene on the second rib and this evaluation was abandoned.
Interestingly, we observed here that the fractional change in
muscle length was dependent on the rib number on which the
bundle inserts. The fibers inserting on the third rib shortened
1.5 times more than the lateral fibers inserting on the fifth rib.
This heterogeneity of respiratory effect within the scalene
muscle was further tested with external forces. The observed
change in occluded airway pressure was 2.0 ⫾ 0.3 times higher
when the load was exerted on the third rib pair than on the fifth.
Hence, scalene muscle cannot be considered any more as a
unique muscle from a mechanical point of view.
Concerning the EMG activity, our results have demonstrated a clear consistent activity in the scalene muscle
during breathing. This activity corroborated the observations in rodents reporting activity at rest (38, 42). Based on
the experiments by De Troyer et al. (7), we could hypothesize that this activity was in fact artefactual. Indeed, the
disappearance of the activity recorded from the scalene
muscle after external intercostal denervation has suggested
that this activity corresponded to a contamination from an
underlying muscle layer. Our experiments of scalene denervation have confirmed both hypotheses: contamination and
true activity. Indeed, section of motor nerves just before
their penetration into the muscle reduced the amount of
activity recorded to 40% of the predenervation values,
implying that 60% of the basal activity actually originated
from the scalene. But the persistence of activity that disappeared after electrical insulation from underlying muscles
confirmed a contamination of signals recorded, particularly
in the lateral portions under respiratory stress. Because it
was not possible to isolate the muscle entirely, a crosscontamination probably explains the limited residual activ-
NEUROMECHANICAL MATCHING IN SCALENE
GRANTS
This work was supported in part by the Fonds National de la Recherche
Scientifique Grant 1.5.066.06 F.
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lateral part, which has a smaller respiratory effect. In awake
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