AMER. ZOOL., 27:991-1000 (1987)
Fiber Ultrastructure and Contraction Kinetics in
Insect Fast Muscles 1
ROBERT K. JOSEPHSON
Department of Psychobiology, University of California,
Irvine, California 92717
AND
DAVID
YOUNG
Department of Zoology, University of Melbourne,
Parkville, Victoria 3052, Australia
SYNOPSIS. Isometric contraction kinetics were measured and fiber structure was quantified in tymbal muscles from different cicada species. Twitch duration is directly correlated
with the size of the myofibrils and with the ratio of the fraction of fiber volume which is
myofibril to that which is sarcoplasmic reticulum (SR) and T-tubules (fast muscles have
small myofibrils and a relatively large volume of SR and T-tubules). Twitch duration is
not significantly correlated with fiber size, with sarcomere length, nor with the fractional
volume of the fibers which is mitochondria, indicating that these structural features are
not strongly involved in the determination of isometric contraction kinetics. In the tettigoniid Neoconocephalus robusius, twitches from forewing muscles of male animals become
progressively shorter over the first five days following the adult molt. This change in
contraction kinetics is associated with an increase in the relative volume of SR and T-tubules. Denervation blocks the acquisition of rapid kinetics, indicating that neural input is
necessary for this transformation.
tural differences are apparent only with the
The cells of striated muscle, the muscle greater resolution available with electron
fibers, occur as a broad set of variations on microscopy. Among ultrastructural differa common theme. Some muscle fibers are ences between muscle fibers are the orgafast, others slow; some easily fatigued, oth- nization and dimensions of thick and thin
ers fatigue resistant; some relatively strong, filaments; the organization, spatial distriothers weak; in some, maintenance of ten- bution, and relative abundance of the sarsion is metabolically efficient, in others coplasmic reticulum (SR) and T-tubules;
costly. These differences in functional the kinds of junctions between SR and
properties are a result of fiber differences T-tubules; the thickness of the Z-line; the
in structural organization and in chemical abundance and distribution of glycogen
granules; and the organization of mitoconstituents (Josephson, 1975).
Some of the differences between fibers chondrial cristae. Other differences
can be seen with a light microscope. Struc- between fibers are biochemical and not
tural features which vary from fiber to fiber directly revealed by ordinary light or elecand which are visible with light microscopy tron microscopy. Biochemical differences
include fiber length, thickness, and shape; among fibers include the specific activity
sarcomere length; dimensions of A and I of aerobic and anaerobic pathways of
bands; position and abundance of nuclei energy production; the specific activity of
and mitochondria; whether the myofibrils myosin ATPase and the lability of this
are obvious (Fibrillenstruktur) or not ATPase in solutions of different pH; and
(Felderstruktur); and the shape, size, and the site of calcium regulation of contracorientation of the myofibrils. Other struc- tion {i.e., whether this is a feature of
the thin filaments or the myosin filaments,
Lehman and Szent-Gyorgyi, 1975). Some
1
From the Symposium on Muscle Fiber Typing as a of the biochemical differences can be
Bioassay of Xerve-Muscle Interaction: Comparison of
revealed with appropriate histochemical
Arthropod and Vertebrate Systems presented at the Annual techniques. Finally, there are some funcMeeting of the American Society of Zoologists, 27tional differences between muscle fibers
30 December 1985, at Baltimore, Maryland.
INTRODUCTION
991
992
ROBERT K. JOSEPHSON
which have, as yet, no known structural or
biochemical substrates. Among these are
the shape of the force-velocity curve; the
extent to which stretch activation (Pringle,
1978), force enhancement during stretch
(Edman et ai, 1978), or mechanical depression due to shortening (Edman, 1980) are
prominent properties; and the occurrence
and extent of latency relaxation (Hoyle,
1980) among others. The "type" of a muscle fiber is defined by its position in the
multidimensional spectrum of possible
functional, structural, and biochemical
variation. The following is concerned with
contraction kinetics and muscle fiber structure and ultrastructure as indices of fiber
type, and relationships between the structure of a muscle fiber and its performance.
ULTRASTRUCTURE AND CONTRACTION
KINETICS OF CICADA MUSCLES
For some time we, together with Dr. H.
Elder of Glasgow University, have been
quantifying relations between muscle
ultrastructure and contraction kinetics in
insect fast muscles. The goals of this program are to determine how well functional
properties of a muscle can be predicted
from muscle ultrastructure or, conversely,
ultrastructure from performance; and to
identify limits to muscle performance
imposed by the muscle's structure. We have
examined wing muscles from members of
the orthopteran family Tettigoniidae, and
tymbal muscles from cicadas. The analysis
of tymbal muscles is most complete, and
cicada muscles will be used to illustrate the
approach and to draw some conclusions.
Tymbal muscles are the sound-producing muscles of adult male cicadas. They lie
in the first abdominal segment and are connected to a modified plate of surface cuticle, the tymbal. Contraction of the muscle
buckles the tymbal, producing a sound
pulse or a set of sound pulses.
For several reasons tymbal muscles are
nearly ideal for the task of correlating muscle contraction kinetics and ultrastructure.
First, the muscles are moderately large, 1050 mg each in cicadas of typical size, and
they are quite accessible. They lie in the
abdomen surrounded by a large air sac,
and so are essentially pre-dissected. Second, each muscle is a single motor unit.
Stimulating the motor nerve to the muscle
initiates twitches whose amplitude is constant and quite independent of the strength
of the stimuli so long as they are above a
single, sharp threshold (Josephson and
Young, 1981). Anatomically the nerve to
the tymbal muscle contains one large
motoraxon and some small axons of
unknown destination and function (Hagiwara et ai., 1954; Pringle, 1954; Wohlers
etal., 1979). Third, the fibers within a tymbal muscle appear to be structurally homogeneous, which reduces sampling problems since a piece from any part of a muscle
may be taken as representative of the muscle as a whole. Finally, tymbal muscles from
different species offer a fairly wide range
of muscle contraction kinetics and an associated wide range in muscle ultrastructure
(Fig. 1). Tymbal muscles of most cicada
species are synchronous muscles with a oneto-one relation between muscle action
potentials and contractions. The tymbal
muscles of a few species, however, are asynchronous muscles, the self-oscillatory muscles found in some insects, especially as wing
muscles in insects with high wing stroke
frequencies. The contraction kinetics and
ultrastructure of synchronous and
asynchronous muscles are quite different
(Josephson and Young, 1981). The muscle
contraction frequencies during sound production for cicadas with synchronous tymbal muscles range in different species from
40 Hz to about 550 Hz in one spectacular
example (Young and Josephson, 1983,
1985; Josephson and Young, 1985): 550
Hz is, by a wide margin, the highest contraction frequency known for any synchronous muscle. There is a good correlation
between operating frequency and twitch
brevity in different cicada species (Young
and Josephson, 1983, 1985), and the differences in contraction frequency represent a fair range in twitch time course. The
slowest contraction frequency, 40 Hz, is
still rather high. All synchronous tymbal
muscles are fast muscles. In establishing
relationships between ultrastructure and
contraction kinetics, it would be useful to
have some slower examples of synchronous
tymbal muscles than any yet reported, but
the fast, high-frequency part of the fiber
spectrum is well represented.
FIBER ULTRASTRUCTURE AND CONTRACTION KINETICS
In the results to be presented, muscle
twitches were measured isometrically.
Numerical values for kinetics are based on
measurements from seven to eight muscles
from each species. Muscles were fixed using
standard procedures for transmission electron microscopy. Sarcomere length was
determined from longitudinal sections
examined with the light microscope. Muscle fiber area, circumference, and maximum diameter were measured from photographs of muscle cross sections taken
through a light microscope. Myofibril
dimensions were determined from electron micrographs. A point-count method
was used to determine the fractional volume of a muscle fiber which is myofibrils,
tubular systems (sarcoplasmic reticulum
and T-tubules), or mitochondria. Typically
three muscles from each species were used
in structural analyses. More complete
information on the techniques is given by
Josephson and Young (1981, 1985).
The correlations to be considered will
be from a group of nine cicada species with
synchronous tymbal muscles. Equivalent
data on muscle ultrastructure and contraction kinetics is available for one species with
asynchronous tymbal muscles, Platypleura
capitata, for comparison with the synchronous muscles. The species with synchronous muscles and an operating frequency
greater than 500 Hz, Okanagana vanduzeei,
is of particular interest for its extraordinary performance. Unfortunately this
species proved a difficult animal from which
to measure twitch contraction kinetics, and
only a few examples of isometric twitches
were obtained from a large number of individuals examined (see Josephson and
Young, 1985). Because of the small sample
size for the physiological measurements, 0.
vanduzeei will not be used in quantitative
comparisons.
Twitch time course is not correlated
with fiber size or sarcomere length
993
contraction kinetics, were muscle fiber size
and sarcomere length.
There was significant variation in the size
of the muscle fibers in the tymbal muscles
examined. The mean fiber area in the nine
species ranged from 2.2 x 103 ^m2 (SE =
0.2 x 10s nm2) in the species with the thinnest fibers to 4.7 x 10s ^m2 (SE = 1.0 x
10s /tm2) in the species with the thickest
fibers. The regression coefficients between
measures of fiber size (fiber circumference,
maximum diameter, area), and those of
twitch brevity (twitch rise time, decay time,
total duration) were all very small and far
from statistically significant.
In Crustacea, fibers which give slow,
facilitating contractions tend to have longer
sarcomeres than fibers which produce fast,
twitch-like contractions (Atwood, 1973). In
the cicada tymbal muscles there was not a
statistically significant relation between
sarcomere length and measures of twitch
brevity (Fig. 2A). However in the cicada
muscles the range of sarcomere lengths
across species was rather small. The sarcomere length in the species with the shortest sarcomeres averaged 2.24 nm, that in
the species with the longest sarcomeres 2.79
jim. Perhaps sarcomere length is a significant determinant of contractile performance only in relatively slow muscles, and
in fast muscles, like those of the cicada
series, sarcomere length is at a practical
minimum. Long sarcomere lengths are
found associated with slow contraction
kinetics in a katydid wing muscle which
contains heterogeneous fibers (Stokes et al.,
1975). The mitochondrial volume density,
that fraction of the muscle fiber volume
occupied by mitochondria, also was not statistically significantly correlated with measures of twitch time course in the ciada
muscles. The range in mitochondrial volume density was quite small, 34% to 42%
of the total fiber volume in the different
species.
Some morphological features of muscle Twitch time course is correlated with
fibers can vary without the variation being fibril size and SR development
reflected in the isometric contraction
The ratio of the volume of the muscle
kinetics. Among structural features which fiber as myofibril to that as sarcoplasmic
were not correlated with twitch time course reticulum and T-tubules (these two cateand which, therefore, do not seem to be gories were not separated in the analysis)
critically involved in the determination of was used as an index of the relative devel-
ROBERT K. JOSEPHSON
'•'.:'•'•'.: "_'•'<"/•'•'•:::•
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995
FIBER ULTRASTRUCTURE AND CONTRACTION KINETICS
20-
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10-
2.0
3.0
4.0
Sarcomere Length, urn
1.0
2.0
3.0
4.0
% Fibril / % SR&T
FIG. 2. Relations between twitch duration and fiber structure, cicada tymbal muscles. Each diamond is from
a different species. The vertices of the diamonds are the mean plus and minus one standard error for both
abscissa and ordinate. Twitch duration was measured from onset to 50% relaxation at 30°C. (A) Sarcomere
lengths are similar in all cicada muscles and there is no correlation between twitch time course and sarcomere
length. (B) There is a clear, statistically-significant correlation between twitch duration and the relative
development of the sarcoplasmic reticulum and T-tubules. The line is the least-squares regression line for
the mean values of the parameters (r = 0.82). The cicada species represented, in order of increasing twitch
duration, are: Psaltoda claripennis (included in A only, erratic fixation with muscles of this species precluded
stereometric analysis), P. harnsn, P. argentata, Tamasa tristigma, Cydochila australasiae, Abncta curvicosta, Arunta
perulata, Chlorocysla vindis, and Cystosoma saundersu.
opment of the tubular systems within the
muscle. Since the volume of the SR is much
greater than that of T-tubules, the ratio is
principally a measure of the relative amount
of SR. Twitch rise time, relaxation time,
and total duration were all significantly
correlated with the ratio of myofibril volume to SR and T-tubule volume (Fig. 2B).
There were even better correlations
between parameters measuring the time
course of a twitch and those reflecting the
size of the myofibrils within a fiber (myofibril area, circumference, or maximum
diameter, Fig. 3). Interestingly, the twitch
rise time in the asynchronous muscle was
about that which would be predicted from
the area of its myofibrils and the regression
between twitch rise time and fibril area
established for the synchronous muscles.
The twitch decay time, on the other hand,
was about five times longer than would be
predicted from the myofibril area of the
asynchronous tymbal muscle. The asynchronous muscle had very little sarcoplasmic reticulum (Fig. 1, lowest panel); the
ratio between fibril volume and SR and
T-tubule volume in this muscle was 18.5
(SE = 1.5), which is well off the scale of the
synchronous muscles (Fig. 2B). The size of
the myofibrils in the asynchronous muscle
FIG. 1. Twitch time course and fiber ultrastructure in cicada tymbal muscles. The traces superimposed on
the micrographs are isometric twitches at 30°C. These are displayed at the same time base (shown in lower
panel) and scaled to the same amplitude. The micrographs are representative fiber cross sections. The upper
panel is from Okanagana vanduzeei. This tymbal muscle is a synchronous muscle, and it is the muscle with the
highest known repetition frequency (550 Hz) of any synchronous muscle. The middle panel is from Cystosoma
saundersii whose tymbal muscle is relatively slow among synchronous tymbal muscles. The bottom panel is
from Platypleura capilala whose tymbal muscle is an asynchronous muscle. The scale in the upper panel applies
to all the micrographs. Abbreviations: F—myofibril; M—mitochondrion; S—sarcoplasmic reticulum; T—
lumen of a T-tuble.
ROBERT K. JOSEPHSON
996
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Fibril Area, urn
FIG. 3. Correlations between twitch kinetics and myofibril area. The diamonds are mean plus and minus
one standard error. The diamond with vertical hatching in A and in B is the asynchronous tymbal muscle
from Platypleura capitata. The lines are least squares regression lines fitted to the values for synchronous
muscles only (i.e., the P. capitata points were not used in the construction of the regression lines). (A) Twitch
rise time is strongly correlated with myofibril area (r = 0.96). The rise time of twitches in the asynchronous
muscle is close to that which would be predicted from the size of its myofibrils. (B) Twitch relaxation time is
also correlated with myofibril size (r = 0.90), but the relaxation time in the asynchronous muscle is about 5
times longer than would be predicted from the size of its myofibrils and the regression derived from synchronous muscles (note the break in the ordinate and the change in scale above the break). The species
represented, in order of increasing fibril area, are: Ps. claripennis, Ps. argentala, Ps. harrisii, T. tristigma, Cyc.
australasiae, Ab. curmcosta, Ar. perulala, CM. viridis, Cys. saundersii, Pi capitata.
is not greatly different than that of synchronous muscles but the development of
the SR is greatly reduced; the rise time of
twitch contractions is not greatly different
than that in synchronous muscles but the
twitch decay time is. Seemingly twitch rise
time is not very dependent on SR development, while relaxation time may well be.
In summary, there are correlations
between fiber ultrastructure and contraction kinetics, and the relations are sensible.
Contractile activity of the myofibrils is initiated by calcium diffusing into the myofibrils after its release from the sarcoplasmic
reticulum, and contraction is terminated
by resequestration of the calcium by the
SR. Fast twitches are found to be associated
with small myofibrils, hence short diffusion
distances for calcium from fibril surface to
center, and with hypertrophied sarcoplasmic reticulum and T-tubules. Increasing the amount of SR increases the volume
of SR from which calcium can be released
to activate the myofibrils, and, more
importantly, increases the area of SR available to transport calcium out of the general
cytoplasm to terminate contraction. The
observation that the asynchronous muscle
in the series has very little SR, yet the twitch
rise time is not extraordinarily long (Fig.
3B), suggests that it is myofibril size and
diffusion time throughout the myofibril
rather than the volume of the calcium store
that limits the rate at which muscle is turned
on.
Fibers can by typed by ultrastructural
criteria, and the ultrastructural types are
related to contractile performance. In the
context of this symposium it is appropriate
to ask if the structural and ultrastructural
differences between insect muscle fibers are
under neural control. Cicadas are poor
candidates for developmental studies since
the nymphal stages are long and spent
997
FIBER ULTRASTRUCTURE AND CONTRACTION KINETICS
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FIG. 4. Twitch duration (onset to 50% relaxation, 35°C) for mesothoracic (filled circles) and metathoracic
(open symbols) wing muscles of the tettigoniid Neoconocephalus robustus in late nymphal instars and after the
adult molt. Vertical lines indicate standard errors, n = 5-7. The points marked " W" are from animals captured
as mature adults but are otherwise of unknown adult age. The other points are from animals captured as
nymphs and raised in the laboratory. (After Ready, 1983; see also Ready, 1986).
underground, and the adult stage is short
and difficult to maintain in the laboratory.
Some information relevant to the question
of the neural control of muscle properties
in insects has come from recent studies of
muscle development in a tettigoniid.
NEURAL INPUT AND MUSCLE
DEVELOPMENT IN A TETTIGONIID
There is an expansive literature documenting neural influences on muscle properties in vertebrates, especially mammals.
In contrast, there is little information on
the neural control of muscle fiber diversity
in arthropods. Neural input is necessary
for the long term maintenance of insect
muscles, which atrophy when denervated
(Rees and Usherwood, 1972). The story is
more complex in Crustacea since nerve terminals may survive for long periods after
axotomy, so nerve section may not remove
trophic neural inputs to a muscle (Hoy et
al., 1967; Bittner, 1973). There are some
hints from insect studies that neural input
is not a dominant influence on muscle fiber
properties. During insect development
there may be major changes in muscle
ultrastructure and contraction kinetics even
though the muscle remains innervated by
the same neurons (Rheuben and Kammer,
1980; Ready and Najm, 1985). Here it
might be argued that changing neurotrophic factors released by the neurons or
altered activity patterns in the muscle
evoked by the neurons are directive for
muscle development, but there is not direct
evidence for this. Some fibers in a portion
of a tettigoniid muscle have long sarcomeres and slow contractile properties but
are innervated by branches of an axon
which also innervates fast fibers elsewhere
in the muscle (Stokes et al., 1975). Thus a
"motor unit" may contain both fast and
slow fibers. Neural input has been shown
to be necessary for the transformation of
fiber type which occurs during the normal
maturation of the crusher claw of the lobster, and here it is likely that it is the activity
pattern imposed on the muscle which is
998
ROBERT K. JOSEPHSON
muscles of the metathoracic segment. Thus
in adjacent segments of N. robustus there
are homologous muscles with vastly different maximum operating frequencies, 200
Hz for the mesothoracic muscles and 25
20Hz for their metathoracic counterparts.
Associated with this difference in maximum operating frequency, the contraction
Q
kinetics of wing muscles in the two segments are quite different, with twitches
10being about half as long in the mesothoracic muscles as in metathoracic homologs
(Josephson, 1984).
Ready (1983, 1986) has shown that the
difference in contraction kinetics between
1.0
2.0
5.0
3.0
4.0
mesothoracic and metathoracic wing muscles is a result of developmental processes
% Fibril / % SR&T
which occur over a short period late in the
FIG. 5. Twitch duration and the relative develop- animal's life. In nymphs one or two instars
ment of SR and T-tubules in cicada tymbal muscles
and in a mesothoracic wing muscle of A', robustus. The before adulthood, and in adults on the first
open circles and the regression line are for the cicada day of adult life, the contraction kinetics
tymbal muscles and are as in Fig. 2B without the of mesothoracic and metathoracic muscles
standard error display. The diamonds are for N. robus- are similar and are like those of metathotus muscles during late development (mean plus and
minus one standard error). The N. robustus muscles, racic muscles in mature adults (Fig. 4). Over
in order of decreasing twitch duration, were from the first 5 days of adult life twitches in the
animals in the last nymphal instar, animals after one mesothoracic muscles become progresday of adult life, animals after 3 days of adult life, sively briefer, and by the fifth adult day the
and animals after 5 days as adults. The values for N. twitch duration is about half of its original
robustus are from Ready (1983). The twitch durations
were originally measured at 25°C; these were cor- value.
rected to 30°C using a Q10 of 1.9 (Josephson, 1984).
Accompanying the increasing twitch
brevity is a progressive increase in the relative development of sarcoplasmic reticuimportant (Govind and Kent, 1982; Go- lum and T-tubules. Interestingly, throughvind, 1985). Another example in which out early adult life the relation between
neural input is necessary for muscle mat- the relative development of sarcoplasmic
uration is seen in the stridulatory muscles reticulum and twitch duration is similar to
of the tettigoniid Neoconocephalus robustus. that predicted by the regression line for
Adult male tettigoniids produce a calling cicada muscles (Fig. 5). The quantitative
song which attracts females. The song is relation between twitch duration and SR
produced by rubbing together specialized development shown in Figures 2B and 5
structures on the forewings. The songs of may be a general one for fast, synchronous
some tettigoniids are remarkable for the muscles. The myofibrils in muscles of N.
high pulse frequency achieved. In N. robus- robustus are ribbon-shaped rather than
tus the pulse frequency during stridulation tubular as in the cicada muscles considered
is about 200 Hz. The muscles involved in above (Elder, 1971). Myofibril cross-secsound production are synchronous muscles tional area in N. robustus depends on the
width of the ribbon (its length in cross sec(Josephson and Halverson, 1971).
tion)
and this varies considerably from fibril
The forewing muscles of N. robustus are
to
fibril
within a single muscle fiber. Thus
used in stridulation and flight, the hind
wing muscles in flight alone. The wing it is not meaningful to compare the relastroke frequency during flight is about 20 tion between twitch parameters and fibril
Hz (Ready, 1983). The muscles of the fore- size in A', robustus with that in cicadas.
wings, those of the mesothoracic segment,
Xeural input is important for the transare serially homologous with the hindwing formation of mesothoracic wing muscles
30 -|
FIBER ULTRASTRUCTURE AND CONTRACTION KINETICS
denervated
25 -I
3 day
20-
999
4
4
3 day
4 day
*?
4 day
A
I
I control
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10-
5-
FIG. 6. The effects of denervation on the acquisition of fast contraction kinetics in mesothoracic wing muscles
of N robustus. Animals were captured as nymphs and maintained in the laboratory until the adult molt. One
day after the adult molt the nerve supplying the first tergocoxal wing muscle was unilaterally exposed and
sectioned. Isometric twitches (30°C) were recorded from the denervated muscle and its contralateral control
3 or 4 days after the operation. The bars indicate mean twitch duration (onset to 50% relaxation). Vertical
lines indicate standard errors (n = 5-7). The left two pairs of bars are results from male animals. The dashed
line above these bars is the expected twitch duration on the first adult day, based on data from Ready (1983)
for 25°C corrected to 30°C using an assumed Q10 of 1.9. Denervation partially blocks the acquisition of rapid
kinetics and the innervated side becomes progressively faster than the denervated muscle. The next two pairs
of bars are results from muscles of females. In females there is not a great increase in twitch brevity following
the adult molt. Denervation alone results in a small difference between experimental and control muscles,
presumably because of a slowing of twitch time course following denervation, but this effect is small compared
to the difference between experimental and control muscles in males during the period of rapid muscle
change. The rightmost column pair is for animals captured as mature adults in which mesothoracic muscles
were unilaterally denervated and twitch properties measured 4 days later (after Novicki and Josephson, 1987).
from muscles with contraction kinetics like
those of ordinary flight muscles to those of
the extraordinary muscles used in stridulation. Denervation of a mesothoracic muscle on the second adult day slows or halts
the transformation in progress (Novicki and
Josephson, 1987). The contraction kinetics
of the denervated muscle, tested a few days
after the operation, are slower than those
of the contralateral control and the difference between denervated muscle and control becomes greater with time. The difference in contraction kinetics between the
denervated muscle and its contralateral
control is probably a result of both a general muscle slowing following denervation
and the specific interruption of a developmental program in progress. Female
animals do not stridulate, and mesothoracic wing muscles from adult females do
not have the very rapid contraction kinetics characteristic of meso-thoracic muscles
from adult males. Mesothoracic wing muscles from females, denervated shortly after
the adult molt, are slightly slower than control muscles when tested a few days after
the operation. Similarly, denervated mesothoracic muscles from mature adult males,
muscles in which the transformation to very
rapid contraction kinetics is already complete, are somewhat slower than contralateral control muscles a few days after the
operation. But in both female muscles during early adult development and in mature
males, the slowing of contraction kinetics
associated with denervation is relatively
1000
ROBERT K. JOSEPHSON
small (5% in females, 19% in males operated on as mature adults, both measured
on the fourth postoperative day). The
major difference between experimental and
control muscles in the early adult males
(41% on the fourth day) must be a result
of blocking the muscle transformation.
Neural input is important for the transformation. It is not known if the neural
input directs the transformation, or merely
provides permissive conditions for a transformation controlled by hormonal or
genetic controls.
Hoyle, G. 1980. Comparative aspects of the onset of
muscular contraction with special reference to
latency relaxation. Comp. Biochem. Physiol. 66A:
57-68.
Josephson, R. K. 1975. Extensive and intensive factors determining the performance of striated
muscle. J. Exp. Zool. 194:135-154.
Josephson, R. K. 1984. Contraction dynamics of flight
and stridulatory muscles of tettigoniid insects. J.
Exp. Biol. 108:77-96.
Josephson, R. K. and R. C. Halverson. 1971. High
frequency muscles used in sound production by
a katydid. I. Organization of the motor system.
Biol. Bull. Mar. Biol. Lab., Woods Hole 141:411433.
Josephson, R. K. and D. Young. 1981. Synchronous
and asynchronous muscles in cicadas, j . Exp. Biol.
91:219-237.
ACKNOWLEDGMENTS
Josephson, R. K. and D. Young. 1985. A synchroOriginal research was supported by
nous insect muscle with an operating frequency
greater than 500 Hertz. J. Exp. Biol. 118:185grants PCM 8201559 and DCB 8416277
208.
from the National Science Foundation. We
W. and A. G. Szent-Gyorgyi. 1975. Regwish to thank J. Malamud and A. Novicki Lehman,
ulation of muscular contraction. Distribution of
for helpful comments on the manuscript.
actin control and myosin control in the animal
kingdom. J. Gen. Physiol. 66:1-30.
Pringle, J. W. S. 1954. The mechanism of the
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