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Quantitative ultrastructure of histochemically identified avian skeletal muscle fiber types.

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THE ANATOMICAL RECORD 218~128-135(1987)
Quantitative Ultrastructure of Histochemically
Identified Avian Skeletal Muscle Fiber Types
Program i n Anatomy, Neurobiology, and Developmental Biology, Department of
Zoological and Biomedical Sciences, Ohio University, Athens, OH 45701
A cryostat retrieval method and combined adenosine triphosphatase (ATPase) and acetylcholinesterase (AChase) method were used to study the
ultrastructure and innervation of histochemically identified skeletal muscle fibers
in different pigeon muscles. The Z-line structure and volume percentage sarcotubular system were analyzed from different muscles selected for their composition by
fiber type. Histochemically, three main fiber types were investigated: slow tonic
fibers with a moderate ATPase activity after preincubation at acid or alkaline pH;
fast-twitch fibers that had high activity after alkaline treatment and low activity
after acid preincubation; and a type considered to be slow-twitch that had low
activity after alkaline, and high after acid preincubation. Both the slow tonic and
slow-twitch fibers had multiple, en grappe innervation, while the fast-twitch fibers
had robust, single end plates. The Z-line of the fast-twitch and slow-twitch fibers had
a regular square lattice pattern, in contrast to the granular, nonlattice structure of
the slow tonic Z-line. The volume percentage sarcotubular system of the slow-twitch
fibers was intermediate between and significantly different from that of the fasttwitch and slow tonic fibers. These correlative analyses suggest that the avian
muscles contain not only the fast-twitch and slow tonic fibers previously known, but
also a slow-twitch fiber that appears to be intermediate between the tonic and the
mammalian slow-twitch fiber type. Based on the abundance of the sarcotubular
system, this fiber type appears to be fast-contracting and -relaxing, in spite of being
multiply innervated.
The characterization of skeletal muscle fiber types is
important for clinical, functional, and developmental
studies because there may be fiber type specificity of the
muscles' reactions to various experimental, ontogenetic,
and pathologic changes. It is clear that a variety of
skeletal muscle fiber types exist, and that the predominant fiber types in mammals differ in some respects
from those of other vertebrates (reviews by Morgan and
Proske, 1984; Buchthal and Schmalbruch, 1980). Most
mammalian muscles consist of two major types, the fasttwitch and its subtypes, and the slow-twitch fibers (classification systems differ for both of these fiber types).
Both fiber types respond to a single stimulus with a n
action potential and twitch, but the slow fiber has longer
twitch times than the fast fibers. Both are usually innervated by a single neuron that terminates in a single
motor end plate. The internal membrane systems have
been described both qualitatively and quantitatively,
and the sarcotubular system is more abundant in fast
fibers (Eisenberg, 1983).
In contrast, some mammalian muscles and those of
most vertebrates have slow tonic fibers that respond
with local depolarizations rather than conducting action
potentials, and have polyneuronal innervation, with
small-diameter neurons terminating in grape-like
The most common method for differentiating muscle
fiber types in any tetrapod vertebrate muscle has been
0 1987 ALAN R. LISS, INC.
to use histochemical assays for myosin adenosine triphosphatase (ATPase) activity. The fast and slow fibers
have different myosins and their ATPase activities can
be differentiated qualitatively by means of differing pH
stabilities and labilities. Thus a fast fiber would have a
high ATPase activity that is maintained after alkaline
preincubation, but is much reduced after acid preincubation. In contrast, slow twitch fibers have a low activity
after alkaline preincubation, and high activity after acid
preincubation. The slow tonic fiber, at least in the birds,
shows a moderate activity after either alkaline or acid
Several investigators have noted that some avian slow
fibers have a histochemical ATPase activity that resembles mammalian slow-twitch fibers; these fibers have a
low ATPase activity that reverses after acid preincubation (Barnard et al., 1982; Toutant et al., 1981). The
morphological characteristics of these histochemically
identified fiber types have not been investigated because
of the difficulty in identifying them other than by histochemical or immunocytochemical methods. We have
modified a cryostat retrieval method, developed by Eisenberg and Kuda (19771, that allows us to examine the
ultrastructure of histochemically identified fibers (Staron et al., 1984).This technique is used here to analyze
Received September 16, 1986; accepted January 8, 1987.
Technical assistance was provided by Laurel Zirnrner.
quantitatively and qualitatively the fiber types in sev- each fiber was labeled for its ATPase activity after acid
eral muscles of the pigeon in order to examine this and alkaline preincubation. Fascicles that were matched
difference in fiber types. The sarcotubular systems of in the resin-embedded preparation were then trimmed
different fiber types were compared quantitatively. Mi- out of the block and mounted onto a blank gelatin captochondrial volume percentages were not included in sule filled with polymerized resin. The mounted prepathe analysis because both glycolytic and oxidative fibers ration was then trimmed further and a few thick (0.5make up the fast-fiber population, and variability would pm) sections were made. These sections were stained
with toluidine blue and after again being matched with
be too great for results to be meaningful.
the drawings of the histochemical preparations, the fiMATERIALS AND METHODS
bers were traced onto transparent plastic sheets a t 200 x
Muscles were taken from 20 pentobarbital-anesthe- magnification so that each fiber could be matched actized adult pigeons, Columba livia, Carneau breed, ob- cording to its histochemical characteristics.
Thin sections were then cut, mounted onto formvartained from the Palmetto Pigeon Plant, of Sumter, SC,
or the Bowman Gray School of Medicine, Winston-Salem, coated slot grids, and initially photographed in the elecNC. The muscles examined were the tonic anterior latis- tron microscope at 150x magnification in order to again
simus dorsi (ALD), the mixed posterior belly of the bi- match the fascicles with the tracings on the transparent
venter cervicis (BVC), the tonic posterior head of the plastic sheets. Individual identified fibers were photo,
prints enserratus superficialis metapatagialis (SSM), and the graphed at 3,000, 7,000 and 2 0 , 0 0 0 ~ and
mixed extensor digitorum longus (EDL). Segments of larged 3.5 times were used for analysis. Prints at
muscles were positioned for cross-sectioning on wooden intermediate magnifications were used for the sarcotutongue blades in a rnixture of tragacanth gum and Tis- bular system measurements, and the high-magnificasue Tek O.C.T. compound (Miles Laboratories, Naper- tion prints were used to analyze the Z-line structure.
ville, IL), then frozen for 20 sec in a slurry of methyl The sarcotubular system volume percentage was meabutane chilled with liquid nitrogen, and warmed to sured according to the methods described by Eisenberg
-20°C in a cryostat. The tongue blades were mounted et al. (1974). One to four (usually three) regions were
onto the microtome chuck, and the muscles were sec- measured to give the mean value for each fiber. The
tioned a t 12-pm thickness and mounted on 22-mm cover measurements were subjected to analysis by one-way
glasses for histochemistry. After each 16 sections, two ANOVA and the Student-Newman-Keuls test.
thicker sections, approximately 25-35 pm thick, were
brushed directly into ice-cold Karnovsky’s fixative in
The method of Ashmore et al. (1978)to simultaneously
cacodylate buffer. This process was repeated two to four
demonstrate ATPase and acetylcholinesterase (AChase)
times per muscle.
activities was used for muscles from five birds to deterElectron Microscopy
mine the innervation patterns of the fiber types in the
The thick sections were fixed for 2-4 h r by floating in muscles studied. For these preparations, the muscles
cold fixative (1% glutaraldehyde and 2% paraformalde- were prepared for longitudinal cryostat sections. Sechyde in 0.1 M cacodylate buffer, pH 7.21, then rinsed tions 40 pm thick were made and mounted on 3%EDTAovernight in cacodylate-buffered sucrose. Dehydration coated slides, allowed to dry overnight, and then prethrough a n alcohol series was followed by infiltration in pared for the ATPase and AChase activity as described
a propylene oxide-Epon and Araldite mixture. The sec- by Ashmore et al. (1978).
tions were flat-embedded in Epon and Araldite. The
Technical Considerations
blocks were sectioned with diamond knives with a
Reichert OMU2 ultramicrotome, mounted on formvar- The sample sizes are not large for this study. Approxicoated slot grids, stained with uranyl acetate and lead mately 20% of the preparations were discarded owing to
citrate, and examined with a Zeiss EM109 electron excessive ice crystal formation. Since we work with small
pieces that are 25-35 pm thick, many sections were lost
during processing, or became folded, or were cut
obliquely, making it impossible to identify individual
The 12-pm sections were processed for myofibrillar fibers. Finally, the freezing tended to reduce contrast
ATPase activity after preincubation at pH 4.2, 4.6, or greatly, and in spite of longer staining times, thicker
10.4 (Guth and Samaha, 1969; Brooke and Kaiser, 19701, sections, and lower accelerating voltage, contrast was
nicotinamide adenine dinucleotide-tetrazolium reduc- often sufficient to obtain data. For the EDL muscle, the
tase (Dubowitz and Brooke, 19731, and toluidine blue for percentage of slow fibers was often quite low, so the
sample size for these fibers is quite small. Because of all
routine histological observations.
these problems, only about 25% of the original preparaMatching the Histochemical Preparations With the
tions provided data for the final analysis.
Thin Sections
The flat-embedded sections for electron microscopy
were traced with a brightfield microscope equipped with
a drawing tube; outlines of fascicles and positions of
blood vessels and nerves were marked. This outline was
superimposed onto the histochemical preparation until
matching fascicles were identified. When regions were
matched, fibers in several fascicles of the histochemical
preparation were traced a t 200 x magnification, and
We have found in prior studies that the anterior latissimus dorsi is homogeneous in its slow tonic fiber population in about half the pigeons; in the remainder of the
birds a few fast fibers (usually less than 1%)may occur
in the muscle (Hikida, 1981).The tonic fibers of the ALD
had a moderate ATPase activity after preincubation at
pH 4.2, 4.6, or 10.4, and the NADH activity was also
uniformly moderate.
The BVC and EDL had a mosaic distribution of only
two fiber types at pH 4.2 preincubation (Fig. l),but a t
4.6 the fast fibers displayed either a low or moderate
ATPase activity (Fig. 2). The slow fibers with high
ATPase activity at pH 4.2 had a low activity a t pH
10.4 (Fig. 3), and therefore had properties similar to
the mammalian slow-twitch fibers.
The slow head of the SSM consisted of fibers similar
to the ALD, with moderate ATPase activity after all
preincubation conditions and moderate NADH activity.
Thus the slow fibers of the SSM were slow tonic. The
interface between the slow SSM and the adjacent fast
head consisted of a small zone with a mosaic pattern of
fiber types, but this portion was not used in the study.
By using the method to simultaneously demonstrate
the AChase and ATPase activities, the pattern of end
plates on histochemically identified muscle fibers could
be determined. As has been found previously, the tonic
fibers of the ALD and SSM had multiple innervation
(Hikida and Bock, 1974), and the pattern consisted of a
group of small round terminals (en grappe) situated a t
intervals along the fibers. The slow fibers of the BVC
and the EDL, identified by the ATPase activity, also had
multiple innervation, while the fast fibers of these muscles had only a single site of innervation (Fig. 4).
only a square lattice pattern (Fig. 6). The Z-lines of the
fast fibers of the EDL and BVC had the normal lattice
pattern (Fig. 7).
The morphometric analysis revealed that three classes
of fibers could be distinguished on the basis of the
amount of sarcotubular system (Table 1).The group
having the least sarcotubular system was made up of
the ALD and posterior SSM, the intermediate class consisted of the slow fibers from the BVC and EDL, and the
group with the most abundant sarcotubular system was
made up of the BVC and EDL fast fibers. There were
significant differences between these groups in terms of
the volume percentages of sarcotubular system.
The ultrastructure of frozen sections differed slightly
from fresh unfrozen sections. The contrast of the sections
was markedly reduced, and some components such as
the nuclei sometimes had ice crystals within them. The
sarcotubular system had no perceptible swelling (Figs.
5-8), and this was verified by comparisons of the volume
percentages of these avian fibers with those of various
mammals, a s described below.
The method of matching histochemically identified
fibers with adjacent frozen sections fixed and embedded
for electron microscopy is tedious and produces a rather
low yield because of various technical difficulties, as
discussed above. We wondered whether the procedure
artifactually altered the sarcotubular volume, so we
compared our results with those for mammalian fiber
Ultrastructure and Morphornetric Analysis
types, as compiled by Eisenberg (1983), and they
The Z-line structure has been used as a major morpho- matched very well (Table 2). The data for our fiber types
logical characteristic for distinguishing between twitch fitted very closely with the values for the guinea pig,
and tonic fiber types (Page, 1969; Hikida, 1972; Hikida rat, and mouse. If a n artifactual swelling had occurred,
and Bock, 1974). The Z-line of twitch fibers has a regular the values for avian fibers would have been much
zig-zag pattern in longitudinal section, and a very regu- greater. Values for the EDL and BVC slow fibers match
lar square lattice pattern in cross section. The Z-line of those €or slow-twitch oxidative fibers of mammals, and
the tonic fiber has a n amorphous, thick appearance in fast fibers in this study correspond to those of the guinea
longitudinal sections of the myofibrils, and a dense gran- pig and mouse.
ular ultrastructure containing no lattice pattern in crossThe fibers classified as slow-twitch have the following
sectional appearance (Hikida and Bock, 1974). The Z- characteristics: The ATPase activity is identical to mamlines of fast-twitch and slow-twitch fibers have no such malian slow-twitch fiber activity; the innervation patdistinction (Goldstewn et al., 1982), but the Z-line of the tern is arranged in many small clusters; the sarcotubular
slow-twitch fiber may be thicker than that of the fast- system volume is intermediate between that of fast and
twitch in longitudinal sections.
tonic fibers; the Z-line morphology is characteristic of
The only fibers that had no Z-line lattice pattern were fast fibers. Until physiological studies are done, we will
those of the ALD and SSM (Fig. 5). The slow fibers of assume these to be slow-twitch fibers because most of
the EDL and BVC contained fibers having Z-lines with the morphological and histochemical characteristics indicate fast fibers.
The existence of different avian slow skeletal muscle
Figs.1-3. Biventer cervicis, serial sections, prepared for ATPase ac- fiber types has been proposed previously on the basis of
tivity after preincubation at pH 4.2 (Fig. 11,4.6 (Fig. 2), and 10.4 (Fig. the histochemical ATPase activity or immunocytochem3). The same fast fibers are indicated by 0,and the slow fibers by X in istry (Barnard et al., 1982; Pierobon Bormioli et al.,
the adjacent sections. After incubation at pH 4.2 (Fig. 11, only two fiber
types are manifested, the slow-twitch (dark) and the fast-twitch (light 1980; Toutant et al., 1981; Shafiq et al., 19841, but charfibers). After pH 4.6, the fast fibers have either a low or a moderate acterization of these slow fiber types has not yet been
ATPase activity (Fig, 2). After incubation at pH 10.4 (Fig. 3), the completed. Barnard et al. (1982) recognized five major
activity is the reverse of that after pH 4.2 Figures 1-3 x 130.
types of fibers in muscles of chicks up to 3 months of
Fig. 4. Longitudinal section of a biventer cervicis muscle prepared age; the three twitch types (including a slow twitch) and
for ATPase after acid preincubation and AChase activity. The neuro- two tonic types are classified on the basis of their histomuscular junctions of the slow-twitch fibers (dark fibers), as indicated chemical ATPase activity. Although Barnard et al. (1982)
by this AChase activity, consist of a group of small punctate sites (en studied the contractile and biochemical AChase characgrappe endings, indicated by arrow) that occur at intervals aIong the
teristics of various muscles, they did not match the
fiber. In contrast, the neuromuscular junction of the fast (light) fiber is
large and single, with finger-like extensions; the end plate occupies a characteristics with specific fiber types, but only inlarge part of the fiber surface (indicated by arrowheads). x325.
ferred these correlations.
Fig. 5. Electron micrograph of the histochemically identified slow tonic fiber of the anterior latissimus
dorsi shows that the Z-line consists of a granular dense mass that has no regular structure. ~ 8 0 , 0 0 0 .
Fig. 6. Electron micrograph of a histochemically identified slow-twitch fiber of the biventer cervicis
having a regular square lattice pattern of the 2-line, and an abundant sarcotubular system. ~ 8 0 , 0 0 0 .
munofluorescence methods indicated that slow fibers, as
revealed by the ATPase reaction, showed two levels of
positive response, indicating that a n ALD-type and another slow-type muscle fiber existed in the leg muscles
(Shafiq et al., 1984). These studies agree with an earlier
study by Pierobon Bormioli et al. (19801, who used antibodies against the ALD and guinea pig soleus. In that
study, fibers of mixed muscles from various vertebrates,
including birds, designated as slow by myosin ATPase
activity reacted with anti-ALD antibodies or with antisoleus, but not with both. This suggests that both a slowtwitch (antisoleus) and slow tonic (anti-ALD) population
exists in many vertebrate muscles.
These different studies point to the existence of at
least two slow fiber types in the chicken, but defining
the characteristics of these other than by histochemistry
or immunocytochemistry has been difficult. Our study
shows that the slow fibers, a s identified by ATPase activity, can be characterized ultrastructurally. This correlative analysis reveals that a muscle such as the BVC has
a slow fiber type that differs from the ALD slow fiber.
The difference exists not only in Z-line morphology, but
the amount of sarcotubular system present. Toutant et
al. (1981)have shown that the chick's BVC has two slow
fiber types, both of which they classify as slow tonic.
Barnard et al. (1982) would call one type slow-twitch,
based on the histochemistry. Our study indicates that in
the pigeon, this is a slow-twitch fiber type, but it also
suggests that slow tonic fibers may not occur in the BVC
of the pigeon at all. The histochemistry of the ATPase
activity shows that slow fibers with a moderate activity
TABLE 1. Sarcotubular system volume percentages in
after both acid and alkaline preincubation are not preshistochemically identified fibers
ent in the pigeon's BVC. That the chicken and pigeon
Fiber type
Mean f SE (Fibers measured)
should differ in this manner is not too surprising, since
these two species differ in ALD fiber composition (HikSSM
Slow tonic
1.04 + 0.45 (38)
Slow tonic
1.67 I 0.35 (15)
ida and Wang, 1981)and response to tenotomy (Hikida,
Slow-twitch 3.21 k 0.83 (32)
o,05 1981).
Slow-twitch 3.51 f 0.98 (11)
The existence of several slow muscle fiber types, espeBVC
5.00 + 0.90 (38) 1
ones having multiple innervation, is significant
5.22 1.13 (9)' (
ns, P < 0.05
because it would influence specificity of innervation and
There were significant differences between each set of values except interpretation of past studies concerned with neuromusfor those bracketed.
cular interactions and regeneration of specific muscle
'Abbreviations: SSM, serratus superficialis metapatagialis; ALD,
anterior latissimus dorsi; BVC, biventer cervicis; EDL, extensor fiber types. It raises several questions, such as what
controls the manifestation of a slow-twitch versus a slow
digitorum longus.
Toutant et al. (1981) correlated the innervation pattern with the ATPase activity and distinguished two
tonic fiber types, one having a high activity a t preincubation pH 4.2, 4.35, and 10.4, while the other had a n
intermediate activit,y at pH 4.2 or 4.35, and low activity
at 10.4. Both of these tonic fiber types were multiply
innervated. The latter tonic type of Toutant et al. (1981)
would be considered twitch by some of the other
Suzuki et al. (1982, 1985) have subdivided fibers of
young chicks into sjx types, and these appear to encompass all fiber types characterized by other investigators.
Their type Isw is variously indicated a s tonic (Toutant
et al., 1981; Suzuki et al., 19821, or twitch (Barnard et
al., 1982; Phillips and Bennett, 1984). Barnard et al.
(1982) and Toutant et al. (1981) indicate that this type is
multiply innervated.
The results of the present study demonstrate that both
slow tonic and slow-twitch fibers occur in the pigeon
muscles. Slow fibers of the BVC and EDL have a n acidstable and alkaline-labile ATPase, multiple innervation,
a Z-line with a lattice substructure, and a sarcotubular
system volume that is intermediate between fast-twitch
and slow tonic fibers. The mammaIian slow-twitch fiber
has a Z-line with a square lattice structure, similar to
other fast-twitch fiber types (Goldstein et al., 1982).
The presence of different types of slow fibersin avian
muscles has also been demonstrated by reactions of
monoclonal antibodies to the chicken ALD myosin. Im-
TABLE 2. Sarcotubular svstem volume Dercentaees of various vertebrates
Fiber tvwe
Schmalbruch, 1979
Eisenberg and Kuda, 1976
Eisenberg et al., 1974
Luff and Atwood, 1971
Volume wercentaee
Eisenberg and Kuda, 1975
This study
'Abbreviations: FG, Fast glycolytic; SO, slow twitch oxidative; FOG, fast oxidative glycolytic; ST,slow
tonic; EDL, extensor digitorum longus; SSM, serratus superficialis metapatagialis, slow head; ALD,
anterior latissimus dorsi; BVC, biventer cervicis; Gastroc, gastrocnemius.
'Sarcoplasmic reticulum only.
tonic muscle fiber type. It is known that the slow-twitch
fiber is maintained and regulated by its neural impulse
activity (Pette, 1984; Pette and Vrbova, 1985). Experiments with avian muscles have suggested that the slow
tonic fiber type can also be developed under the influence of a tonic neural activity (Renaud et al., 1978;
1983). If both slow tonic and slow-twitch fibers are
formed because of a constant tonic activity pattern, then
what determines the type to be formed when genes are
present for both types, as in the pigeon, and probably
other species, including man?
The tonic fiber has a multiple innervation, and is also
polyneuronally innervated (KuMer and Vaughan Williams, 1953). It responds to indirect stimulation with a
local depolarization that increases with longer stimulation, and does not normally propagate a n action potential. The adult mammalian slow-twitch fiber is usually
innervated by a single neuron that terminates in a n end
plate, and indirect stimulation results in a n action potential and twitch. The innervation of the avian slowtwitch fiber is similar to the tonic fiber with its multiple
innervation, and multiple innervation suggests that the
avian slow-twitch fiber is also activated by local depolarization. This contradicts its morphology, which suggests
it is designed for a rapid activation and relaxation.
Therefore this study shows that by using a correlative
technique such as this cryostat retrieval method,
whereby histochemistry and electron microscopy can be
done on the same identified muscle fibers, it is possible
to gain much more information about the nature of the
muscle fibers and their relationships between various
species. This study also indicates that mammals may
not be as unique in their muscle fiber type composition
a s previous studies might have suggested, as both mammalian and avian muscles have fast-twitch, slow-twitch,
and tonic fiber types; however, this avian slow-twitch
fiber is intermediate between the slow tonic and the
mammalian slow-twitch fiber.
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This study was supported in part by grants from the
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ties of myofiber types in thigh muscles of the chicken. Acta Histomicrograph. ~ 8 0 , 0 0 0 .
chem. Cytochem., 15:362-371.
Suzuki, A., T. Tsuchiya, S. Ohwada, and H. Tamate (1985) Distribution
Fig. 8. An electron micrograph of a histochemically identified slowof myofiber types in thigh muscles of chickens. J. Morphol., 185:145twitch fiber from the bibenter cervicis shows little damage due to the
freezing and preparat0r.y procedures used for this cryostat retrieval Toutant, J.P., T. Rouaud, and G.H. LeDouarin (1981) Histochemical
properties of the biventer cervicis muscle of the chick: A relationmethod. The sarcotubular system (in this case the sarcoplasmic reticship between multiple innervation and slow-tonic fibre types. Hisulum) shows little evidence of dilation, and the filament arrangement
tochem. J.,13:481-493.
is normal. x68,400.
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identifier, ultrastructure, fiber, skeletal, muscle, avian, typed, quantitative, histochemical
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