Regional patterns of pectoralis fascicle strain in the pigeon Columba livia during level flight
Concord Field Station, Department of Organismic and Evolutionary Biology, Harvard University, Old Causeway Road, Bedford, MA 01730, USA
* Author for correspondence (e-mail: biewener{at}fas.harvard.edu)
Accepted 6 December 2004
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Summary |
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In-series segment strains differed from 2% to 17.2%, averaging differences of 6.1% at the Ant SB site and 1.4% at the Mid SB site. Temporal patterns of in-series fascicle segment strain were similar at both sites. Regional fascicle strains also exhibited similar temporal patterns of lengthening and shortening and were most uniform in magnitude at the Ant SB, Mid SB and TB sites (total strain: 33.7%, 35.9% and 33.2% respectively), but were smaller at the Post SB site (24.4%). Strains measured along the aponeurosis tracked the patterns of contractile fascicle strain but were significantly lower in magnitude (19.1%). Fascicle lengthening strains (+25.4%) greatly exceeded net shortening strains (-6.5%) at all sites.
Much of the variation in regional fascicle strain patterns resulted from
variation of in vivo recording sites among individual animals,
despite attempts to define consistent regions for obtaining in vivo
recordings. No significant variation in EMG activation onset was found, but
deactivation of the Ant SB occurred before the other muscle sites. Even so,
the range of variation was small, with all muscle regions being activated
midway through lengthening (upstroke) and turned off midway through shortening
(downstroke). While subtle differences in the timing and rate of fascicle
strain may relate to differing functional roles of the pectoralis, regional
patterns of fascicle strain and activation suggest a generally uniform role
for the muscle as a whole throughout the wingbeat cycle. Shorter fascicles
located in more posterior regions of the muscle underwent generally similar
strains as longer fascicles located in more anterior SB regions. The resulting
differences in fiber length were accommodated by strain in the intramuscular
aponeurosis and rotation of the pectoralis insertion with respect to the
origin. As a result, longer Ant and Mid SB fascicles were estimated to
contribute substantially more work per unit mass than shorter Post SB and TB
fascicles. When the mass fractions of these regions are accounted for, our
regional fascicle strain measurements show that the anterior regions of the
pectoralis likely contribute 76%, and the posterior regions 24%, of the
muscle's total work output. When adjusted for mass fraction and regional
fascicle strain, pectoralis work averaged 24.7±5.1 J kg-1
(206.6±43.5 W kg-1) during level slow (4-5 m
s-1) flight.
Key words: muscle, pectoralis, strain, work, flight, bird, sonomicrometry
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Introduction |
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Recent cine-MRI imaging studies of the human biceps brachii
(Pappas et al., 2002) and
soleus (Finni et al., 2003
)
muscles and X-ray imaging of the rat soleus muscle
(Monti et al., 2003
),
demonstrate non-uniform patterns of fascicle and/or muscle-tendon aponeurosis
strain when the human muscles shortened at low to moderate forces and the rat
soleus contracted isometrically in situ. In vivo measurements of
strain in human soleus and gastrocnemius muscles using ultrasound also show
the compliant nature of aponeurosis and tendon during walking and
counter-movement exercises (Fukunaga et
al., 2001
; Kawakami et al.,
2002
; Narici et al.,
1996
). In their study of the human biceps brachii, Pappas et al.
(2002
) found that distal
fascicles near the biceps tendon strained less than those located centrally
within the muscle. Similarly, a recent study
(Ahn et al., 2003
) of a less
complex muscle, the semimembranosus of the American toad (Bufo
americanus, after Linneaus: source for all other taxonomic
identifications reported), also showed heterogeneous strain patterns when
fascicle segments along the muscle's length were recorded using sonomicrometry
under both in vivo and in vitro conditions. Ahn et al. found
that proximal and central fascicle semimembranosus segment strains were much
larger and differed substantially in pattern compared with strains recorded in
the distal region, similar to the pattern observed in the human biceps brachii
(Pappas et al., 2002
).
Heterogeneous strains in the toad semimembranosus occurred despite the muscle
segments exhibiting similar electromyographic (EMG) patterns of activation.
The growing evidence that strain heterogeneity may occur along fascicles and
between different regions on a whole muscle level reinforces patterns observed
previously in single isolated muscle fibers (e.g.
Edman and Flitney, 1982
;
Edman and Reggiani, 1984
;
Kawakami and Lieber, 2000
).
Nevertheless, it is noteworthy that other studies have found homogeneous
patterns of strain along single fibers
(Cleworth and Edman, 1972
;
Mutungi and Ranatunga, 2000
),
consistent with general assumptions made in past studies of whole muscle
function.
In general, architecturally complex muscles are believed to allow for
regional specialization of a muscle's function. Compartmentalization of a
single muscle into functionally distinct neuromuscular regions has been
described for several larger mammalian muscles, such as the cat gastrocnemius
and plantaris (English, 1984;
English and Letbetter, 1982
),
the cat biceps femoris and semitendinosus
(Chanaud and MacPherson, 1991
;
English and Weeks, 1987
), the
pig masseter (Herring et al.,
1979
,
1989
), and the rat gluteus
maximus (English, 1990
).
Neuromuscular compartments are defined by having discrete motor unit
territories and fiber type characteristics, and their presence suggests that
the functional role of a muscle may be varied based on regionally differential
recruitment. To date, functional specialization within a muscle has largely
been based on fiber architecture and histochemical features, motor unit
territory, and differential patterns of EMG activation. When combined with
recent observations of heterogeneous in vivo strain patterns within
skeletal muscles, these studies reinforce the view that regional differences
in fascicle strain may be correlated with recruitment of distinct
neuromuscular compartments to provide varying functional roles for a single
muscle.
In light of these observations, the goal of our present study was to
investigate regional patterns of in vivo fascicle strain and EMG in
the pectoralis muscle of the pigeon Columba livia in greater detail
than has been done previously. The avian pectoralis is a large and
architecturally complex muscle, with fibers differing in both orientation and
length. In addition to providing the major downward motion of wing for
aerodynamic lift, the pectoralis may also rotate (pronate) the wing at the
shoulder. The muscle may therefore contract differentially to depress and
rotate the wing during different phases of the downstroke, as well as in
relation to differing modes of flight
(Dial et al., 1988).
The pectoralis muscle of birds is divided into sternobrachial (SB) and
thoracobrachial (TB) regions, based on their origins from the body and their
attachment to a large central aponeurosis (APON), or membrana intramuscularis,
which runs from the muscle's tendinous insertion on the deltopectoral crest
(DPC) of the humerus for a distance of about two thirds of the muscle's length
(Fig. 1; Baumel, 1993). Whereas the more
posterior fibers of the SB and all of the TB fibers insert onto the central
aponeurosis, the more anterior SB fibers insert directly onto the DPC. Kaplan
and Goslow (1989
) showed that
the pigeon pectoralis is innervated by two main nerve branches: a rostral
branch that innervates the anterior SB and a caudal branch that innervates the
posterior SB and TB. This led Boggs and Dial
(1993
) to hypothesize a
rostro-caudal pattern of activation and functional recruitment from more
anterior SB to more posterior SB and TB motor units of the muscle
(Sokoloff et al., 1998
). Boggs
and Dial (1993
) observed that
EMG recordings obtained from multiple regions of the pectoralis SB and TB
during take-off, level slow flight, and landing flight appeared to support
this hypothesis, with TB fibers being activated later than the most anterior
SB fibers.
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In a related study, Biewener et al.
(1998) examined in
vivo fascicle strains in the anterior and middle SB regions of the pigeon
pectoralis (termed `anterior' and `posterior' in their study) in relation to
DPC measurements of muscle force obtained under similar conditions of slow
level flight. Significant differences in the magnitude and pattern of fascicle
length change relative to muscle force (i.e. `work loop' behavior) were
observed, in part due to a difference of 6% strain between the two sites
(relative to a total fascicle strain range of 32%). Temporal patterns of EMG
activation relative to fascicle strain were uniform. Although this earlier
study provided an initial assessment of fascicle strain patterns at these two
sites, it did not assess broader patterns of regional muscle strain,
particularly in more posterior regions of the pectoralis. The goal of the
present study was to expand our analysis of regional in vivo fascicle
strain patterns within the avian pectoralis, in addition to assessing
`in-series' segment strains along individual fascicles. As before,
measurements of regional strain and activation pattern are related to the
muscle's role in producing motions of the wing at the shoulder associated with
generating aerodynamic power for flight.
In carrying out this analysis, we test two hypotheses. The first is that
in-series segment strains are uniform along the length of a fascicle. This is
generally assumed in studies of whole muscle function. The second hypothesis
is that regional fascicle strains within the pigeon pectoralis vary inversely
with fascicle length. That is, we hypothesize that short fascicles undergo
larger strains than long fascicles. Our second hypothesis arises from the fact
that, despite its extremely broad origin (arising from the thoracic ribs,
enlarged sternal carina and furcula), the pectoralis has a short focal
tendinous insertion on the ventral surface of the DPC
(Baumel, 1993), requiring that
fascicles of different length must accommodate (i.e. produce) similar whole
muscle length changes. This suggests that shorter, more posterior SB and TB
fascicles may undergo greater strains than longer fascicles located in the
anterior and middle SB regions. Alternatively, it is possible that variation
in the series elastic compliance among fascicles within the muscle and
rotation of the muscle, as a whole, may allow shorter fascicles to strain
similarly to long fascicles. Because shorter TB and posterior SB fascicles
insert along the length of the muscle's intramuscular aponeurosis, the
muscle's aponeurosis likely represents a significant component of the series
elastic compliance of these posterior fascicles. This component is lacking
with respect to more anterior SB fibers, which do not insert along the
aponeurosis. Hence, our alternative hypothesis is that regional fascicle
strains are uniform despite differences in fascicle length. To explore this we
made in vivo strain recordings along the aponeurosis, in addition to
those made along the fascicles.
Hypotheses of uniform strain along the length of a fascicle and among
different regions within a muscle not only assume uniform strain within
sarcomeres of individual fibers, but also between fibers that are arranged
in-series, or overlap, and do not traverse the entire length of the
fascicle(s). This is the case for fibers within the avian pectoralis
(Gaunt and Gans, 1993;
Trotter et al., 1992
), as well
as for other long fibered, strap-like muscles in certain mammals and
amphibians (see Trotter et al.,
1995
, for a review). Consequently, whereas force transmission
via shear transfer between adjacent contracting muscle fibers and
their surrounding connective tissue matrix may ensure more uniform strain and
effective force transmission along the muscle's length, an in-series fiber
arrangement raises the possibility that heterogeneous patterns of strain may
arise along the length of a muscle's fascicles. Assessing the nature and
magnitude of strain along a fascicle's length and among different regions of a
muscle are of considerable significance for calculating the work and power
that a muscle performs. Often this is based either on an indirect assessment
of total muscle length change or, more recently using sonomicrometry, one or
two localized measures of in vivo fascicle strain
(Askew et al., 2001
;
Biewener and Corning, 2001
;
Biewener et al., 1998
;
Daley and Biewener, 2003
;
Gabaldón et al., 2004
;
Hedrick et al., 2003
;
Roberts et al., 1997
;
Tobalske et al., 2003
), from
which whole muscle length change is calculated assuming uniform strain
throughout the muscle. If fascicle strains vary inversely with their length
(hypothesis 2), then a localized measurement may be prone to underestimating
or overestimating total muscle work and power.
The avian pectoralis is an ideal muscle for examining in-series and regional fascicle strain patterns using sonomicromety because its superficial fascicles are accessible to study. Given the muscle's complex architecture and central role in flight, quantification of its regional pattern of fascicle strain not only offers an important test of strain uniformity on a whole muscle level and allows fascicle contractile strain patterns to be related to intramuscular series elastic compliance, but provides insight into whether neuromuscular recruitment patterns may be linked to the pectoralis' role in the control of wing motion for maneuvering and unsteady flight, as well as serving as the main flight motor for generating aerodynamic power.
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Materials and methods |
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Surgical procedures
After training was complete sterilized sonomicrometry (SONO) crystals and
electromyography (EMG) electrodes were implanted in different regions of the
pectoralis and a strain gauge was attached to the deltopectoral crest of the
humerus. The pigeons were anesthetized using isoflurane administered
via a mask (3% for induction and 2-3% during surgery, at a flow rate
of 0.4 l min-1). Once an appropriate level of anesthesia was
induced, the feathers over the left shoulder, left pectoralis and upper back
were plucked and removed. Surgical areas were isolated by taping back
surrounding feathers and scrubbed with betadine solution. A 2-3 cmincision was
then made in the skin over the pigeon's back between its wings, and a 6 cm
incision was made along the ventral surface of the left pectoralis (near the
base of the sternum). Ten 2.0 mm sonomicrometry crystals (38 AWG, SonoMetrics
Corp., London, Canada) and four fine-wire bipolar EMG electrodes were then
passed from the back, subcutaneously beneath the wing, to the opening over the
pectoralis.
The SONO crystals were inserted within the pectoralis along fascicles in four defined regions of the muscle, identified as: anterior sternobrachialis (Ant SB, N=5), middle SB (N=5), posterior SB (N=4), and thoracobrachialis (TB, N=4) (Fig. 1). In three of the animals sonomicrometry crystals were implanted along the intramuscular aponeurosis (APO) - also known as the membrana intramuscularis, instead of the Post SB or TB sites. In these cases, the EMG electrode was implanted in muscle fascicles inserting onto the aponeurosis from the posterior SB region of the muscle. In addition to regional fascicle strain measurements made at these five sites, we also obtained in-series fascicle strain recordings at the Ant SB and Mid SB sites by implanting three crystals along the fascicle, with the central `pinging' crystal emitting a sound pulse that was received by the more proximal and distal crystals adjacent to it (Fig. 1A).
All crystal pairs were implanted at a depth of 4 mm beneath the
superficial fascia of the muscle and at a distance of
10-12 mm apart. The
crystals were implanted in small openings made parallel to the fascicles by
puncturing the muscle surface and gently spreading with small sharp-pointed
scissors. After being inserted into the muscle, crystal pairs were aligned to
ensure maximum signal quality that was displayed on an oscilloscope during the
surgery. The openings were then closed using 4-0 silk suture. Suture ties were
also made to anchor the sonomicrometry crystal lead wires to the pectoralis
3-5 mm away from the implantation site to prevent movement artifacts in
the recorded signals. Silver fine-wire (0.1 mm diameter, California Fine Wire,
Grover Beach, CA, USA), 1 mm bared tip, twisted offset hook, bipolar EMG
electrodes were inserted adjacent to the crystal sites using a 23-gauge
hypodermic needle and anchored to the pectoralis with 3-0 silk suture.
Throughout the procedure, sterile saline was used to keep the muscle moist.
After the SONO crystals and EMG electrodes were implanted, the ventral opening
over the pectoralis was sutured.
The animal was then positioned to attach a strain gauge to the DPC of the
humerus to obtain in vivo bone strain recordings of muscle force. The
dorsal surface of the DPC was first exposed by making a 15 mm incision
over the left shoulder and retracting the overlying deltoid muscle. A small
single-element metal foil strain gauge (1 x2 mm active grid, type
FLA-1-11; Tokyo Sokki Kenkyujo Co., Ltd., Tokyo, Japan) was then passed
subcutaneously from the opening over the back to the opening over the
shoulder. Next the periosteum of the DPC was removed by lightly scraping with
a scalpel, and the bony surface dried using a cotton applicator dipped in
methyl-ethyl ketone. After this, the strain gauge was bonded to the dorsal
surface of the DPC, perpendicular to the humeral shaft, using a
self-catylizing cyanoacrylate adhesive. During the downstroke, the DPC is
pulled ventrally by the contracting pectoralis, so that the dorsal surface
develops a principal axis of tensile strain that is nearly perpendicular to
the long axis of the humerus (Dial and
Biewener, 1993
). This makes the strain gauge sensitive to forces
produced by the pectoralis but not to other muscle or aerodynamic forces
transmitted by the bone between the elbow and the shoulder. This approach has
been used in our previous studies (Dial
and Biewener, 1993
; Biewener et
al., 1998
; Tobalske et al.,
2003
) to record in vivo flight forces from calibrated DPC
bone strain recordings. After bonding the strain gauge to the DPC, a miniature
`back plug', consisting of three Microtech (3xGM-6, Boothwyn, PA, USA)
connectors to which the SONO, EMG and strain gauge lead wires were
pre-soldered and insulated with epoxy, was secured to thoracic vertebral
ligaments over the pigeon's back using 2-0 silk suture. The remaining skin
incisions were then sutured with 3-0 silk and the pigeons were allowed a 24 h
period for recovery prior to carrying out experimental flight recordings.
Experimental recordings
Multiple (15-26) flight trials were recorded from each bird over the period
of the following day, and 5-7 representative trials were selected from each
individual for analysis. In each trial, 11 wingbeats representing the three
main phases of flight were studied. Based upon the sonomicrometry recordings
of muscle fascicle length change, the first three wingbeats of a trial were
considered to represent the `take-off' period of flight, the five middle
wingbeats of the trial as `level flight', and the last three recorded
wingbeats as representative of the `landing' period of flight.
All signals were transmitted from the bird to the recording equipment via a lightweight 4.5 m long multi-lead shielded cable (4 x6-lead cable, type NMJF6/30-4046SJ, Cooner Wire, Chatsworth, CA, USA) from the back plug connector on the bird. The weight of the unsupported portion of the cable that trailed behind the animal was estimated to be 33.5 g, about 6% of the birds' mean body mass. Outside the flight corridor, the lightweight cable was distributed via heavier, shielded cable to the recording amplifiers (one Micromeasurements Vishay 2120A strain gauge bridge amplifier, Raliegh, NC, USA; four Grass P-511 EMG amplifiers, West Warrick, RI, USA; and two 4-channel Triton 120.2 sonomicrometry amplifiers, San Diego, CA, USA). The outputs from these amplifiers were sampled by an A/D converter (Axon Instruments, Digidata 1200, Union City, CA, USA) at 5 kHz and stored on a computer for subsequent analysis. The EMG signals were amplified 1000 x and filtered (60 Hz notch, 100-3000 Hz bandpass) before sampling. Sampled EMG signals were subsequently bandpass filtered from 40 to 1500 Hz, using a 4th order zero-lag digital butterworth filter. Sonomicrometer and strain gauge recordings were also filtered after sampling, using a 4th order zero-lag digital Butterworth 40 Hz low pass filter to remove high frequency noise introduced by the multiple sonomicrometry leads in the cable.
DPC force calibration and morphometrics
Following the flight trials, the pigeons were euthanized with an overdose
of sodium pentabarbitol delivered intravenously via the brachial
vein. The distal portion of the pectoralis muscle was then exposed beneath its
attachment to the ventral surface of the DPC and a 00 silk suture made around
the entire muscle. The silk suture was then attached to a force transducer
(Kistler 9203, Amherst, NY, USA), and a series of pull calibrations were
performed with the bird held by hand and tension applied along the muscle's
main axis to the DPC. A linear regression of the rise and fall of DPC strain
versus measured force, sampled via the computer's A/D
converter, was used to determine a dynamic calibration for pectoralis force
(Biewener et al., 1998).
After calibrating the DPC strain gauge, the entire pectoralis was then exposed to verify EMG electrode and SONO crystal placement. In all cases, the SONO crystals were aligned within 2° of the fascicle axis, so that errors due to misalignment were <0.1%. The pectoralis muscle was then dissected free from its skeletal attachments and photographed using a 5.2 megapixel digital camera, with ruler in view for length calibration. Measurements of pectoralis mass, fascicle length (Table 1) and fascicle orientation relative to each sonomicrometry crystal pair were then obtained using digital calipers and a digital balance. Measurements of fascicle length, pinnation angle, and the coordinate positions of the sonomicrometry recording sites were also determined from the digital images using using NIH ImageJTM (Fig. 1B). Fascicle length measurements agreed closely with those measured using calipers directly on the muscle. A tracing obtained from the digital image of the pectoralis from pigeon 5 was also used to construct a two-dimensional (2D) geometric model to assess how measured patterns of fascicle and aponeurosis strain related to overall length and shape changes of the muscle during a wingbeat cycle. The model predicted the instantaneous position of the SONO crystals from their resting position and the instantaneous fascicle and aponeurosis strains. Computations for the geometric model were carried out in MATLAB R13 (The MathWorks, Natick, MA, USA). Coordinates for the sonomicrometry recording locations of each muscle were referenced to the caudal base of the muscle in order to determine average coordinates for each defined recording site (Ant SB, Mid SB, Post SB, TB and APO) and to assess the variation in recording sites among animals (Fig. 1B).
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For the purposes of estimating regional contributions of fascicle strain to overall pectoralis work output, fractional masses of the different pectoralis regions, from which sonomicrometry measurements of fascicle strain had been obtained (Fig. 1), were then determined by sectioning the muscle through its depth midway between the adjacent SONO recording sites and recording the separate masses of the muscle regions on a balance. Fractional masses of the different regions reported in Table 1 were then used to calculate the fractional work component of each region to total muscle work. Even so, this approach relies on using the same time-varying measurement of whole muscle force obtained from our DPC strain recording applied to the individual regional fascicle strain recordings to estimate regional contributions of muscle work.
Sonomicrometry
Sonomicrometry techniques and analysis to measure in vivo fascicle
length changes followed those of Biewener and Corning
(2001) and Biewener et al.
(1998
). Signals from the Triton
120.2 amplifier were adjusted for the 5 ms delay introduced by the Triton's
filter and were corrected for offset errors (underestimate of length: 0.82 mm
for the 2.0 mmcrystals) introduced by the greater speed of sound through the
epoxy coating of each crystal compared with the muscle, as well as a 2.7%
correction to account for the greater speed of sound through skeletal muscle
(1540 m s-1; Goldman and
Hueter, 1956
) versus water (1500 m s-1).
Fractional length changes, or fascicle strains
(
Lseg/L0), were calculated
based on segment length changes measured between the crystals
(Lseg) relative to their resting length
(L0), measured when the birds stood quietly at rest on the
perch.
To confirm that the fascicle strains measured during the course of this
investigation were representative of particular regions of the muscle, we
assessed the repeatability of our measurements by also collecting a second set
of SONO measurements from adjacent sites of the anterior and mid SB regions of
pigeon 5. In this bird, measurements were first recorded from the Ant SB, Mid
SB, Post SB, and the TB regions, after which the crystals in the Ant SB and
Mid SB regions were re-implanted 5 mm rostrally (toward the furcula)
relative to their original positions. Following a second 24 h recovery period,
experimental recordings were again made for the same flight conditions to
compare the adjacent sets of strain measurements obtained at the Ant SB and
Mid SB sites.
Statistical analysis
Two-factor analysis of variance (ANOVA) was used to test for differences in
regional strain measurements, for strain differences between in-series
fascicle strain measurements at the Ant SB and Mid SB sites. The factors
considered in the ANOVA analyses were the bird and the fascicle location; we
report F and P values for the location factor. Data were
considered independent at the trial level, values for a particular trial were
determined by computing the mean for all wingbeats in that trial. Results were
considered significant at P<0.05. All computations were performed
using the MATLAB R14 Statistics Toolbox (The MathWorks, Natick, MA, USA).
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Results |
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Regional strain patterns
Regional in vivo fascicle strain recordings obtained from
different sites distributed throughout the pectoralis also exhibited
consistently similar patterns of strain with respect to the timing of muscle
activation and force development (Fig.
4). Although differing sites exhibited variation in the magnitude
of lengthening and (net) shortening strain (Figs
4 and
5;
Table 3), all sites lengthened
and shortened at generally similar times. Similar temporal patterns of strain
also corresponded to uniform patterns of EMG activation (Figs
4A,B and
6). Fascicles within the TB
region generally showed the largest difference in strain pattern, exhibiting a
slight delay in the onset of fascicle shortening. In addition, lengthening
strains recorded from the Post SB region were lower in magnitude than
lengthening strains recorded at the other fascicle sites, resulting in lower
overall Post SB strains. Strains measured along the intramuscular aponeurosis
(Figs 4B,C and
5) were substantially less than
those recorded along fascicles at all muscle sites. Figs
4C and
6 also show that APO strains
are slightly delayed in timing; i.e. shortening begins and ends slightly later
than in the fascicles. However, the temporal pattern of APO lengthening and
shortening generally mirrored fascicle strain patterns and was not significant
different. Significant variation (P<0.0001) in regional pectoralis
strain magnitude was observed (Table
3). When compared across all animals for which recordings were
obtained at each muscle site, total strains at the Ant SB, Mid SB and TB sites
were generally uniform, averaging 33.7±4.2%, 35.9±4.6%, and
33.2±5.8%, in contrast to 24.4±6.0% at the Post SB site and
19.1±3.9% along the aponeurosis. For all sites, the magnitude of
lengthening strain (mean for all sites: +25.4±4.7%) greatly exceeded
net shortening strain (-6.5±0.9%) relative to the muscle's resting
length (Figs 4,
5).
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Implications for pectoralis shape change
Based on the average strains recorded at each fascicle site and along the
aponeurosis among the six pigeons, we constructed a two-dimensional geometric
model of the pectoralis to assess how the recorded patterns of muscle strain
related to its overall length and shape changes during a wingbeat cycle.
Variation among animals in the recording locations of the regional fascicle
strain measurements determined from the digital images was substantial
(Fig. 1B), and likely
contributed to some of the inter-individual variation in strain magnitudes
recorded at each site. Fig. 7
shows the results of our model for three time points during the wingbeat
cycle: maximum strain (for the mid SB site, start of downstroke), maximum
pectoralis force (measured from the DPC strain gauge), and minimum strain (for
the mid SB site, end of downstroke). At maximum strain
(Fig. 7A), the displacement of
the more anterior fascicles, relative to their resting position, and their
distal attachment to the DPC is mainly in a superior direction, consistent
with the humerus and wing being in their maximally elevated position at this
time. Additionally, there is evidence of a posterior displacement of the Ant
and Mid SB fascicles, suggesting humeral retraction in combination with
elevation during the upstroke. Strain in the TB fascicles also results in an
upward but more anterior displacement, whereas strain of the post SB region is
mainly in the anterior direction. The strain patterns and resulting
displacements suggested by the 2D muscle model indicate that significant
fascicle rotation occurs, in addition to lengthening strain. Strains and
displacements of the muscle at the time of peak pectoralis force
(Fig. 7B) are consistent with
past observations in pigeons and other birds that the pectoralis develops peak
force when it remains stretched near to its maximum length approximately
one-third through the downstroke. At minimum strain
(Fig. 7C), the displacement of
the fascicles is generally posterior to their resting positions. In all but
the TB site, the displacements are also in a ventral direction, consistent
with maximal depression of the humerus and arm wing at this time. The TB site
suggests a relative dorsal movement, but this (and the modeled `wrinkling' of
the aponeurosis along its length) is likely the result of our simple 2D model
of the muscle, which ignores out-of-plane strains that are certain to affect
the muscle's overall geometry. Displacements at minimum strain are small
relative to those at maximum strain, consistent with fascicle lengthening
contributing fourfold more than net fascicle shortening
(Fig. 5) to overall fascicle
shortening during the downstroke.
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Fascicle strain versus resting fascicle length
Least-squares regression (Fig.
8) showed no significant (r2=0.14;
P>0.05) relationship between total fascicle strain and a
fascicle's resting length. Indeed, rather than an inverse relationship being
observed, the trend suggests a positive though weak correlation between strain
and fascicle length.
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Timing of regional muscle activation and fascicle strain relative to force
Regional EMG patterns of pectoralis activation were highly uniform. No
significant differences (P>0.05, two-way ANOVA considering bird
and implant location) were observed among individuals in terms of EMG onset,
but EMG offset differed significantly within the muscle, with the anterior
sternobrachialis offset occurring before the rest of the muscle
(P<0.05, two-way ANOVA and Tukey-Kramer post-hoc test,
Fig. 6). Similarly, EMG onset
times varied by less than 2 ms and EMG offset times by less than 3 ms in those
individuals for which the most significant regional differences were observed.
Within all individuals and at all muscle locations the pectoralis was
activated midway through lengthening during the upstroke and was deactivated
about midway through shortening during the downstroke, EMG activation
generally preceded the onset of muscle force by 3-8 ms and ended 5-15 ms after
the muscle had developed peak force (Fig.
6). EMGs recorded from fascicles immediately adjacent to the
intramuscular aponeurosis were generally delayed 5-10 msrelative to the timing
of EMGs recorded along fascicles at sites further from the aponeurosis.
Regional muscle work-loop patterns
Fig. 9 shows regional work
loops generated by different regions of the pectoralis muscle in two pigeons
that displayed the greatest variation in work loop pattern. Work loops are
plotted with fascicle length expressed as both strain
(Fig. 9A,C) and length
(Fig. 9B,D). Fascicle strains
recorded at all sites relative to pectoralis force resulted in work loops that
are entirely counter-clockwise. Note, however, that variation in work loop
pattern among sites is wholly dependent on variation in the magnitude and
pattern of fascicle length change relative to muscle force recorded at the DPC
strain gauge site (the actual work loop behavior of individual fascicles would
require independent isolated intramuscular force measurements, which are not
possible). Because the more posterior regions (Post SB and TB) of the muscle
have both shorter fascicles and reduced strains, their contribution to the
mechanical work output of the muscle, as a whole, was substantially reduced
compared to more anterior SB regions (Figs
9 and
10;
Table 4). Net mechanical work
(loop area) among sites varied by over twofold in pigeon 1 and 1.7-fold in
pigeon 5. The other pigeons (not shown) exhibited similar variation in the net
work output among different fascicle regions
(Table 4). For the trials shown
in Fig. 9, cycle duration was
0.114 s, resulting in power outputs that ranged from 20.5 to 7.9 W. Overall,
the pigeons' wingbeat frequency averaged 8.47±0.4 Hz (0.118 s cycle
duration).
|
|
|
To estimate the fractional contributions of the different regions to total
muscle work and power output, we related the net work and power output
measured at individual fascicle recording sites
(Fig. 9) to the fractional
muscle mass represented by each site (Table
1). Fig. 10 shows
the inter-individual means (± S.E.M.) of the fraction of
total pectoralis mass estimated for each region (open bars) together with the
fraction of mass-weighted work that each region generated (shaded bars). These
data are also reported in Table
4, which shows the regional muscle work estimated for each site
and mean total muscle work performed by the pectoralis as a whole (1.282 J),
together with the fractional work estimated for each region. Fractional mass
(34%) and work output (43%) was largest in the Ant SB region, followed by the
Mid SB (28% mass, 33% work). Because strains at these two sites were greater
than those recorded at the Post SB site, and Ant and Mid SB fascicles are much
longer than fascicles in the Post SB and TB sites, the Ant and Mid SB regions
of the muscle were estimated to produce a disproportionate amount of work
compared with the Post SB (17% mass, 11% work) and TB (21% mass, 13% work)
regions. Thus, regional fascicle strains indicate that the anterior regions of
the pectoralis contributed 76%, and the posterior regions 24%, of the muscle's
total work output. When adjusted for mass fraction and regional fascicle
strain, pectoralis work for the six pigeons averaged 2.564 J (for the left and
right pectoralis combined), or 24.7±5.1 J kg-1 muscle. This
corresponds to a power output of 21.7 W based on the mean cycle duration
across individuals (0.118 s), or 206.6±41.5 W kg-1 muscle
during level slow (4-5 m s-1) flight.
Repeated strain measurements in adjacent fascicles
Strains recorded on sequential days in adjacent parallel sites (5 mm
apart) in the anterior and mid SB regions of the pectoralis muscle of pigeon 5
resulted in strains that differed by as little as 1.1±0.7% (proximal
Mid SB) to as much as 10.3±0.9% (proximal Ant SB), with an average
difference of 3.7±0.9% among the four adjacent sites sampled
(P<0.05; d.f.=7; Fant=20.0;
Fmid=43.3). Although not shown, no discernible differences
in the temporal pattern of strain between adjacent sites were observed.
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Discussion |
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In-series fascicle strain and strain heterogeneity
Recordings of in-series fascicle segment strains in the Ant SB and Mid SB
regions of the pectoralis showed frequent instances (9 of 12 cases) in which
significant differences in strain magnitude were observed along individual
fascicles, with strain differences ranging from 2.0 to 17.2% strain. When
averaged across animals the differences were 6.2% between proximal and distal
Ant SB segments and only 1.4% between proximal and distal Mid SB segments.
Although the in-series strain measurements within individual animals
contradict our hypothesis that fascicles strain uniformly along their length,
when averaged across animals the results provide stronger support for this
hypothesis. Heterogeneous strain patterns along individual fascicles have
recently been observed in the toad semimembranosus under both in vivo
and in vitro contractile conditions
(Ahn et al., 2003). Ahn et al.
found what when central and proximal semimembranosus fascicle segments
shortened during hopping, the distal segment was initially stretched before
shortening to a much smaller extent than shortening of the central and
proximal segments. Under in vitro isometric conditions, central and
proximal semimembranosus segments also shortened by stretching the distal
segment of the fascicle.
Such radically different patterns of fascicle segment strains observed in the toad semimembranosus were not observed here. Although the magnitude of strain often varied between Ant SB and Mid SB proximal and distal fascicle segments, the overall in-series strain pattern of pectoralis fascicle shortening and lengthening during the wingbeat cycle was quite uniform (Fig. 2). Our repeated measurements of in-series fascicle strain in pigeon 5 also indicate that up to 4% of the variation in strain magnitude observed at any given recording site may be attributable to variation in (at least our) experimental technique owing to differences in crystal alignment during implantation and motion relative to the fascicles to which the crystals are anchored.
Recent analyses of myofascial force transmission within and between muscles
(Huijing, 1999) show that
forces developed within a muscle can be transferred laterally to other
muscles. That muscle fibers do not operate as independent force generators is
reinforced by the work of Purslow and Trotter
(1994
), who showed that
structural linkages between muscle fibers and their endomysium and perimysium
likely function to provide lateral force transmission via shear
transfer from the fiber to its connective tissue matrix rather than solely
along the muscle fiber's (and fascicle's) axis. Consequently, localized
fascicle strains may not necessarily be uniform along a fascicle's length.
Recent studies using cine-MRI, ultrasound, and x-ray imaging have also found
regional differences in fascicle strain that may in part arise from in-series
strain heterogeneity (Pappas et al.,
2002
; Finni et al.,
2003
; Monti et al.,
2003
). Consequently, based on these findings and the results
observed here, it is clear that assumptions of uniform in-series fascicle
strain at the whole muscle level need re-examination and deserve further
study. Nevertheless, the generally consistent in-series fascicle strain
patterns that we observed when averaged across individual birds suggest that
interpretations of pectoralis muscle function in pigeons, and likely other
birds, based on a localized measurement of fascicle strain are qualitatively
robust and likely to yield reliable quantitative measurements of whole muscle
work and power.
Regional patterns of fascicle strain in relation to intramuscular series elastic compliance
Although different regions of the pectoralis showed little difference in
the timing of fascicle shortening and lengthening and EMG activation,
significant variation in the pattern and magnitude of fascicle strain was
observed among the four sites (Ant SB, Mid SB, Post SB and TB) sampled.
Regional differences in the magnitude of fascicle strain among these sites
were generally consistent across individual animals. As a result, significant
differences remained when strains for the four sites were averaged across the
six birds (Table 3).However, at
least some of the variation in regional strain pattern among individuals
likely resulted from experimental variation in the specific sites that were
targeted for implantation during surgery to quantify strain patterns for
different regions of the muscle (Fig.
1B). The greatest difference in fascicle strain magnitude occurred
within the posterior SB region. Although strains within the Ant SB and Mid SB
differed by an average of only 6% (average strain difference=0.022), strains
within the Post SB were 30% less (average strain difference: 0.104) than the
average for the Ant SB and Mid SB sites.
The much greater contribution of fascicle lengthening (+25.4±4.7%)
versus net fascicle shortening (-6.5±0.9%) to the total 32%
shortening strain of the pectoralis was also generally consistent for the four
sampled regions, and consistent with our earlier results for Silver King
pigeons flying under similar conditions (+20±5% and -12±4%;
Biewener et al., 1998). A
similar pattern of relative fascicle length change associated with shortening
work has also been observed in the pectoralis of cockatiels Nymphicus
hollandicus and doves Streptopelia risoria flying over a range
of speeds in a wind tunnel (+25±6% and -7±4%, total: 32%;
Hedrick et al., 2003
) and for
mallard ducks Anas platyrhynchos during ascending flight
(+22±4% and -8±3%, total: 30%;
Williamson et al., 2001
).
Although this might suggest a robust pattern for the avian pectoralis during
flight, Askew and Marsh (2001
)
found a more uniform pattern in blue-breasted quail Coturnix
chinensis during vertical take-off flight (+11±2% and
-12±2%, total: 23%), with even more limited lengthening (+8±2%)
versus net shortening (-14±2%) during horizontal flight. In
their study of take-off flight in four different-sized Phasianid species,
Tobalske and Dial (2000
) also
observed symmetric lengthening relative to shortening strains in the smallest
species (Northern bobwhite Colinus virginianus: +10±2% and
-9±3%, total: 19%) compared with the largest species (wild turkey
Meleagris gallopavo: +21±1% and -14±8%, total: 35%). In
addition to showing a scaling effect on total muscle shortening strain,
Tobalske and Dial's results also suggest that the relative contributions of
lengthening versus shortening strain may be size-dependent within the
Phasianidae, consistent with the results of Askew and Marsh
(2001
) for quail. However, as
cockatiels and ring-neck doves are generally intermediate in size relative to
both quail species, lengthening versus shortening strain patterns of
pectoralis almost certainly reflect other factors as well, such as wing
loading and wing shape, which are likely to affect pectoralis muscle strain
and wing stroke amplitude and which differ considerably between these
species.
When pooled across all recording sites and animals, regional fascicle strains within the pigeon pectoralis showed no evidence of an inverse relationship with fascicle length (Fig. 8). Although counter to our second hypothesis, this likely results from series elastic compliance within the muscle that allows shorter fascicles to strain more similarly to long fascicles and rotation of the fascicles about their origin. Strains measured along the aponeurosis averaged 19.1%, with APO shortening and lengthening occurring slightly after fascicle length change (Figs 4 and 6). This allows shorter, posterior fibers of the SB and all of the fibers of the TB that insert along the aponeurosis to undergo strains generally similar to (or even less than) the long anterior fibers of the SB (Fig. 1), as force is transmitted to the deltopectoral crest of the humerus.
A simple two-dimensional geometric model of the pectoralis, based on
average strains recorded in the aponeurosis and at the different fascicle
regions (Fig. 6), shows how
overall length and shape changes of the pectoralis in relation to local
fascicle strains are accommodated via compliance of the aponeurosis
and fascicle rotation. The results of this analysis demonstrate that more
anterior SB fascicles undergo substantial elevation as well as retraction at
maximum strain, which is likely mediated via fascicle rotation.
Rotation, in addition to linear strain, of fascicles during muscle contraction
is well documented in ultrasound imaging studies of human soleus and
gastrocnemius muscles (e.g. Fukunaga et
al., 2001; Narici et al.,
1996
). Strain displacements of more posterior fascicles are more
anteriorly and superiorly oriented. However, it is important to note that our
model, and the superficial fascicle strain measurements on which it is based,
do not account for out-of-plane forces and strains of the muscle, which are
likely to affect the relative magnitude and timing of aponeurosis strain
relative to those of the muscle's fascicles. As a result, distortions in the
shape change of the muscle (e.g. along the aponeurosis relative to the TB
fascicle) based on averaged relative strains for each region are observed, but
are unlikely to occur. Nevertheless, by mapping measurements of regional
muscle strain from localized sonomicrometry recordings onto a simple geometric
model of the muscle, we are able to show better how the pectoralis changes
length and shape over the course of a contraction cycle and how regional
differences in length change are accommodated by the muscle's internal
compliance.
Implications for muscle work and power
Our results show that normalizing local fascicle strain recordings to an
average fascicle length for the muscle, as a whole, provides the most reliable
assessment of whole muscle work and power. This has been the most common
approach for analyzing muscle work and power output under in vivo
conditions for birds in flight (Biewener et
al., 1998; Hedrick et al.,
2003
; Tobalske et al.,
2003
; Williamson et al.,
2001
) and for evaluating in vivo muscle function during
terrestrial locomotion (Biewener and
Corning, 2001
; Biewener et al.,
2004
; Daley and Biewener,
2003
; Gabaldón et al.,
2004
; Roberts et al.,
1997
). Because all fascicles contracted with similar strains, it
is likely that more posterior fascicles of the pigeon pectoralis contributed a
much smaller share to whole muscle work than the muscle's longer, more
anterior fibers. This cannot be stated with full certainty because local
forces within the fascicles were not measured. Nevertheless, our results
indicate that by applying a localized measure of fascicle strain to the
muscle's average fascicle length, regional differences in muscle work
can be accounted for with reasonable accuracy.
Because no difference in the timing of activation was observed among
fascicle regions, regional differences in muscle work are unlikely to reflect
regional differences in the role of the pectoralis in controlling motions of
the humerus and wing. Instead, the differing orientation and length of
fascicles in the pectoralis appear to be linked to an overall coordinated
movement of the humerus and wing, at least during level flight. Whether more
distinct patterns of regional muscle activation and strain within the
pectoralis occur during non-steady and maneuvering flight remains to be
determined. Our findings reinforce the view of the pectoralis as the principal
motor for flight, which produces a coordinated depression and (some degree of)
pronation of the wing during the downstroke for aerodynamic lift, whereas
other, principally more distal, wing muscles serve to adjust the wing's shape
and orientation during maneuvering and landing
(Dial, 1992). As a result,
differences in the timing of pectoralis activation and force development
relative to other muscles controlling the wing are likely most important for
adjusting movements of the wing to differing flight requirements, rather than
differential recruitment within the pectoralis itself.
Our measurement of 207±41.5 W kg-1 muscle for the Carneau
pigeon pectoralis observed here based on more detailed examination of regional
muscle strain patterns is more than twofold higher than our earlier
measurement of 108±29.6 W kg-1 (calculated as mass-specific
positive power, not net power, for equivalence here) obtained for the
pectoralis of Silver King pigeons (Biewener
et al., 1998) using similar methods but based on strain recordings
at only two sites (roughly corresponding to Ant SB and Mid SB). In both
studies average total pectoralis strains were similar (30-35%). Consequently,
most of the difference in muscle work and power must reflect differences in
pectoralis force measurement at the DPC. In both cases, our measurements of
pectoralis force and fascicle strain yield much lower values than Usherwood et
al. (2005
), who recently found
a value of 273 W kg-1 using direct wing pressure recordings to
estimate aerodynamic lift for smaller wild-type pigeons flying under similar
conditions. However, the coefficient of variation of these measurements is
high and Usherwood et al. do not attempt to evaluate the variation of their
estimate. In a study of cockatiels and ringed turtle doves flying at 4-5 m
s-1 in the CFS wind tunnel, Tobalske et al.
(2003
) observed
100 W
kg-1 for cockatiels and
150 W kg-1 for doves
(again, reported here as total positive power) based on in vivo
pectoralis force and strain recordings. These compare favorably with earlier
measurements of
85 W kg-1 pectoralis positive power for
black-billed magpies Pica pica obtained by Dial et al.
(1997
) during wind tunnel
flight at the same speed. Nevertheless, magpies have lower aspect ratio wings
and similar wing loading as cockatiels, and so would be expected to have
higher, not lower, power costs at a similar speed.
These differences in mass-specific muscle power output certainly reflect
differences and variation in experimental technique, as well as interspecific
differences in wing shape and wing kinematics. Tobalske et al.
(2003) note that calibration
of the DPC strain gauge may lead to some underestimate of muscle force.
However, the magnitude of this is difficult to assess. Achieving reliable
estimates of the mechanical power output of flight in different avian species
and across different flight conditions is of considerable interest. The
consistency of our regional measurements of pectoralis strain indicates that
estimates of whole muscle strain are likely more reliable than estimates of
whole muscle force. Consequently, refinement and improvements in force
measuring technique, combined with the application of novel techniques
(Hedrick et al., 2004
;
Usherwood et al., 2005
;
Spedding et al., 2003
) and
comparison of these techniques and approaches, including aerodynamic modeling,
are needed to improve our understanding of how the mechanical power
requirements of flight vary among species and flight conditions.
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Acknowledgments |
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