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Division of Pulmonary/Critical Care Medicine, Department of Medicine, The Cedars-Sinai Medical Center Burns & Allen Research Institute, University of California Los Angeles School of Medicine, Los Angeles, California 90048
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Fournier, Mario, and Michael I. Lewis. Functional role
and structure of the scalene: an accessory inspiratory muscle in
hamster. J. Appl. Physiol. 81(6):
2436-2444, 1996.
Although the scalene muscle (Sca) is a primary
inspiratory muscle in humans, its respiratory function in other species
is less clear. The electromyographic (EMG) activity of the Sca was
studied during resting ventilation (eupnea) in both the awake and
anesthetized hamster and after a variety of respiratory challenges in
the anesthetized animal. The EMG activities of the medial Sca and the
costal diaphragm were compared. The medial Sca, the major component of
the Sca, originates from cervical transverse processes 2 to 5 and
inserts primarily onto rib 4, with a small segment onto rib 3. In both the anesthetized and awake animal, the Sca was always silent during quiet breathing. With
CO2-stimulated hyperpnea, the Sca
was always recruited during inspiration in phase with the diaphragm.
Active recruitment of the Sca was also observed after resistive loading and total airway occlusion. After ipsilateral phrenicotomy, the Sca was
persistently recruited during eupnea. The specificity of the EMG
signals was tested both by excluding cross contamination from other rib
cage muscles and by selective denervation studies. Muscle spindles were
identified in the medial Sca histochemically, suggesting that the
respiratory activity of the Sca can also be modulated by changes in
muscle length and/or load. These results indicate that the Sca
functions as an accessory inspiratory muscle in the hamster and may
play an important role in conditions of chronic load.
electromyographic activity; respiratory muscles; neck muscles; muscle spindles
INTRODUCTION ALTHOUGH EARLIER STUDIES in humans suggested that the
scalene muscle (Sca) functioned predominantly as an accessory
respiratory muscle (4, 17, 25, 31), later studies using improved techniques demonstrated unequivocally that the Sca was always recruited
during inspiration with eupneic breathing (7, 9, 11, 14, 32). Thus it
is now well accepted that the Sca functions as a primary inspiratory
muscle in humans, as had been previously suggested (25).
Studies in the rabbit had also suggested a primary inspiratory role for
the Sca (28). However, absence of enhanced perfusion of the Sca during
augmented ventilation or after phrenicotomy failed to support such an
assumption (23). Similarly, studies in the anesthetized supine dog
indicated that high levels of CO2 rebreathing as well as a wide range of increased inspiratory
resistances did not change the Sca blood flow (2, 26, 27). In addition, electromyographic (EMG) recordings of the Sca in the dog failed to
demonstrate any significant respiratory role at rest or under a variety
of experimental conditions, such as hypercapnia, inspiratory resistance, hyperinflation, and phrenicotomy (6, 8, 10, 13). By
contrast, one study reported that the dog Sca was active during eupnea
and that its activity was increased with inspiratory resistance (5; but
see Ref. 10). Recently, the Sca was shown to be inactive in lightly
anesthetized baboons during quiet breathing in the supine and head-up
posture (12). Although the role of the Sca of this primate differs from
that in humans, no further respiratory challenges were imposed to test
for an accessory inspiratory function.
Results of studies in the rat clearly differ from those of the species
described above. In chronic preparations, inspiratory activity in the
medial Sca during non-rapid- eye movements (non-REM) sleep was
demonstrated (22, 29) as well as increased Sca recruitment during
CO2 challenge (22) and after
phrenicotomy (29). Such findings suggest an important respiratory role
for the Sca in the rat.
We hypothesized that the Sca of the hamster may behave in a similar
fashion to that of the rat, as these rodent species often share similar
structural and functional properties of their respiratory muscles. The
rationale for the present study is the fact that the hamster remains
the best characterized animal model of emphysema (30). Should the Sca
demonstrate respiratory functions, adaptive changes in the Sca might be
evident in the emphysema model, as chest wall and/or neck
muscles are recruited to compensate for the mechanical inefficiency of
the diaphragm due to hyperinflation. Indeed, functional and cellular
adaptations of the diaphragm and other respiratory muscles in the
hamster model of emphysema have been reported (1, 16, 18, 21). However,
before such studies in an emphysemic model, it remains imperative to
document the precise respiratory role, if any, of the Sca muscle in the
normal adult hamster. The purpose of this study was
therefore to evaluate the Sca in the normal healthy hamster with regard
to 1) the anatomic configuration of
Sca, since no reliable information is available for this species; and
2) the pattern of EMG activity in
Sca during different respiratory maneuvers, to determine whether it
plays any significant role during breathing.
MATERIALS AND METHODS Experimental Animals
Anatomical Studies
Detailed dissection of the Sca was performed in six animals under a high-power dissection microscope. To determine the presence of distinct portions of the Sca, the origins and insertions of the various components were identified. The relationships between the Sca and other neck and rib cage muscles were examined for the purpose of identifying the most appropriate locus for electrode implants. This permitted the definition of important landmarks which allowed electrode implantation in intact animals, without sectioning superficial musculature, nerves, etc. Additional information confirming anatomical structures and/or identifying individual variations was also obtained from animals used in the EMG studies (see below).EMG Studies
Acute experiments. In 10 animals, a short midclavicular longitudinal skin incision was performed on the right side to expose the medial Sca at the lateral edges of the pectoralis profundis cranialis and rectus abdominis muscles. A pair of electrodes was implanted in the Sca at the level of the second intercostal space immediately rostral to a slip of the serratus ventralis thoracis which is superficial to the lateral segment of the Sca. This muscle slip is intercalated between the lateral and the anterior segment under which it originates on rib 3, thus creating a natural division into two medial Sca segments. A small incision through the abdominal musculature was made below the right costal margin to expose the abdominal surface of the diaphragm. A pair of electrodes was implanted in the midcostal region of the right hemidiaphragm. To rule out the possibility of cross contamination in the Sca EMG signals by volume conduction from other muscles, electrodes were also implanted in the right external intercostals, parasternal intercostals, and serratus muscles. The third external intercostal was accessed by gently separating slips of the serratus and EMG electrodes implanted immediately lateral to the Sca. The second parasternal intercostal was implanted immediately medial of the Sca. Electrodes were implanted in the large serratus slip that is intercalated between the Sca and the external intercostal muscles at the level of second intercostal space. Finally, in two additional experiments, the ventral Sca was accessed through the neck incision (for tracheostomy) by gently separating (without sectioning) neck muscles, and electrodes were implanted in the largest area of the muscle between the first rib and C6. Electrodes were made of fine fluorocarbon-insulated multistranded stainless steel wires (38-gauge; Cooner Wire) that had 1 mm of insulation removed near the tip. The electrodes for each pair were positioned ~3-mm apart within all muscles except the ventral Sca. Because this muscle is so small, very fine Teflon film-coated wires (50-gauge; California Wire), with 1 mm of insulation removed at the tip, were implanted and positioned ~1.5- to 2-mm apart. One additional wire acting as common ground was also implanted subcutaneously. Leads were connected to calibrated differential amplifiers (Dantec), and the signals were band-pass filtered between 10 Hz and 2 KHz, with a 60-Hz filter incorporated, and further amplified (Service Associate). The same calibration and amplification were used for all experiments. EMG signals were monitored on a storage oscilloscope (Gould), and selected episodes were saved and displayed on a plotter (Hewlett-Packard). Experimental protocol and testing. EMG activities from the various rib cage muscles and the diaphragm were obtained from anesthetized and tracheostomized hamsters in a supine position. Further tests were also made with animals in a prone position or lying on their side. Although not systematically studied, no differences were observed in these recordings compared with those obtained in the supine position. Records of raw EMG activity of the medial Sca were compared with those of the costal diaphragm to characterize the inspiratory phase. However, no efforts were made to accurately determine differences and/or similarities in onset and offset times for their respective respiratory activities (i.e., relative to each other). Basic quiet-breathing patterns were recorded from different sets of electrodes. CO2-induced ventilatory stimulation was obtained by increasing dead space with either short (2.5- cm3) or long (6-cm3) tubing connected to the tracheal cannula. Tests of incremental airflow resistance were performed by successively inserting short needles of various sizes (20- to 30-gauge) at the tracheal cannula. For each procedure used on a given animal, several minutes were allowed for the animal to return to an eupneic state between the series of tests. Denervation of the right hemidiaphragm was obtained by ipsilateral phrenicotomy performed in the neck at the subclavicular level. The medial Sca was denervated by sectioning of the major muscle nerve branches at the level of the first rib. The ventral Sca was denervated by sectioning of the nerve branches at their cervical levels. Chronic preparations. Chronic instrumentation was performed in three hamsters to record EMG activities of the Sca and diaphragm while awake and to test whether the presence of anesthesia is a major factor in determining the pattern of activation of the Sca during breathing. In developing the chronic preparation, we anesthetized the animals as described above. Surgical techniques were performed under aseptic conditions. Similar incisions were made to expose the medial Sca and the costal diaphragm, and identical recording electrodes as described above were implanted. These fine wires were then loosely tunneled subcutaneously toward a small skin incision performed in the dorsal neck. The wires were exteriorized and sutured in the superficial back muscles of the animal to secure placement. The exteriorized wires were rolled into a small loop that was tied to prevent unraveling. Abdominal muscles were carefully sutured in layers. All skin incisions were closed with wound clips. A tracheostomy was not performed in the chronic preparation, as we wished to record spontaneous recruitment patterns of the Sca and diaphragm muscles in the awake animal in which the upper airway was intact. A single dose of buprenorphine (0.25 mg/kg sc) was given for analgesia during the recovery period. During the following 72 h, animals were studied on at least 2 separate days for ~2 h each time. To observe spontaneous activity of the Sca (both respiratory and nonrespiratory patterns) during normal behavior, individually housed animals were studied while they were awake and freely moving in the cage with only electrode wires swiveling above the grid. At the end of the study, after animals were killed, electrode positions were identified to confirm correct placement and no dislodgment.Histochemical Identification of Muscle Spindles
In five hamsters, the Sca was dissected, mounted, and pinned on cork at approximately in vivo resting muscle length (including rib attachment), frozen in isopentane cooled to its melting point by liquid nitrogen, and stored at
70°C until analysis. Muscle cross sections (10 µm thickness) were cut in a cryostat (Reichert-Jung 2800E) at
20°C. Sections were stained for myofibrillar actomyosin adenosinetriphosphatase after acid preincubation (3) as well as after
alkaline preincubation with prior tissue fixation. Muscle sections were
fixed with 2% paraformaldehyde in a 0.1 M cacodylate buffer (pH 7.4)
for 2 min at room temperature. Sections were rinsed with 0.18 M
CaCl2 before a 12-min
preincubation in 0.1 M 2
-amino 2-methyl-1-propanol
buffer (pH 9.6) before standard incubation was resumed at pH 9.4. This
latter method allows the histochemical identification of extrafusal
muscle fibers as the type I (light staining) or type II (dark staining)
with subgrouping of type II also achievable. It also allows one to
classify intrafusal fibers as nuclear
bag1,
bag2, and chain fibers (24). In
all animals, sections from the medial Sca at the level of the third intercostal space were examined at high magnification (×450) for the presence of muscle spindles by using a Leitz Laborlux S (Leica) microscope. Selected areas were photographed (Olympus). In addition, further studies were done in one hamster in which four separate sections at the level of the first three intercostal spaces as well as
above the first rib were examined.
RESULTS
Anatomical Studies
The general anatomical structure of the hamster Sca is depicted in Fig. 1A. The Sca originates from the transverse processes of the cervical vertebrae C2 to C6 and has costal insertions onto ribs 1, 3, 4 and, in ~50% of the animals, onto rib 5. Its anatomy is characterized by three distinct portions: scalenus ventralis, scalenus medius, and scalenus dorsalis (Fig. 1B). The medial portion represents the major component of the Sca with >85% of the muscle mass. The dorsal portion is also less than half the size of the ventral portion. The tendons of origin from C2 to C5 are shared among the three Sca portions. An additional tendon with origin at C6 is often shared by the ventral and dorsal portions only. These latter portions also have costal insertions onto rib 1 only. The ventral Sca inserts on the first rib from the chondrocostal junction and extends laterally. The very small dorsal Sca portion inserts at the most dorsal part of rib 1 near the vertebra and extends laterally to overlap with the ventral portion, often making it difficult to distinguish their respective areas of insertion. The most important portion of the Sca, the scalenus medius, is primarily characterized by its largest area of insertion onto rib 4 that extends dorsolaterally from the chondrocostal junction to cover the middle one-third of the rib. One additional thin and narrow muscle slip also inserts at the chondrocostal junction of rib 3. In all animals studied, a Sca insertion onto rib 2 was never observed. Finally, an occasional muscle slip that appears vestigial and may not be mechanically significant, inserts approximately at the center or middorsal area of the muscle onto rib 5.
In the medial portion, when individual segments of origin were
examined, a topography in the pattern of costal insertion was found
(Fig. 2). Muscle segments with tendons
originating from the more rostral transverse processes have more dorsal
costal insertions. Conversely, individual muscle segments with more
caudal tendons of origin insert more ventrally onto ribs. Although
exact areas of insertion vary slightly among animals, there is a
conserved pattern of insertion among muscle segments generally, with
the following order: the C2
segment overlapping the C3
segment; C3 overlapping
C4; and
C4 overlapping
C5.
The segmental pattern of cervical innervation of the Sca has not been determined in the hamster. Preliminary observations, based on nerve dissection only, indicated that cervical axons form the muscle nerve that branches near the first rib to innervate different parts of the medial Sca. Cervical nerve branches may directly innervate the ventral and dorsal portions at their respective segmental levels.
EMG Studies
Anesthetized animals. In all 10 normal healthy animals observed under anesthesia, the Sca was always inactive during quiet breathing (Fig. 3A). In three cases, animals were also positioned prone or on their side during eupnea, but there was no indication of active recruitment of the Sca. In five of seven animals, the addition of 2.5 cm3 of dead space to the tracheal cannula resulted in hyperpnea that was associated (within seconds) with the recruitment of the Sca during inspiration. The inspiratory recruitment pattern was always in phase with the diaphragm (Fig. 3B). In the remaining two animals, exposure to 6 cm3 of dead space readily demonstrated similar Sca activation as well (not shown). In all 10 animals, total occlusion of the tracheal cannula immediately recruited the Sca during the inspiratory phase (Fig. 3C).
A series of incremental resistive challenges were used to test for Sca recruitment. In two of three animals, the medial Sca remained inactive when airway resistance was slightly increased by placing a 20-gauge needle at the tracheal cannula (Fig. 4A). Clear recruitment of the Sca was observed in all animals challenged with 22- (Fig. 4B), 25- (Fig. 4C), 27-, and 30-gauge needles. The Sca was always rapidly and highly recruited with the diaphragm during spontaneous sigh maneuvers (not shown).
In five animals, the response of the medial Sca to ipsilateral phrenicotomy was examined (Fig. 5). The medial Sca was always silent during eupnea (Fig. 5A) but in all cases was immediately recruited after section of the phrenic nerve (Fig. 5B). Moreover, after ipsilateral phrenicotomy, the medial Sca was further activated in response to CO2-induced hyperpnea (Fig. 5C), as well as to total airway occlusion (Fig. 5D).
Validation experiments. There was concern that the recorded EMG signals attributed to the medial portion of the Sca may have had their origin in other surrounding inspiratory muscles. Because many respiratory-related muscles are located within very short distances from the locus of the Sca-recording electrodes, it remained possible that cross contamination by volume conduction from a very active muscle might be a source of EMG signals picked up by the Sca leads. Although the parasternal intercostal muscles, located medially, are active during eupnea (not shown), no EMG activity was recorded from the Sca during quiet breathing, as described above. The activity of the external intercostal muscles was the most likely source of respiratory EMG signals for cross contamination (10). In anesthetized and supine hamsters, the third external intercostal muscle was silent during resting breathing, but it was gradually recruited with increased resistance to air flow. It was highly recruited during total airway occlusion (Fig. 6A). However, the anatomic configuration is such that this muscle is not in direct contact with the Sca except for a very small portion of its lateral segment at the third intercostal space. Fortuitously, a very large slip of the serratus muscle is intercalated between both the Sca and the intercostals and, thereby, could prevent cross talk between the respective activities of those muscles. We hypothesized that if contamination were to take place, it should therefore be evident, with some respiratory pattern, in the EMG signals recorded from the serratus muscle. With the challenging maneuver of total airway occlusion, the serratus muscle was found to be totally silent while both the intercostal and the Sca muscles were very active (Fig. 6, B and C).
In two additional animals, the ventral Sca was also tested to verify the specificity of the EMG signals. The ventral Sca, with insertion on the first rib only (Fig. 1), is also highly recruited with total airway occlusion (Fig. 7A) in a way similar to the medial Sca (Fig. 3C). After selective denervation of the medial Sca, all EMG activity disappeared from it, whereas the ventral Sca demonstrated an increased level of recruitment (Fig. 7B). If cross contamination had occurred, EMG signals would be expected to still be present in the denervated medial Sca. Finally, section of most cervical nerve branches to the ventral Sca eliminated activity in this muscle (Fig. 7C). Thus the EMG signals depicted for the Sca in Figs. 3, 4, 5, 6, 7 had their origin from the Sca, without contamination (i.e., cross talk) from other respiratory muscles.
Awake animals. In all three awake animals, the Sca was always silent during quiet breathing while the animals were prone and relatively inactive (Fig. 8A). However, while the animal was in the prone position and relatively quiet, the Sca was observed to be active during various head and neck movements, such as a rapid lateral head rotation (Fig. 8B). For periods lasting several seconds, tonic activity interspersed with nonrespiratory irregular bursts was also observed in the Sca during a variety of ambulatory activities, including exploring the cage, walking around, or digging in the bedding (not shown). During other simple behaviors, for example grooming, the Sca was recruited in short nonrespiratory bursts in phase with the repetitive head movements associated with licking of the abdomen (Fig. 8C). A change in posture, for example standing on hind limbs against the side of the cage, did not elicit any spontaneous respiratory activity from the Sca. No respiratory recruitment of the Sca was observed over a wide range of respiratory frequencies in the awake animal.
Histochemical Identification of Muscle Spindles
Muscle spindles were identified in the medial Sca in all five animals. Although no efforts were made to further classify intrafusal fibers or estimate spindle density, spindles of the bag and chain variety were clearly evident within the small area of muscle observed. At the level of the third intercostal space, the mean number of spindles was 3.2 ± 0.8 (SD), ranging from two to four among all animals. Sets of two spindles, and in one case three, were often found to be in the same area, as depicted in Fig. 9, generally corresponding to a region where the largest number of type I fibers were located. In one animal, muscle sections were studied at four levels (~5 mm apart) along the muscle length (~21 mm). Within a section just above the first rib, five spindles were counted, localized mostly near the major blood vessel branches entering the Sca. In the first intercostal space, only one spindle was identified, whereas two and three were found in the second and third intercostal spaces, respectively.
DISCUSSION
The present study comprehensively examined the functional respiratory role of the Sca in the normal adult hamster and focused primarily on the medial Sca, the most important of its three components. The major finding of this study was that, in the hamster, the Sca has a respiratory function that can be best characterized as an accessory inspiratory muscle. The Sca was always found to be inactive during quiet breathing in both the anesthetized and the awake animal, precluding a primary inspiratory role. However, in the anesthetized hamster, several maneuvers used, such as CO2-stimulated hyperpnea, incremental resistive loading, total airway occlusion, or ipsilateral phrenicotomy, clearly demonstrated phasic inspiratory activity of the Sca in the hamster.
Specificity of the EMG Signals
The possibility was tested and excluded that cross contamination between the Sca and other nearby inspiratory muscles might account for the source of the EMG signals recorded in the present study. Prior studies in the dog reported EMG activity in the Sca even during quiet breathing (5). However, it was later demonstrated that the likely origin of the EMG signals was from the underlying active external intercostals (10). In the hamster, the serratus muscle is located between the Sca and the underlying external intercostal muscles, suggesting that it may act as a shield, preventing cross contamination of EMG signals from the underlying external intercostals. In the intact animal, if cross contamination of the EMG signals were taking place, the serratus muscle should have displayed an inspiratory EMG pattern originating in the external intercostal muscles. However, no EMG signals were recorded from the serratus even during the most challenging provocation of total airway occlusion. The fact that this was not the case is evidence of the propriety of the Sca EMG signals. In addition, further support and evidence of the specificity of the recorded EMG signals were demonstrated in experiments of selective denervation of the medial and ventral portions of the Sca during resistive breathing in which both portions exhibited strong inspiratory activity. The medial Sca became silent after denervation, whereas the ventral Sca displayed even greater activity, possibly as a mechanical compensation for the insult. Finally, with denervation of both ventral and medial portions of the Sca, all EMG signals disappeared during the same occlusion episode. If contamination had taken place, then some phasic EMG signals should still be present in the Sca.It is likely that the configuration of the recording electrodes is an extremely important factor regarding the specificity of the EMG signals in the present study. Similar electrode designs have also been used in chronic preparations of the rat (22, 29). These electrodes may differ significantly from the types used in the dog (6, 8, 10, 13).
Respiratory Role of the Sca
In humans, the Sca is always recruited during inspiration, even during periods of quiet breathing, thus making it a primary inspiratory muscle (7, 9, 11, 14, 32). In the present investigation, phasic inspiratory activity could not be observed in the Sca during quiet breathing in both the anesthetized and awake hamster. This suggests that anesthesia was not a significant factor preventing the identification of some residual inspiratory activity in the Sca of the hamster that would otherwise be present in the awake animal. In the present study, however, dead space ventilation and resistive loading resulted in clear recruitment during inspiration, always in phase with the diaphragm. This suggests an accessory inspiratory role for the Sca in the hamster. Of interest, enhanced recruitment of the Sca in the rat was also observed after challenge with 5% CO2 during non-REM sleep (22). In contrast to the present study, phasic inspiratory recruitment of the Sca during non-REM sleep in the rat, in the absence of metabolic challenge to respiration, was also reported by these authors (22, 29).Although the Sca in the hamster functions as an accessory muscle of inspiration, the medial Sca was shown to be instantly recruited during eupnea after ipsilateral phrenicotomy, thus becoming a "primary inspiratory muscle," as the imposed load was irreversible. Increased activation of the ventral Sca after selective denervation of the medial portion of the Sca may represent another example of compensation. In the nonanesthetized rat during non-REM sleep, the activity of the medial Sca was also reported to be greatly increased after bilateral phrenicotomy (29). This suggests that, in rodents, the Sca may be an important inspiratory muscle, readily responding to increased respiratory demands. This function may be crucial in conditions where mechanical loads are chronically imposed. However, this contrasts with experiments in the dog where even after bilateral phrenicotomy, the Sca was still not recruited (10).
Muscle spindles were readily observed in all cross sections of the medial Sca cut at the level of the third intercostal space. The presence of muscle spindles in the hamster medial Sca suggests its role in proprioception. This contrasts with spindle paucity in the costal diaphragm of hamster and rat (M. Fournier, unpublished observations; see also Ref. 20, Fig. 7A) and their total absence in the cat (15). Muscle spindles were also recently reported to be numerous in the Sca of the dog (10). Because the Sca of the dog exhibits no respiratory function even under loaded conditions (10), the proprioceptive role of the Sca in this species may be limited to its postural function. In the hamster, it is possible that afferent activity from Sca muscle spindles is sufficiently augmented in response to an increase in respiratory load and/or a change in muscle length (as rib cage configuration is altered), to generate suprathreshold synaptic potentials in some Sca motoneurons. This may reflect the graded activation of selective Sca motor units as inspiratory demand is increased. The findings of the present study are in agreement with such a proposal.
Positional and/or anatomical differences between the species may underlie some of the discrepancies observed in recruitment of the Sca. With quadrupedal species such as the hamster, the caudal displacement of the rib cage may be less marked, whereas the gravitational pull may be substantial in upright humans. In fact, in humans the EMG activity of the Sca while in upright position was reported to be much greater than in supine position (11, 14, 32), suggesting that the gravitational load on the rib cage is increased in that case. In contrast, in lightly anesthetized baboons, no differences between supine and head-up posture was observed in the Sca during eupnea (12). Similarly, in the present study with awake animals, during resting ventilation, the Sca either remained silent or exhibited only nonrespiratory activity when the hamster was standing upright on its hindlimbs against the side of the cage. Other positional changes were also tested on several occasions during quiet breathing in the anesthetized hamster such as a shift from supine to prone or lateral decubitus positions. In either position, the medial Sca remained similarly inactive. However, these changes in position were not systematically studied in all animals. By contrast, others have shown that the activity of the medial Sca can be modulated by positional changes in the rat during non-REM sleep (22). For example, the greater the degree of "curl-up" posture, the greater the inspiratory activity of the medial Sca.
Differences in muscle architecture, in chest wall configuration, or in the strength of respiratory drive may also be factors contributing to the discrepancy among species. In the rat, the medial Sca inserts onto the ribs, as low as rib 6 (22), which is intermediate between the hamster (mainly at rib 4) and the dog (as low as ribs 7 or 8; 10). Unlike in quadrupeds, the medial Sca in humans is limited to insertions onto the first rib only (31). With such wide differences regarding muscle insertions onto ribs, the pattern of chest movement during breathing which might be accounted for by contraction of the Sca would be expected to differ among the species. These structural differences may also be designed to accommodate chest wall compliance that may vary greatly among species. In general, in adult mammals, the smaller the body size, the more compliant the chest walls (19). This could therefore translate into reflex and/or dynamic mechanisms leading to recruitment strategies among respiratory muscles that also differ across species, to support and optimize ventilation.
In summary, our studies demonstrate the unique anatomical characteristics of the hamster Sca and support an accessory inspiratory role for the muscle. The recruitment of the Sca after a variety of challenging maneuvers (e.g., CO2 stimulation, resistive load, phrenicotomy, partial denervation) suggests that the muscle may play an important role under conditions of chronic load, such as those imposed by the hyperinflated state of emphysema.
ACKNOWLEDGEMENTS
The authors are grateful to Ling Tang and Xiaoyu Da for technical assistance. They also thank Dr. Sandra Howell for making equipment available for recording EMG activity.
FOOTNOTES
Address for reprint requests: M. Fournier, Div. of Pulmonary/Critical Care Medicine, Cedars-Sinai Medical Center, 8700 Beverly Blvd., Rm. 6732, Los Angeles, CA 90048 (E-mail: fournierm{at}csmc.edu).
Received 18 September 1995; accepted in final form 6 August 1996.
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