First published online February 4, 2005
Journal of Experimental Biology 208, 771-786 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01432
Regional patterns of pectoralis fascicle strain in the pigeon Columba livia during level flight
Arya Soman,
Tyson L. Hedrick and
Andrew A. Biewener*
Concord Field Station, Department of Organismic and Evolutionary
Biology, Harvard University, Old Causeway Road, Bedford, MA 01730,
USA
View larger version (24K):
[in a new window]
|
Fig. 1. (A) Recording sites within the pigeon pectoralis, showing the locations of
the sonomicrometry (SONO) crystals used to record in-series fascicle strain in
the anterior (Ant) and middle (Mid) regions of the sternobrachialis (SB)
portion of the pectoralis, together with SONO measurements obtained in the
posterior (Post) SB and thoracobrachial (TB) portion of the pectoralis to
assess regional patterns of fascicle strain. Electromyography (EMG) electrodes
were implanted immediately adjacent to the SONO crystal pairs. The middle SONO
crystal at the Ant and the Mid sites was used to `ping' the two opposing
receiving crystals to obtain adjacent in-series measurements of fascicle
segment strain at these two locations. Additionally, in three birds
measurements of aponeurosis (APO) strain were obtained to examine
series-elastic stretch of the aponeurosis resulting from forces transmitted to
the deltopectoral crest (DPC) from the TB and more posterior regions of the
SB. Measurements of overall muscle force were obtained from a strain gauge
attached to the dorsal aspect of the DPC, the ventral surface to which the
pectoralis has a tendinous insertion. See text for further details. (B) Map of
the pectoralis muscle based on digital images obtained from the muscles of the
six birds, showing the fascicle architecture and average recording locations
(magenta fascicles) for each muscle region. Measurements of fascicle length
and pinnation angle relative to the aponeurosis (shown in red) were determined
from the images and referenced to a coordinate system at eight defined points
along the SB and six points along the TB. To compare across animals, the
positions of the recording sites were normalized as a percentage of SB and TB
length relative to the caudal tip of the muscle. The locations (mean ±
S.D.) of the fascicle recordings sites is shown below.
|
|
View larger version (28K):
[in a new window]
|
Fig. 2. Representative in-series fascicle segment strain recordings obtained at the
anterior and middle SB pectoralis sites for two wingbeats during slow
( 4-5 m s-1) level flight, together with the EMG recorded from
the distal location in each instance. EMG signals were bandpass filtered from
40 to 1500 Hz and sonomicrometer fascicle strain recordings were low-pass (40
Hz) filtered using a 4th order zero-lag digital Butterworth filter. In
general, the pattern of fascicle strain (P>0.05 for time of
maximum and minimum strain) and timing of EMG activation (P>0.05)
were consistent across proximal and distal sites and at both locations among
the birds sampled. In-series fascicle strain magnitude was also generally
similar (in the cases shown for pigeon 3, distal fascicle strain averaged 3.5%
less than that recorded from the proximal site), with differences in strain
magnitude averaging less than 3.8% when proximal and distal sites were
compared across all individuals at both locations sampled (see
Table 2).
|
|
View larger version (15K):
[in a new window]
|
Fig. 3. Summary histogram showing in-series fascicle strains (mean ±
S.D.) measured at the anterior and middle SB regions of the
pectoralis among the five birds sampled.
|
|
View larger version (36K):
[in a new window]
|
Fig. 4. (A,B) Representative fascicle strain and EMG recordings obtained at the
four sampled regions of the pectoralis muscle, together with strain recordings
of the aponeurosis and overall muscle force obtained from the DPC strain
gauge. Recordings are for two wingbeats obtained from pigeons 1 and 3 during
slow (4-5 m s-1) level flight. EMG signals were bandpass
filtered from 40 to 1500 Hz, and sonomicrometer and strain gauge recordings
were low-pass (40 Hz) filtered, using a 4th order zero-lag digital Butterworth
filter. In-series proximal and distal segment strain measurements obtained at
the Ant and Mid SB sites were averaged to yield the overall patterns of
fascicle strain depicted here for those muscle sites. (C) Mean fascicle and
aponeurosis strains during a single wingbeat cycle based on data recorded from
all individuals for which recordings were made at each site. Data were
normalized to a full wingbeat cycle before being averaged, to maintain
temporal consistency across individual animals.
|
|
View larger version (17K):
[in a new window]
|
Fig. 5. Summary histogram showing regional patterns of fascicle strain (mean
± S.D.) measured at five sites (see
Fig. 1) within the pectoralis.
Note that strains measured along the intramuscular aponeurosis represent
passive length changes associated with series-elastic stretch of the
aponeurosis resulting from forces transmitted by the TB and posterior SB
fibers that insert on the aponeurosis.
|
|
View larger version (28K):
[in a new window]
|
Fig. 6. Summary histogram of the timing (mean ± S.D.) of muscle
activation and strain recorded from the different regions of the pigeon
pectoralis, together with total muscle force measured at the DPC. Time zero is
defined relative to when the pectoralis exerts peak force, with the force
histogram spanning the period of force development by the muscle. EMG
histograms span from the mean onset to the mean offset of the EMG. Strain
histograms span from the onset of muscle lengthening to the end of muscle
shortening. The central bar within the strain histograms represents the time
the muscle region reaches its peak length.
|
|
View larger version (19K):
[in a new window]
|
Fig. 7. Map of pectoralis fascicle architecture and geometry at three time points
during the downstroke: (A) maximum (Mid SB) strain at start of downstroke, (B)
maximum DPC pectoralis force, approximately one-third through downstroke, and
(C) minimum (Mid SB) strain at end of downstroke. Distal end displacements of
the defined fascicle regions shown as solid colored diamonds are referenced to
their resting position (open diamonds), proximal ends were fixed in position
and are shown as solid coloured circles. Displacements were determined using a
2D model of the pectoralis derived from digital images of the muscles that
were referenced to a calibrated coordinate system, based on fascicle lengths
and angles measured at eight defined points along the SB and six defined
points along the TB portions of the muscle. Fascicle displacements reflect the
average inter-individual strains recorded at each site, combined with their
average coordinate locations (see Fig.
1B).
|
|
View larger version (10K):
[in a new window]
|
Fig. 8. Total fascicle strain plotted versus fascicle length for level
flight, based on measurements obtained for all recordings sites in six
pigeons. No significant relationship between total strain and fascicle length
was observed (least squares regression: r2=0.144,
P>0.05).
|
|
View larger version (35K):
[in a new window]
|
Fig. 9. Work loops obtained from different regions of the pectoralis muscle in two
pigeons plotted with fascicle length expressed as both strain (A,C) and length
(B,D). The black arrow denotes the counter-clockwise path of the work loop,
indicating the positive net work (area contained within the work loop in B,D)
performed during the muscle's fascicles over the course of the wingbeat cycle.
Note that the more posterior regions of the muscle have both shorter fascicles
and reduced strains (A,C), leading to reduced mechanical work output. Cycle
duration was 0.11 s for both pigeons, giving power outputs ranging from 7.9 to
20.5 W. All loops are taken from the 5th wingbeat of one trial from each
bird.
|
|
View larger version (15K):
[in a new window]
|
Fig. 10. Histogram showing the mass-fractions (open bars) and work-fractions (shaded
bars, inter-individual mean ± S.E.M.) of muscle work
estimated for the four muscle regions (SB: Ant, Mid, Post and TB; see
Fig. 1) from which in
vivo fascicle strains were sampled. Mass-fraction data were obtained for
all six pigeons, whereas work-fractions were obtained for those animals and
regions in which reliable work loops (Fig.
9) were obtained over multiple wingbeat cycles. Mass-weighted work
fractions were calculated by multiplying the net work from each region by the
fractional mass (Table 1), then
dividing by the summed averages for all regions. The average summed work was
1.28 W and average duration was 0.12 s. Individual bird values were based on a
minimum sample of 8 wingbeats, with an average sample size of 40 wingbeats
(Table 4).
|
|
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
© The Company of Biologists Ltd 2005
