Download Insect Muscles Innervated by Single Motoneurons: Structural and

AMER. ZOOL., 27:1001-1010 (1987)
Insect Muscles Innervated by Single Motoneurons:
Structural and Biochemical Features1
DARRELL R. STOKES
Department of Biology, Emory University, Atlanta Georgia 30322
SYNOPSIS. Three locomotory muscles of adult male cockroaches have been biochemically
and structurally compared. All fibers of two muscles are innervated by the same motoneuron; both muscles are monofunctional—used only in running. Fibers of the third
muscle are also innervated by a single, but different motoneuron. This muscle is bifunctional—used in both walking and flying. Histochemical observations of enzymes associated
with energy production indicate that the three muscles are each comprised of a homogeneous population of fibers. However, qualitative differences do correlate with muscle
use. The bifunctional muscle shows high oxidative and glycolytic enzyme localization; the
monofunctional muscles show a low profile for these enzymes. Quantitative determinations
of specific activity for similar enzymes corroborate the histochemical observations. Light
and electron microscope observations also indicate that fibers from each of the two muscle
groups are structurally homogeneous and distinct. The two monofunctional muscles parallel one another for all structures examined and are different from the bifunctional
muscle. The bifunctional muscle fibers have cross-sectional areas twice that of the monofunctional muscles, have a greater myofibrillar diffusion distance, and have about half as
many actin per myosin filaments. Stereometric analyses show volume densities for mitochondria and tracheoles to be five times greater; membrane systems associated with excitation-contraction coupling, however, are half as extensive; and myofibrillar volume about
1.3 times less. These data form the basis for studies of denervation and cross-reinnervation,
and the role of individual motoneurons in specifying muscle fiber properties.
INTRODUCTION
Nearly two decades ago in a symposium
devoted to the diversity of striated muscle
in both invertebrate and vertebrate organisms, the organizer noted that the chemical
considerations of muscle constitute a specialized and complex field, "one which,
unfortunately is still somewhat remote from
contact with other aspects," (Hoyle, 1967,
p. 435). Since that time great strides have
been made, particularly in the utilization
of histochemical techniques to assess the
functional properties of muscle fibers and
motor unit organization of vertebrate muscles (Burke, 1981). Indeed it is only because
of these techniques that subtle differences
in muscle fibers have been demonstrated.
Despite numerous developmental and
design advantages of invertebrate neuromuscular systems {i.e., the conservative
innervation of individual muscles and the
homogeneity of whole populations of mus' From the Symposium on Muscle Fiber Typing as a
Bwassay of Xene-Muscle Interaction: Comparison of
Arthropod and Vertebrate Systems presented at the Annual
Meeting of the American Society of Zoologists, 2730 December 1985, at Baltimore, Maryland.
cle fibers), there is a paucity of literature
relating histochemical fiber types to either
structure or function. The most notable
exceptions are studies on crustacean
dimorphic claw muscles (Ogonowski et al.,
1980; Ogonowski and Lang, 1980; Govind
et al, 1981; see also papers by Atwood and
Lnenicka, 1987; Govind <?/ al, 1987; Rathmayer and Maier, 1987) which include the
development of muscle fiber types as well
as structure and function; and studies of
the locomotory muscles of the cockroach
(Hart and Fourtner, 1979; Stokes et al,
1979; Morgan et al, 1980). It is clear, particularly from those studies on insect muscles, that there are more questions than
answers; that we need to know more about
the relationship between muscle fiber histochemistry, structure, and function.
In the preceding paper it is shown that
several ultrastructural features of insect
muscles are correlated with muscle performance (Josephson and Young, 1987). In
this paper the ultrastructural and histochemical-biochemical features of insect
muscle fibers innervated by single motoneurons are examined for their predictive
value as determinants of muscle perfor-
1001
1002
DARRELL R. STOKES
178
179
FIG. 1. Transverse sections of a metathoracic coxa of P. americana stained to show histochemical comparisons
of A. NADH-TR, and B. GPD in muscle 177c and in muscles 178 and 179. Scale bar = 1 mm.
muscles in 19-21 day adult male cockroaches with this goal in mind.
There are differences in gross appearSINGLE U N I T MUSCLES
ance and in behavioral use of these two sets
Only three muscles of the cockroach of muscles. In terminal nymphs, muscle
{Periplaneta americana) metacoxa are known 177c is white in color and functions as the
to be innervated by single motoneurons— main trochanteral extensor of the leg durmuscles 177c, 178, and 179 (notation of ing walking and running. At the terminal
Carbonell, 1947). The innervation of mus- molt, when adult structures (i.e., wings)
cles 178 and 179 was established by Becht appear, the muscle becomes pink and in
(1959) and Pearson and lies (1971); that addition to its maintained role in walking
for 177c by Becht (1959) and more recently and running, becomes a wing depressor
by Malamud and Stokes (unpublished). In (basalar) during flight. Thus in the adult
comparison to other coxal muscles which roach, the muscle has a bifunctional role.
have been studied, the motoneurons sup- The single axon which innervates all fibers
plying 178, 179, and 177c produce fast of this muscle projects from a soma located
twitches of large amplitude which antifa- in the metathoracic ganglion; the axon
cilitate. T h e ultrastructural and histo- exits via nerve 4. Thus the entire muscle
chemical features of 178 and 179 have been and its motoneuron comprise a single motor
described previously (Fourtner, 1978; Hart unit.
and Fourtner, 1979), and there is a comMuscles 178 and 179, the posterior and
parative literature on the physiological, anterior trochanteral extensors, respecstructural, and histochemical features of tively, are white in all developmental stages.
both sets of mesothoracic homologues, Both are monofunctional—activated in
muscles 135c, 136, and 137 (Usherwood, both nymphs and adults during fast walk1962; Smit et al., 1967; Jahromi and ing only (Pearson, 1972). Both muscles are
Atwood, 1969; Morgan and Stokes, 1979; innervated by the same motoneuron,
Stokes et al., 1979; Morgan et al., 1980). located in the metathoracic ganglion with
None of these studies, however, has been an axon which exits via nerve 5.
done with a view towards comparing structural and biochemical components of musHlSTOCHEMlSTRY
cles uniquely innervated by single motoHistochemical techniques clearly show
neurons, and, ultimately the role of single that fibers of the two motor units are very
motoneurons in shaping muscle fiber prop- different. Fibers of muscle 177c were preerties. I have examined all three of these
dicted to be histochemically distinct from
mance. These data will serve as the basis
for studies on nerve-muscle interactions.
1003
MUSCLES INNERVATED BY SINGLE MOTONEURONS
the monofunctional pair and homogeneous. The shared innervation by a single
motoneuron, similar white color, and similar behavioral role led me to predict that
muscle fibers of 178 and 179 should be
histochemically indistinguishable. Cross
sections of frozen metacoxa were incubated in reaction media designed to localize 1) nicotine adenine dinucleotide tetrazolium reductase (NADH-TR, method
of Novikoff et al., 1961), an enzyme associated with mitochondrial oxidation, and
2) alpha glycerophosphate dehydrogenase
(GPD, method of Wattenberg and Leong,
1960), an enzyme indicative of glycolytic
pathways. Typical results are shown in Figure 1. All fibers of muscle 177c stained
very darkly for both enzymes indicating a
strong oxidative (A) and glycolytic (B)
capacity. Fibers of 178 and 179, however,
while homogeneous in profile as predicted,
are not oxidative and appear only weakly
glycolytic. Histochemical tests for myosin
ATPase (Morgan et al, 1980) show both
sets of muscles to stain intensely, supporting their physiological role in fast contraction. Thus fibers of 177c appear to have a
fast oxidative glycolytic profile (FOG); 178
and 179 have a fast glycolytic profile (FG).
Note in Figure 1 that other muscles show
more than one histochemical profile, an
observation which correlates with innervation by multiple excitatory motoneurons
or combinations of excitatory and inhibitory motoneurons (Stokes et al, 1979).
ENZYME SPECIFIC ACTIVITY
Histochemical techniques provide a
qualitative assessment of enzyme localization within myofibers, but do not indicate
the quantitative levels of enzyme specific
activity. For this one must turn to in vitro
studies. It is assumed that in vitro capabilities, and thus measurements, will parallel
the in vivo capacities for anaerobic and
aerobic metabolism. I have examined the
specific activity of two enzymes, alpha glycerophosphate dehydrogenase (GPD) and
citrate synthase (CS). GPD is a cytoplasmic
enzyme whose activity is indicative of glycolytic capacity. CS is a mitochondrial
enzyme whose activity reflects oxidative
TABLE 1. Specific activity of muscle metabolic enzymes'
Muscle
Enzyme
177c
178
179
47.1 ± 6.4
(9)
16.7 ± 1.2
(6)
49 .3± 7.2
(11)
18 .8 + 1.6
GPD
(6)
• Expressed as nM min"1 mg protein"1; x ± SE. For
178 and 179, means are based on pooled left and right
muscles. For 177c, means were determined for left
and right muscles independently. These means were
then used to calculate the values shown here.
" Values in parentheses represent number of animals.
CS
1,018.5 ± 98.2
(10)"
782.3 ± 21.7
(6)
capacity. Muscles 178, 179, and 177c were
removed from the metathorax and separately homogenized in 100 mm Tris buffer
(pH 7.4) at 4°C and sonicated. For one
group of samples the homogenates were
centrifuged to obtain a supernatant which
was then assayed for GPD. Homogenates
of a second group of samples were assayed
directly for CS. Both enzymes were assayed
spectrophotometrically; GPD after a procedure used by Chefurka (1958); CS by a
method reported by Alp et al. (1976). Specific activity is expressed as nM min"1 mg
protein"1, protein being determined by the
method of Bradford (1976). Results are
shown in Table 1. The specific activities
for 178 and 179 parallel one another for
both enzymes studied. The specific activities for CS and GPD, however, are more
than 20 and 40 times higher, respectively,
in 177c than in 178 or 179. These results
corroborate the histochemical data presented in Figure 1.
STEREOMETRIC ANALYSES
Stereometric analyses were performed
upon electron micrographs to determine
the per cent composition of ultrastructural
constituents within fibers from the two
muscle groups. A grid drawn on a transparency was placed upon the micrographs
and the structural component beneath each
grid intersection was recorded (Freere and
Weibel, 1967; Stokes et al, 1975). A minimum of 200 intersection points was analyzed for each micrograph. The volume
fraction of a particular structure was cal-
1004
DARRELL R. STOKES
culated by determining the fractional per
cent of intersection points overlying the
structure in the entire field. The fibers were
assumed to be longitudinally homogeneous. Five categories of structures were
tabulated—myofibrils, mitochondria, sarcoplasmic reticulum-transverse tubules (SRTTS), tracheoles, and "other." The results
are shown in Table 2 and representative
micrographs of transverse profiles of the
three muscles are illustrated in Figure 2.
Myofibrils
The myofibrils of all three muscles are
long, strap-like structures (Fig. 2). Fibers
of the bifunctional muscle, 177c, have
invested about 50% of their volume in contractile material represented by the myofibrils. The two monofunctional muscles, 178
and 179, are roughly similar in myofibrillar
volume and about 1.3 times greater than
177c. This does not necessarily mean that
fibers of 178 and 179 are capable of generating a greater overall force for these
measurements do not take into account
other possible means for increasing contracticle material in parallel {i.e., fiber
diameters and number of myofibers). As
shown in Figure 2, muscle 177c does have
more mitochondria which would have the
most obvious affect of reducing the amount
of contractile material per unit volume and
enhancing the oxidative potential of a fiber.
Thus fibers which stain strongly for mitochondrial enzymes are likely to have
reduced myofibrillar volumes. An exception to this might be muscles (e.g., cicada
tymbal muscle) which have particularly
high volume densities for SR-TTS (Josephson and Young, 1985).
Mitochondria, tracheoles, and glycogen
Mitochondrial density is one of the best
correlates of muscle fiber type as well as
function. Highly oxidative fibers would be
expected to have a large volume density
for mitochondria. Thus it is not surprising
that the pink fibers of 177c, all of which
stained positively for NADH-TR, are also
rich in mitochondria. Nearly 32% of the
myofiber area is represented by mitochondria. This is a fivefold increase over the
mitochondrial densities of 178 and 179.
Mitochondria of 177c are also much larger
(often >2 Mm) than those found in 178 and
179 and are considerably more electron
dense (see Fig. 2). The investment in myofibers of tracheoles was found to be five times
greater in 177c than in 178 or 179. In
many instances tracheoles were observed
deep within the muscle fiber, an arrangement which would help to maximize movement of respiratory gases to and from the
many nearby mitochondria. Fibers of 177c
also possess numerous dense bodies similar
to glycogen profiles reported for muscle
135c (Smit et al., 1967). These profiles
appear in large numbers around many
mitochondria (Fig. 2A) where they represent about 2.5% of the myofiber volume.
Their proximity to the mitochondria suggests an availability for mitochondrial oxidation. Presumed glycogen volume densities are tabulated as "other" in Table 2.
Sarcoplasmic reticulum-transverse
tubules
The SR appears in transverse sections of
all these muscles as an interconnected series
of membranous structures which define the
borders of each myofibril. In some profiles
the SR forms three or four stacked rows
of vesicles, which in muscle 177c often surround the mitochondria (Fig. 2A). The
TTS appears within the meshwork of SR
vesicles and is distinguished by flattened
cisternae and electron dense membranes.
Muscles 178 and 179 appear to have a
larger number of TTS per unit length of
SR than does 177c; however, this was not
quantified. In some cases it has been possible to show a relationship between volume densities of SR-TTS and the time
course of a muscle twitch. Fast twitch muscles in many insects appear to have a greater
investment of myofiber volume in SR-TTS
than do slow twitch muscles (Josephson,
1975; Josephson and Young, 1987). In the
cockroach however, the relationship
between SR-TTS volume densities and
muscle fiber type is less clear. Earlier histochemical studies (Morgan et al., 1980)
indicate that 177c, 178, and 179 all stain
intensely for myosin ATPase, an indicator
1005
MUSCLES INNERVATED BY SINGLE MOTONEURONS
c
B
M
i
V
JVTVm
-^
FIG. 2. Electron micrographs of muscles A, 177c; B, 178; C, 179, in cross section. The granular material
surrounding some mitochondria in A is presumed to be glycogen. M, mitrochondria; SR, sarcoplasmic reticulum; arrows, transverse tubules; scale bar = 0.5 /im. Insets in A and B are enlargements of the myofilaments;
scale bar = 0.14 /*m.
1006
DARRELL R. STOKES
TABLE 2. Muscle fiber ultrastructural volume densities (%x ± SE).
Muscle
Structure
Myofibrils
Mitochondria
SR-TTS
Tracheoles
Other
1
177c
50.3
31.9
14.5
0.5
2.6
±
±
±
±
±
179
178
1.0
0.9
0.7
0.1
0.9
67.1
5.5
27.1
0.1
0.2
±
±
±
±
±
0.7
0.5
0.8
0.1
0.2
64.7 ± 1.3
6.0 ± 0.4
29.0 ± 1.3
0
0.1 ± 0.1
n = 8, 7, 5 for muscles 177c, 178, 179, respectively; 5 fibers per animal.
of fast contraction. Usherwood (1962) has
shown that the twitch time courses for the
mesothoracic homologues are not significantly different. Yet our volume determinations indicate that 178 and 179 have
twice the volume of SR-TTS as 177c. This
may mean that oxidative fibers have a
smaller overall volume density of SR-TTS
than do nonoxidative fibers, regardless of
whether they stain positively for myosin
ATPase or have comparable twitch times.
It may be that highly oxidative fibers utilize
other membrane systems to help sequester
calcium following a twitch—perhaps mitochondria, which are obviously prevalent in
177c.
OTHER STRUCTURAL FEATURES
Several structural features which have
been studied in other arthropods with
respect to muscle contraction performance
were chosen for investigation of the two
histochemically distinct motor units of the
cockroach metacoxa. These are muscle
fiber cross-sectional areas, sarcomere
lengths, maximum diffusion distances for
calcium, and the ratio of thin to thick filaments. Results for the three muscles are
shown in Table 3.
Fiber areas
Fiber cross-sectional areas were determined by cutting out tracings of enlarged
photographed fibers and comparing the
weights of these profiles with the weight
of a similar piece of paper of known area.
As can be seen in Table 3, the mean area
of fibers from 178 and from 179 are indistinguishable, but are almost half as large
as fibers from 177c. Fast twitch muscles
tend to be comprised of larger fibers than
slow twitch muscles (Jahromi and Atwood,
1969, 1971); however, this is not a hard
rule. The dorsal band of the dorsal longitudinal muscle of the katydid, N. robustus,
the slowest contracting part of the muscle,
is comprised of fibers similar in area to the
fast contracting ventral band fibers (Stokes
et al., 1975). Trade-offs related to the
endurance and strength requirements of
the muscle for specific behaviors are likely
to impact on muscle fiber areas. This is
probably the case for the two sets of muscles studied here. While both are fast contracting, the 177c muscle fibers are twice
as large. Fibers of 177c are highly oxidative, and contain five times more mitochondria than the smaller glycolytic fibers
of 178 and 179. The larger area of 177c
fibers very well could be a trade-off
response to increased aerobic needs for
support of flight, while maintaining sufficient contractile components for walking
and running. Fiber typing certainly indicates aerobic capacity, but to be useful in
predicting fiber areas, some knowledge of
contraction kinetics would normally be
necessitated.
Sarcomere lengths
Sarcomere lengths were determined for
the three metacoxal muscles by measuring
the length of 10 consecutive sarcomeres in
suitably enlarged photomicrographs. Mean
values for individual sarcomeres from these
muscles are not significantly different; 3.3,
3.4, and 3.5 ^m for 177c, 178, and 179,
respectively (Table 3). These values are in
reasonable agreement with sarcomere
lengths of 3.7 nm reported by Fourtner
(1978) for muscles 178 and 179, using
somewhat different methods. Sarcomere
lengths ranging from 2 jam to more than
10 jim have been reported for arthropod
muscles (see Hoyle, 1967; Atwood, 1973).
1007
MUSCLES INNERVATED BY SINGLE MOTONEURONS
TABLE 3. Muscle fiber structural features.
Muscle
Feature
177c
6
178
1,203 ± 93.6"
638 ± 30.2
(6)
(7)
3.3 ± 0.2
3.4 ± 0.1
(6)
(6)
0.163 ± 0.004
0.148 ± 0.007
(8)
(7)
2:1
>2:1
* Values are means ±SE; number in parentheses = number of animals.
bd
- 5 fibers/animal.
c
10 sarcomeres/animal.
Fiber area
(Mm')
Sarcomere length 0
(Mm)
Diffusion distance"1
(Mm)
T h i n : thick filaments
Thus, the sarcomere lengths observed for
the three metacoxal muscles studied are
relatively short. Sarcomere lengths have
also been shown to correlate reasonably
well with contraction speed (Atwood, 1973;
Josephson, 1975; Stokes et al., 1975). In
general, speed of contraction is inversely
related to resting sarcomere length (but
see Hoyle and McNeill, 1968). Thus, the
metacoxal muscle, having short sarcomeres, should be fast contracting—a property already predicted from histochemical
tests for myosin ATPase (Morgan et al.,
1980). Physiological studies on the mesothoracic homologues (Usherwood, 1926;
Morgan, 1982) and on the metathoracic
177c muscle (Malamud and Stokes, unpublished) indicate that, indeed, they are fast
contracting with twitch rise times on the
order of 10 msec.
Diffusion distances
The activation of skeletal muscle is
dependent upon the inward spread of excitation via the TTS to the SR. Calcium is
released from the SR vesicles and must diffuse into the myofibrils in order to activate
sliding of the myofilaments (Ebashi and
Endo, 1968). Thus, the speed at which the
myofilamens are activated should be related
to the maximum distance of myofilaments
from the SR. Shorter diffusion distances
would mean a faster activation time course
and thus a faster overall twitch. Parallel
studies of contraction dynamics and ultrastructural measurements of diffusion distances on several insect muscles support
this observation (e.g., Stokes et al., 1975;
Josephson and Young, 1987).
179
617 ± 59.6
(8)
3.5 ± 0.1
(6)
0.145 ± 0.006
(5)
>2:1
I measured myofibril widths from electron micrographs and calculated the diffusion distance from the SR as one-half the
total myofibril width (Table 3). The mean
diffusion distances are not significantly different for 178 and 179. Mean diffusions
distances for 177c, while greater by about
10%, are probably not sufficiently great to
contribute to measureable differences in
twitch time course. Thus, one would predict from histochemical fiber typing that
both groups of muscle are fast; and, from
measurements of myofibril diffusion distances, and sarcomere lengths, one would
predict that the two sets of muscles are
comparable with respect to twitch time
course.
Ratio of thin to thick filaments
Many insect muscle fibers have a ratio of
thin to thick myofilaments which is greater
than the 2:1 ratio characteristic of vertebrate striated muscle. In general, these
fibers have long sarcomeres and are slow
contracting (Josephson, 1975). Other
insect muscle fibers, particularly flight
muscles, that operate at faster work
rhythms, have the usual 2:1 ratio (Auber,
1967).
As shown in the insets of Figure 2 A and
B, there is a difference in the ratio of thin
to thick filaments in the two groups of
cockroach muscles, despite the observation
that both are typified by short sarcomere
fibers and histochemically show a fast
myosin ATPase profile. Muscle 177c, the
bifunctional flight muscle has the usual 2:
1 ratio, with myosin filaments in a hexagonal array and each myosin surrounded by
1008
DARRELL R. STOKES
six actin filaments. However, both monofunctional muscles 178 and 179 have a ratio
of thin to thick filaments greater than 2:1.
The myosin filaments are still arranged
hexagonally, but some 10-12 actin filaments appear in an orbit around each of
the myosin filaments. There does not appear to be a clear-cut relationship between
this ultrastructural feature of these two
muscle sets, their histochemical profiles,
and their contraction dynamics. It may be
that the added thin filaments in 178 and
179 simply enhance the probability for
cross bridge formation during the rather
brief moments that these muscles are activated during fast funning. In the absence
of any capability for sustained activity (few
mitochondria and low oxidative potential),
additional mechanisms to enhance cross
bridge formation would facilitate force
generation which is necessary for brief,
powerful locomotory spurts.
DISCUSSION
It is shown in this study that the histochemical-biochemical profile of muscles
innervated by single motoneurons is
strongly correlated with structural properties of the muscle fibers. Further it is
clear that muscle fiber typing can be used
to assess many performance features of
muscles associated with different behaviors.
The single unit bifunctional flight muscle (177c) is comprised exclusively of FOG
fibers with a high specific activity for both
oxidative and glycolytic enzymes associated with energy production. The expectation based on this profile is that the muscle
fibers should be structurally homogeneous
and comprised of short sarcomere fibers
well invested with mitochondria and ready
access to both high energy fuel and an oxygen supply. One would also predict that
the SR-TTS would be well developed and
that the myofibrils would be designed to
accommodate rapid movement of calcium
from the SR to the myofilaments. Functionally, these features describe a muscle
which would be fast-contracting and
fatigue-resistant, something one might
expect of a muscle used for flight. That
they are relatively fatigue-resistant is evidenced by the observation that adult males
(19-21 days) can sustain tethered flight for
15 min or more (Malamud and Stokes,
1984). Furthermore, stimulation of the single axon supplying this muscle at flight frequency (30 Hz) shows that twitch amplitude is maintained above 50% of the initial
twitch amplitude for about 9 min (Malamud and Stokes, unpublished).
The single-unit monofunctional muscles
(178, 179), however, which are comprised
of FG fibers with a relatively low specific activity for oxidative and glycolytic
enzymes, should also be homogeneous, but
structurally very different than 177c for
components associated with energy production only. One would anticipate a much
smaller volume density for mitochondria, tracheoles, and glycogen. Sarcomere
lengths, on the other hand, would be short
and myofibril organization should accommodate rapid movement of calcium, features which are indicative of fast muscle
fibers. This profile describes a muscle which
should be fast, but also readily fatiguable.
Again, this is what one would expect of a
muscle used only for very brief, high speed
walking or running.
Comparisons brought out in this study,
for the most part, support histochemical
predictions, for these two very different
motor units. Only the volume densities for
SR in the two sets of muscles are disparate.
It should be pointed out that a volume density of 15% for 177c is still quite high. The
very fast twitches (mean rise time of 7.3
msec), observed for katydid dorsal longitudinal muscle which operates at 200 Hz,
have SR volume densities ranging from 16
to 30% (Stokes et al., 1975).
Fiber typing does not appear to be a useful predictor of muscle fibril volume density, muscle fiber area, or the ratio of thin
to thick filaments. These structures are
most likely adaptations for enhanced force
production in myofibers. Muscle strength
is not always intuitively related to contraction speed or staying power, features which
can be reasonably assessed from fiber typing. The large cross-sectional areas of fibers
from 177c do suggest, however, a means
MUSCLES INNERVATED BY SINGLE MOTONEURONS
of compensation for a large investment of
mitochondria, while at the same time maintaining strength.
The heterogeneity of fibers and the
broad array of histochemical, structural,
and physiological differences between the
two muscle groups, suggests an interaction
between the single motoneurons and the
muscle fibers that goes beyond activation.
The accessibility of the motoneurons to
manipulation and the divergent properties
of the muscle targets make these two motor
units an attractive model system for studies
of denervation and cross-reinnervation,
and the role of identified motoneurons as
determinants of muscle design.
1009
Ebashi, S. and M. Endo. 1968. Calcium ion and muscle contraction. Progr. Biophys. Molec. Biol. 18:
123-183.
Fourtner, C. R. 1978. The ultrastructure of the
metathoracic femoral extensors of the cockroach, Periplaneta americana.]. Morph. 156:127—
140.
Freere, R. H. and E. R. Weibel. 1967. Stereologic
techniques in mircoscopy. J. Roy. Microsc. Soc.
87:25-34.
Govind, C. K., DeF. Mellon, Jr., and M. M. Quigley.
1987. Muscle and muscle fiber type transformation in clawed crustaceans. Amer. Zool. 27:
1079-1098.
Govind, C. K., P. J. Stephens, and V. Trinkaus-Randall. 1981. Differences in motor output and fiber
composition of the opener muscle in lobster
dimorphic claws. J. Exp. Zool. 218:363-370.
Hart, T. F. and C. R. Fourtner. 1979. Histochemical
analysis of physiological and morphologically
identified muscles in an insect leg. Comp. BioACKNOWLEDGMENTS
chem. Physiol. A. 64:437-440.
This work was supported by a grant from Hoyle, G. 1967. Diversity of striated muscle. Amer.
Zool. 7:435-449.
the Emory University Research Commit- Hoyle,
G. and P. A. McNeill. 1968. Correlated phystee. Special thanks are due Ms. Georgette
iological and ultrastructural studies on specialJohnson for assistance with the stereometized muscles. Ib. Ultrastructure of white and pink
fibers of the levator of the eyestalk of Podophric analyses and Mr. Ted Schiff for assisthalmus vigil (Weber). J. Exp. Zool. 167:487-495.
tance with the assays for GPD.
Jahromi, S. S. and H. L. Atwood. 1969. Structural
features of muscle fibers in the cockroach leg. J.
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