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Musculotopic innervation of the primary flight muscles the pectoralis pars thoracicus and supracoracoideus of the pigeon Columba liviaA WGA-HRP study.

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THE ANATOMICAL RECORD 225:35-40 (1989)
Musculotopic Innervation of the Primary Flight
Muscles, the Pectoralis (Pars Thoracicus) and
Supracoracoideus, of the Pigeon (Columba M a ) :
A WGA-HRP Study
A. SOKOLOFF, T. DEACON, AND G.E. GOSLOW, JR.
Biological Anthropology, Harvard University, Cambridge, Massachusetts 02138
(A.S., T.D.);Department of Biological Sciences, Northern Arizona University,
Flagstaff,Arizona 8601 1 (G.E.G.)
ABSTRACT
The distribution of motoneurons innervating the primary depressor and elevator muscles of the wing of the domestic pigeon (Columba liuia) was
studied by using the retrograde axonal tracer lectin-conjugated horseradish peroxidase (WGA-HRP). Injection of WGA-HRP into the pectoralis (pars thoracicus)
labeled neurons in the ventromedial corner of the lateral motor column of the
spinal cord. These neurons were arranged in a column extending from spinal
segment X or XI to spinal segment XI1 or XIII. The pectoralis, the primary depressor muscle of the wing, consists of two parts which are anatomically and
functionally distinct, the sternobrachialis (SB) and thoracobrachialis (TB). Injection into the SB labeled neurons in the rostra1 and middle regions of the pectoralis
motoneuron column. In contrast, injection into the TB labeled neurons in the
middle and caudal regions of the pectoralis motoneuron column. Injection into the
primary elevator muscle of the wing, the supracoracoideus, labeled neurons in the
lateral motor column in spinal segments X and XI. These motoneurons were located dorsolateral to motoneurons labeled following pectoralis injection. These
data demonstrate musculotopic segregation of the motoneurons innervating the
primary flight muscles in the pigeon and, further, illustrate that the SB and TB
subregions of the pectoralis are innervated by discrete aggregations of motoneurons.
This report and the preceding one (Kaplan and Goslow, 1989) describe aspects of the neuromuscular organization of the major muscles used for wing elevation
and depression during flight in the pigeon (Columba
liuia). The major depressor muscle of the wing, the pectoralis (pars thoracicus), consists of two parts, the sternobrachialis (SB) and thoracobrachialis (TB). The two
parts are separated by an intramuscular aponeurosis,
possess independent origins and fascicle architecture,
and exhibit different proportions of fast oxidative and
fast oxidative glycolytic fibers (Kaplan and Goslow,
1989). The supracoracoideus (SC), the major elevator
muscle of the wing, lies deep to the pectoralis. Its fascicles arise from the dorsal half of the carina, the adjacent body of the sternum, and a small area on the
base of the coracoclavicular membrane. The tendon of
insertion passes dorsally through the triosseal canal
(formed by the clavicle, coracoid, and scapula) to insert
onto the dorsal surface of the posterior edge of the proximal humerus. This specialized “pulleylike” arrangement is an avian feature which appears fundamental
for wing elevation.
Flight in birds represents a highly derived and successful form of locomotion among tetrapods. Neither
the evolution of bird flight (Padian, 1986) nor its neural control is understood. Requisite to such understand0
1989 ALAN R. LISS, INC
ing is a description of the anatomical organization of
the neurons which innervate the muscles of flight. In
many vertebrate species, peripheral muscles are innervated by spatially discrete pools of motoneurons (e.g.,
Hollyday, 1980; McHanwell and Biscoe, 1981; Fetcho,
1987). Recent studies have shown that populations of
motor units in some muscles are organized into functional subunits. These functional subunits often receive innervation from a discrete aggregation of motor
pool neurons whose axons course through a single firstorder nerve branch (Iliya and Dum, 1984; English and
Weeks, 1987; Weeks and English, 1987). Such anatomical segregation suggests that the central nervous system may recognize distinct functional compartments
within individual peripheral muscles (English and
Weeks, 1987). The musculotopic segregation of motoneurons innervating flight muscles has been demonstrated in the chick and chicken (Martin and Hrycyshyn,
1981; Ohmori et al., 1982; Straznicky and Tay, 1983))
but the topographic organization of motoneurons in-
Received March 15, 1988; accepted September 27, 1988
Please address correspondence to A. Sokoloff, Biological Anthropology, Harvard University, 11 Divinity Ave., Cambridge,
MA 02138.
36
A. SOKOLOFF ET AL
and viewed under brightfield, darkfield, and polarized
light microscopy.
TABLE 1. Location of muscle injections
Case
1
2
3
43
54
64
74
SB/TB2
X
X
X
X
Muscles iniectedl
SB
TB
sc
X
X
X
X
X
X
X
84
9
10
‘TB-thoracobrachialis;
SB-sternobrachialis;
SC-supracoracoideus.
’Entire pectoralis injected.
31njections into the left SB/TB and the right SC.
41njections into the right SB and the left TB.
nervating the anatomically and functionally distinct
SB and TB parts of the pectoralis has not been studied.
The central organization of the motoneurons which innervate the SC and the SB and TB parts of the pectoralis has not been described in the pigeon. This study
illustrates the organization of the spinal cord motoneurons which innervate the SC and the SB and TB parts
of the pectoralis in the adult pigeon.
MATERIALS AND METHODS
Ten adult pigeons, C . Zivia (250-450 g), were anesthetized (25 mg/kg ketamine and 2 mg/kg xylazine,
I.M.), and in various combinations, the SB, TB, and SC
were surgically exposed and injected with a 5% solution of lectin-conjugated horseradish peroxidase (WGAHRP, Sigma) (Table 1).To sample a wide range of motor units while minimizing the possibility of tracer
leakage to adjacent muscles, WGA-HRP was delivered
via multiple, small intramuscular injections with a 10pl Hamilton syringe. A total of 2 p1 was delivered to
the SC (three or four injections of 0.5-0.7 p1 each)
and a total of 10-15 p1 was delivered to the SB and to
the TB (three or four injections of 3-4 pl each). During
surgery, care was taken to preserve the integrity of the
fascial membranes separating the SB and TB and the
SB and SC. It has been reported that intact fascial
membranes form a barrier to the leakage of tracer from
an injected muscle (Haase and Hrycyshyn, 1986).
After postinjection survival times of 44-50 hr the
animals were euthanatized and immediately perfused
through the left ventricle with 0.9% saline followed by
a fixative containing 0.5%paraformaldehyde, 1.5%glutaraldehyde, and 1.5% sucrose in 0.1 M phosphate buffer. The spinal cord was exposed, spinal nerves I-XX
were identified, and segments VIII-XVI were removed
and stored for 1-2 days in a 20%sucrose solution in 0.1
M phosphate buffer. Spinal cord tissue was embedded
in gelatin and cut in serial 75-pm sections in either
transverse or horizontal planes on a freezing microtome. Tissue sections were collected in a solution containing 30% sucrose and 30% ethylene glycol in 0.1 M
phosphate buffer and stored for up to 1 week at 0°C.
Spinal cord tissue was processed with a modified version of Mesulam’s (1978)tetramethylbenzidine method
(Deacon et al., 19831, counterstained in neutral red,
OBSERVATIONS
The brachial enlargement extended from the middle or caudal part of spinal segment X t o caudal XIII.
The ventral horn a t these levels is divisible into separate medial and lateral motor columns (Huber, 1936)
which together constitute lamina 9 of the pigeon spinal
cord (Leonard and Cohen, 1975). In the present study,
unilateral intramuscular injections into the SB, TB,
and SC only labeled cells in the lateral motor column
(LMC) of the ipsilateral ventral horn.
Injection into the ipsilateral SB and TB resulted in
ipsilateral labeling in the LMC from the caudal part of
spinal segment X to middle XI11 (Fig. 1A). In four
birds, the extent of the column of labeled neurons differed by as much as one segment in both rostral and
caudal directions. Labeled neurons were observed from
caudal X to middle XI11 (case l),from rostral XI to
middle XI1 (case 2), and from middle XI t o caudal XI1
(cases 3 and 4; Fig. 2A) In each case, the column of
neurons labeled with SB and TB injections was restricted in its rostral and caudal extremes to the ventromedial corner of the LMC whereas a t middle levels
(caudal XI and rostral XII) it expanded dorsolaterally
to fill much of the LMC (Figs. l A , 3). Neurons labeled
with SB and TB injections possessed round or polygonal cell bodies ranging from 22 to 50 pm in diameter.
Individual differences were also noted in the rostrocaudal extent of neuron labeling following injections
into the right SB and left TB. Neurons labeled after SB
injections extended from middle X to rostral XI1 or caudal XI1 (cases 5 and 6, respectively), from middle XI to
rostral XI11 (case 7), and from caudal XI to middle XI1
(case 8). Neurons labeled after TB injections extended
from caudal X to caudal XI1 (case 51, from rostral XI1 to
caudal XI1 (case 71, and from rostral XI1 t o caudal XI11
(cases 6 and 8). In general, neurons innervating the SB
extended from one-half to one-and-one-half spinal
segments rostral to neurons innervating the TB and
neurons innervating the TB extended from one-half to
one-and-one-half spinal segments caudal to neurons innervating the SB (Fig. 2B). Rostrocaudal overlap in the
position of neurons innervating the two parts was observed in the middle levels of the pectoralis column
(segment XI1 in cases 6-8 and segment XI in case 5).
Within this region of rostrocaudal overlap, neurons labeled with TB injections were located dorsally or dorsolaterally to neurons labeled with SB injections (Fig.
3).
Intramuscular injection of WGA-HRP into the SC
resulted in the labeling of neurons in a column extending from rostral X to caudal XI (case 9) and from middle X to caudal XI or rostral XI1 (cases 4 and 10, respectively; Fig. 2A). These neurons were situated in
the ventrolateral corner of the LMC in spinal segment
X, but in segments XI and XI1 they were located in a
tight cluster in the center of the LMC directly dorsolateral to the pectoralis column (Figs. lB, 3). Neurons
labeled with SC injections formed a morphologically
heterogeneous population with perikarya generally
ranging from 25 to 55 pm in diameter. A few larger
polygonal cells (55-70 pm) were also observed.
MUSCULOTOPIC ORGANIZATION; FLIGHT MUSCLES
37
Fig. 1. Motoneurons labeled following intramuscular injection of
WGA-HRP. A: Photomicrograph of a section from caudal segment XI
following injections into the sternobrachialis and thoracobrachialis
parts of the pectoralis muscle (case 3). The diagram on the right indi-
cates the location of the photo. B: Photomicrograph of a section from
middle segment X following injection into the supracoracoideus muscle (case 9). Calibration bar = 100 pm.
DISCUSSION
ally to cells innervating the pectoralis muscle and were
located laterally to pectoralis neurons in regions where
the SC and pectoralis columns overlapped. Because of
the experimental paradigm used in the present study it
was not possible to definitively determine the relative
rostrocaudal position of the motoneurons innervating
the pectoralis and SC muscles. However, our data suggest that motoneurons innervating the SC extend more
rostrally than motoneurons innervating the pectoralis
and that SC motoneurons are located dorsolateral to
pectoralis motoneurons in regions where the pectoralis
The localization of motoneurons innervating the pectoralis and SC described in the present study is in general agreement with previous studies of the innervation of the wing muscles of the chicken (Ohmori et al.,
1982) and chick (Martin and Hrycyshyn, 1981;
Straznicky and Tay, 1983). Ohmori et al. (1982) severed nerves to the pectoralis and SC muscles in the
adult chicken and reported cell degeneration in the
ventromedial corner of the ipsilateral LMC. They
noted that cells innervating the SC were offset crani-
A. SOKOLOFF ET AL.
38
A
Caudal
Fig. 2. Rostrocaudal distribution of supracoracoideus and pectoralis motoneurons. A Labeled motoneurons following injections into
the right supracoracoideus (SC) and left pectoralis (case 4). B: Labeled
motoneurons following injections into the right sternobrachialis (SB)
and left thoracobrachialis (TB) (case 5). Spinal segments X-XI1 are
B
Caudal
indicated. Note: the black dots indicate the rostrocaudal location
of labeled neurons only; the number of dots does not correspond to
the actual number of motoneurons innervating the SC, SB, or TB
muscles.
and SC columns overlap (Figs. 2A, 3). Ohmori et al. the chick by Martin and Hrycyshyn (1981) may reflect
(1982) also investigated the innervation of the rostral differences in the techniques employed, species differand caudal nerve branches to the pectoralis and re- ences in the innervation of the pectoralis and the SC, or
ported that the neurons composing the rostral branch differences in the ages of the animals studied. The abwere located rostral to neurons composing the caudal sence of contralateral degeneration in the experiments
branch. This offset pattern in chickens is reminiscent of Ohmori et al. (1982) suggests that the contralateral
of the rostrocaudal offset in labeled neurons following innervation of the chick pectoralis muscle observed by
right SB and left TB injections in pigeons and suggests Martin and Hrycyshyn (1981) may be a transient feaa similar topographic organization of the wing muscle ture in the development of wing muscle innervation.
neurons in the two species.
The absence of large labeled neurons following injecStraznicky and Tay (1983) injected HRP into the pec- tions into the pigeon TB and SB muscles in the present
toralis muscle in the chick and observed labeled neu- study is consistent with previous cytoarchitectonic
rons in the ventromedial corner of the LMC in the mid- studies of the pigeon spinal cord (Huber, 1936; Leonard
dle segments of the brachial enlargement. Martin and and Cohen, 1975).
The results from the present study demonstrate an
Hrycyshyn (1981) also noted labeled neurons in the
ventromedial corner of the LMC following HRP injec- anatomical segregation of the motoneurons innervattions into the pectoralis muscle of chicks, but further ing the SB and TB parts of the pectoralis. The SB,
reported 1) labeled neurons in dorsolateral regions of which differs from the TB in fiber composition, fascicle
the LMC, 2) a few labeled neurons in the contralateral architecture, force distribution, and patterns of electriLMC, 3) the presence of very large labeled neurons cal activity during flight (Dial et al., 1987, 1988; Ka(70-pm diameter) in the pectoralis motor pool, and 4) plan and Goslow, 19891, is innervated by the rostral
overlap in the transverse position of neurons labeled branch of the ventral cord of the brachial plexus by
with SC and pectoralis injections. We were unable to neurons located in the rostral and middle portions of
confirm any of these observations for the pigeon. Dif- the pectoralis motor column. The TB, in contrast, is
ferences in the present results from those reported for innervated by the caudal branch of the ventral cord of
MUSCULOTOPIC ORGANIZATION; FLIGHT MUSCLES
39
Fig. 3. Rostrocaudal extent and relative location of motoneurons
innervating the supracoracoideus (SC), sternobrachialis (SB), and
thoracobrachialis (TB) muscles. Diagram produced by superimposing
data from all cases. Symbol: 0 , SC; W, SB; A, TB. Note: the symbols
indicate the spatial distribution of neurons only; the number of symbols does not correspond to the actual number of motoneurons innervating the SC, SB, or TB muscles.
the brachial plexus by neurons located in the middle
and caudal regions of the pectoralis motor column. The
segregation of motoneurons innervating the SB and
TB, in association with histological and electromyographic differences between the two parts, suggests an
organization of the pigeon pectoralis which is similar to
the compartmental organization described for the lateral gastrocnemius and tibialis anterior muscles of the
cat (Iliya and Dum, 1984; English and Weeks, 1987).
By virtue of this anatomical segregation, the TB and
SB motoneuron populations may be capable of independent activation.
Comparative kinematic and electromyographic studies of selected tetrapods have led to speculation that
the transition from a primitive musculoskeletal design
to a more specialized state may have occurred with
little change in the basic motor pattern that controls
the shoulder during locomotion (Goslow et al., 1989).
Any test of such a hypothesis requires the identification of the homologous musculoskeletal elements from
one group to the next. At present we have only a superficial understanding of the homologies of shoulder
muscles (see for review Jenkins and Goslow, 1983).The
rostrocaudal segregation of motoneurons innervating
the different heads of the pectoralis in the dog (Krogh
and Towns, 1986) and rat (Baulac and Meininger,
1981) is reminiscent of the separate innervation of the
SB and TB in the pigeon, but comparable data on the
innervation of the reptile pectoralis are lacking. And,
although the pigeon and chicken show similar organization in the rostra1 and lateral location of the SC motoneuron pool relative t o the pectoralis motoneuron
pool, we are unaware of information on the innervation
of the presumed homologue of the SC in either reptiles
or mammals. The apparent conservatism of spinal motoneuron organization (McHanwell and Biscoe, 1981;
Fetcho, 1987) may help to determine the homologies of
the shoulder muscles in this system in which musculoskeletal patterns are highly derived to serve different
locomotor specializations.
ACKNOWLEDGMENTS
We thank Mary Kramer for comments on the manuscript. One of us (G.E.G.) was funded by NSF grant
DCB87-18727.
40
A. SOKOLOFF ET AL.
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