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* Muscle Proteomics and Nanotechnology Section, Laboratory of Muscle Biology, National Institute of Arthritis and Musculoskeletal and Skin Diseases; and
NIH Magnetic Resonance Imaging Research Facility, National Institute of Neurological Disorder and Stroke, NIH, and Department of Health and Human Services, Bethesda, Maryland, USA
1Correspondence: Laboratory of Muscle Biology, Bldg. 50, Rm. 1140, National Institute of Arthritis and Musculoskeletal and Skin Diseases, NIH, Bethesda, MD 20892-8024, USA. E-mail: wangk{at}exchange.nih.gov
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: multimodal imaging • Z-band lattice • myofilament length regulation • sarcomere proportion • supercontraction
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, 2)
, the swimbladder muscle of toadfish (2
3
4)
, and the tymbal muscle of cicadas (5
, 6)
. Known as "sonic" muscles, they typically operate at frequencies above 
50 times per second (Hz), rates that are 2- to 3-fold of those that can be attained by typical skeletal muscle (2)
. Most sonic muscles are synchronous (or neurogenic) whereby each nerve impulse triggers one muscle contraction. This is in contrast to other high frequency muscles such as some insect flight muscles that are asynchronous (myogenic), and in this situation each nerve impulse produces multiple stretch-activated contractions that are propagated by the antagonistic movement of the thorax and the wings (7)
. Synchronous superfast muscles frequently incorporate speed-enhancing organization that allows ample ATP production and delivery, fast calcium triggering, and rapid relaxation, along with efficient force transmission. Here we present insights from the tymbal muscle of the male periodical cicada, Magicicada cassini (brood X), as billions of these insects emerged in 2004 to pay their once-in-17-year visit above ground to mate in the northeast and midwest United States. We have explored the functional anatomy of this muscle by state-of-the-art multimodal imaging and examined the structural and functional properties on how it produces the incessant mating sound by vibrating the tymbals and resonating sound in the body cavity. We observed that myofilament structure is specifically adapted for high speed and endurance in cicada tymbal muscle.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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For microcomputed tomography (micro-CT) imaging, specimens were immobilized on a foam pad and placed in the scanning chamber. Images were obtained on a MicroCAT II scanner (Imtek, Knoxville, TN) using an X-ray voltage of 35 kVp with 500 µA and an exposure time of 3 s per projection radiograph. Total image acquisition time was 42 min. A three-dimensional (3D) CT image volume was reconstructed from 1440 projections (1024x1376 image matrix with 2x2 binning) acquired at 0.66° intervals over a complete circle. Isotropic resolution of the reconstructed 3D image was 60 µm.
For magnetic resonance (MR) imaging, specimens were immobilized in a custom-built chamber filled with Fomblin LC-08 perfluorinated polyether (Solvay Solexis, Thorofare, NJ) to minimize image distortions due to magnetic susceptibility differences between tissue and air. The hollow abdominal cavity of the male cicada was also filled with Fomblin. Fomblin is an ideal compound for MR imaging since it is inert and does not have a large background signal as that typically seen when the sample is suspended in isotonic saline. Imaging data were acquired on a 7.0 Tesla microimaging NMR spectrometer using a 89 mm vertical superconducting magnet (Bruker Spectrospin, Karlsruhe, Germany) with a 35 mm ID actively shielded gradient. The system used a Bruker Avance NMRI console controlled by Paravision 3.0.1 software (Bruker Instruments, Billerica, MA). Images were acquired using a 3D spin-echo sequence with an echo time of 10.1 ms, a repetition time of 500 ms, and an acquisition bandwidth of 101 kHz. A 30 mm ID birdcage volume RF resonator was used in these experiments. Isotropic image resolution was 78 µm.
Vibration and Sound Recording
Vibration measurements from the external surface of the tymbal during sound production were obtained using a Brüel & Kjær Model 8329 Laser Vibrometer (Brüel & Kjær North America, Norcross, GA). Wings of male cicadas were clipped at their hinges to expose the tymbal, and the insect was adhered to a stable base. The laser spot was positioned on the surface of the tymbal and focused to maximize the signal. No reflective tape on the target is needed with this instrument, as the natural reflectivity of the tymbal surface produced a strong vibration signal. Spatial resolution of the laser was less than 250 µm. The laser vibrometer has a 25 kHz bandwidth so the output was low-pass filtered with a SR650 filter (Stanford Research Systems, Sunnyvale, CA) and digitized with a National Instruments A/D card (Austin, TX) at 100 kHz. Simultaneous sound recordings were made with an amplified microphone at a sampling rate of 100 kHz.
Light and Electron Microscopy
Thoracoabdominal regions from male cicadas were dissected in chilled PBS containing Sigma protease inhibitor cocktail (Sigma, St. Louis, MO; 1:100 dilution) and then placed in cold fixative composed of 3% glutaraldehyde and 2% paraformaldehyde in 0.1 M cacodylate buffer (pH 7.2) for 2 h. Tymbal and flight muscle fibers were microdissected from the thoracoabdominal region and fixed for an additional 40 min, washed twice with cacodylate buffer, and postfixed for 1 h with 1% osmium tetroxide in 0.1 M cacodylate buffer. Samples were stained with 1% tannic acid (aq) for 30 min, washed with distilled water, and then en bloc stained with 2% uranyl acetate (aq) for 30 min. Tissue blocks were dehydrated in ascending concentrations of ethanol, infiltrated with Spurrs resin overnight, embedded, and polymerized at 60°C for 12 h. All chemicals for electron microscopy (EM) were purchased from Electron Microscopy Sciences (Ft. Washington, PA).
Longitudinal and cross-sections of muscle samples were prepared for light microscopy by staining semithick sections with 1% toluidine blue (aq) at 50°C for 30 s. For EM, ultrathin sections were collected on copper grids, stained briefly with uranyl acetate (2% aq) and lead citrate (0.1% aq), and viewed with a Philips CM-120 transmission electron microscope (Eindhoven, the Netherlands). Images were recorded on large format negatives and digitally scanned. Negatives were calibrated to a carbon replica grid taken at the same magnification. Morphometric measurements were performed with ImageJ software, and mitochondrial percentages were obtained by overlaying a transparent 6.4 mm square grid over images printed at a final magnification of x10,000 and counting the number of grid intersections that overly mitochondria.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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3.0 cm body length) was first to appear in May, followed in June by the smaller sized M. cassini and M. septendecula (2.3 cm body length). M. cassini are distinguished by their entirely black abdomen, whereas M. septendecim and M. septendecula exhibit orange stripes along the underside of each abdominal segment. In all species, strikingly bright red eyes are a hallmark feature. Other members of the Magicicada species exist in the same regions. However, these closely related species emerge on a 13 yr lifecycle (8)
. In addition to the periodical cicadas, there are the annual Dogday cicadas (Tibicen canicularis) that emerge every year in July and August.
Periodical cicadas spend the majority of their life as nymphs underground suckling on sap from tree roots, a mere 1% of their lifetime is spent above ground (see Supp. 1 showing the lifecycle of the cicada). It is believed that a genetically determined developmental synchronization of the species is responsible for their timely exodus to the surface to reproduce. When the soil temperature exceeds 64°F (9)
, the underground-dwelling nymphs emerge and attach to small plants or trees to molt their exoskeleton. Metamorphosis takes 1–1.5 h to complete, and during this time the wings unfold, elongate, and harden. After a few hours, the cream-colored exoskeleton of the newly morphed cicadas turns black and hardens and the cicadas climb to the tops of tree branches to fully mature. This "teneral" adult stage lasts for a period of 4–6 days.
Males of each of these 17 yr periodical species are easily identified by their characteristic mating call used to attract females (10)
. M. septendecim produces a pure tone song that resembles the word "pharaoh," whereas the mating song of M. cassini consists of a series of ticks followed by a final buzz (Supp. 2 movie). M. septendecula, on the other hand, produces short chirps with each string of chirps lasting 10–30 s (Supp. 3 movie). Each of these species produce a protest call when gently perturbed.
Once the males have attracted a female, they will mate over a period of 1 h whereby males clasp onto the posterior aspect of the female and introduce their sperm to fertilize the eggs (Supp. 4 movie). A few days after egg fertilization, the females deposit their eggs under the bark of small branches of trees using their ovipositor (Supp. 4 movie). While in the branch, the eggs mature over a period of 2 mo and then rupture from their capsule emerging as small nymphs that then fall to the ground and rapidly burrow into the soil (Supp. 1 image). These offspring begin the underground nymph stage and will emerge to mate after 17 yr (Brood X, 2021).
Functional anatomy of the tymbal organ
How do the male cicadas produce these series of songs and choruses used to attract females of the same species? The anatomical basis of sound generation is the tymbal organ located in their first abdominal segment (Fig. 1
). A pair of superfast tymbal muscles originates from a common midline ventral structure termed the chitinous V. Each muscle projects dorsolaterally and collectively forms a V-shaped structure that can be visualized in 3D micro-CT (Fig. 1B
), in cross-sectional micro-CT and MR imaging (Fig. 1C and D
), and in the transected abdominal cavity (Fig. 1E
). An animated micro-CT movie of the tymbal muscle position within the cicada is in the supplemental data (Supp. 5).
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Each tymbal muscle inserts into a chitinous tendon plate known as the apodeme plate that narrows into a thin tendon-like structure or apodeme (Fig. 2
B). The apodeme tendon attaches to the inner supero-posterior aspect of a stiff-ribbed cuticular membrane (tymbal) that is located beneath the folded wing (Figs. 1F
and 2A and B)
. Viewed laterally with the wing removed (Figs. 1E
and 2A)
, the roughly triangular shaped tymbal measures 2 mm in width and 3.5 mm in height. On the external surface, 11 vertically arranged, chestnut-colored sclerotised ribs course from the top to the bottom of the tymbal. These long ribs narrow to 50 µm at the midpoints of the ribs (equator) and widen to 100 µm above and below the equator. Center-to-center spacing of the long ribs was 160 µm at their midpoints. At the tymbal equator, the long ribs are interposed by short, 350 µm long vertical tan-colored ribs located equidistant at 80 µm intervals between the long ribs (Fig. 2A
).
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When tymbal muscles contract and pull on the apodeme, they cause the ribbed tymbals to buckle inward, or "click," resulting in a resonating sound emitted from large air sacs in the thorax and abdomen (Fig. 2C
). This click is amplified by the vast air-filled space in the abdominal cavity of the males, which is largely responsible for the resonating sound produced by the tymbal organ. The hollow abdominal cavity, in effect, acts as a Helmholtz resonator in a similar fashion to the way that a guitar or violin resonates the string vibrations within the hollow chamber of the instrument.
Left and right muscles of the tymbal organ contract alternately (Fig. 2C
; Supp. 6), a pattern that has been shown to be the case in Magicicada and other cicada species (5
, 6
, 10
, 11)
. Contraction is initiated by an action potential from a large motor neuron supplying each tymbal muscle, resulting in an all-or-nothing twitch with a single, sharp threshold that takes 8 ms to reach full tension (10)
. During sustained song and protest calls, tymbal muscles from M. cassini contract at a frequency of 50 Hz (5
, 10)
.
Sound production and rattling of tymbals
Vibration measurements of the tymbal surface using a laser vibrometer revealed a pattern of tymbal deformations resolved to the submillisecond range (Fig. 2D-G
). Muscle contractions (50 Hz) are indicated in Fig. 2E
. During one muscle contraction and one tymbal "click" (Fig. 2F
), a series of vertically aligned stiff ribs in the tymbal membrane buckle inward sequentially beginning from the posterior aspect of the tymbal membrane and progressing to the anterior aspect. As a result, the buckling ribs generate a series of subpulses (Fig. 2F
). In the protest call, five to six regularly spaced 800 Hz subpulses were observed on the membrane surface during one click. These subpulses consisted of three initial smaller amplitude pulses followed by two to three larger amplitude subpulses (Fig. 2F
). Within each subpulse, a dampened oscillation was observed at a frequency of 7.1–7.4 kHz (Fig. 2G
). The frequency of this oscillation corresponded to the dominant sound output frequency recorded simultaneously with a microphone from the immediate vicinity of the tymbal (red line in Fig. 2G
).
The external surface of the tymbal exhibited an incremental inward movement ranging between 5–20 µm per subpulse (Fig. 2G
) with a total inward deflection of 100 µm based on integrated velocity measurements. At the end of the subpulses, an outward restoring movement of the tymbal appeared to be relatively rapid, taking only 0.5 ms to complete in comparison to the inward deflection or "click," which took 7.5 ms (Fig. 2F
). These recordings indicated that the tymbal membrane was restored to its original convex shape very rapidly and suggest that a small release of tension in the muscle caused a large change in the shape of the tymbal. This rapid recovery of the tymbal is likely due to the spring-loaded nature of the stiff ribs embedded within the resilin-rich tymbal (12)
.
Interestingly, each pulse resulting from a muscle contraction yielded only five to six stages of rib buckling. This may imply that the buckling of ribs occurs in five to six groups or that only five to six ribs buckle in each tymbal click. Previous work on sound frequencies of M. cassini suggested that the successive buckling of nine ribs is responsible for the production of a nine component subpulse complex (10)
. Why this discrepancy in subpulses between these two studies exists is not understood.
Tymbal muscle: matching hexagonal lattices of myofilaments with perforated Z-bands
Since the driving force of rattling is provided by the tymbal muscle, its design features were examined microscopically, and transverse and longitudinal sections were compared with flight muscle on fiber size, mitochondrial content, sarcomeric structure, and myofilament lattice patterns (Fig. 3
). Tymbal muscle fibers were typically arranged into fascicles containing 15–25 fibers. On average, tymbal muscle fibers were 40% smaller in cross-sectional area than flight muscle fibers (2667±583 µm2, n=93, vs. 4482±1673 µm2, n=54, respectively) and, per unit area, exhibited a significantly higher density of mitochondria (34±3%) than in flight muscle (25±1%). Mitochondria were large and ovoid and aligned longitudinally in rows between myofibrils (Fig. 3D and E
). They were also localized around the peripherally located myonuclei (Fig. 3E
). In general, however, mitochondria were not found in subsarcolemmal regions devoid of myonuclei, as is usually the case in endurance muscle fibers of vertebrates. Air tubes (tracheoles), a common feature of insects that supply oxygen to muscle, invaginated into the muscle fiber and were observed coursing throughout the sarcoplasm (Fig. 3B
).
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Myofibrils in tymbal muscle were fibrillar in structure and showed a similar appearance to those in flight muscle, measuring 1 µm in diameter (Fig. 3B
). The myofilaments in the contractile unit (sarcomere) were arranged in a highly organized double hexagonal array of thin and thick filaments (3:1 ratio) with abundant sarcoplasmic reticulum (SR) encircling each myofibril (Fig. 3B and C
) especially at the level of the Z-band (Fig. 3C
). Triadic couplings were located at each end of the A-band (Fig. 4
A). As in the case of the sonic muscle of male midshipman fish (4)
, the smaller fiber size, higher mitochondrial content, and elaborate SR in tymbal muscle appear to be common adaptations of these fibers to accommodate their high speed contraction and endurance needed to produce mating sounds.
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The most conspicuous difference in tymbal muscle was the shorter myosin containing thick filament length (width of the A-band) compared with thick filaments in flight muscles (compare Fig. 3F and G
). Measuring 2.12 µm in the tymbal muscle (Fig. 3F
) vs. 3.04 µm in flight muscle (Fig. 3G
) and in leg muscle (data not shown), thick filaments in tymbal muscle were 30% shorter in length. Thin filaments also showed a proportional reduction in length in tymbal muscle. The measured length of thin filaments from the proximal edge of the Z-band was 1.08 µm in the tymbal muscle and 1.59 µm in the flight and leg muscles. The 3:1 ratio of thin to thick filaments in the overlap region was similar in all muscles, as well as the diameters of the filaments (10 nm for thin filaments and 20 nm for thick filaments) and lattice spacing of 60 nm between thick filaments (Fig. 3B and C
). M lines were nondescript in both tymbal and flight muscle (Fig. 3F and G
).
Z-bands, which transmit the force produced by the pulling of thin filaments by the molecular motors on the thick filaments to the cytoskeleton and membranes (13)
, were moderately wider in tymbal (180 nm) than in flight muscle (160 nm) in longitudinal sections (Fig. 3F and G
) and nearly two to three times thicker than those of vertebrate muscles. Lattice structure in cross-sectional views of the Z-band consisted of an interconnected hexagonal network with vertices that corresponded to the dimension of the hexagonal arrays in A-bands (Fig. 3C
, insets). A 3D cross-sectional view of the Z-band lattice is shown in a stereo pair in Fig. 4A
(filtered and reverse contrasted). Hexagonal arrays in the Z-band were subdivided by linear densities that created six roughly triangular shaped spaces, with each arm of the triangle measuring 50 nm (Fig. 4B
).
Of great interest in the tymbal muscle was the unexpected ability of its sarcomeres to supercontract to very short length in isolated myofibrils. Two stages of sarcomere contraction, contracted and supercontracted, are shown in Fig. 4C and D
. When contraction was induced in tymbal muscle fibers by caffeine, thick filaments traversed the Z-band into the neighboring sarcomere, resulting in sarcomeres with a length shorter than the A-band width (i.e., shorter than thick filament lengths). We predict such supercontraction was made possible by the presence of perforations within the Z-bands (Fig. 4C
) as well as by the fact that both the Z-band and the thin filament lattice have the same hexagonal lattice as the thick filaments in the A-band (as shown by the diffraction patterns of the cross-sectional lattices in Fig. 3C
inset). These perforations in Z-bands are potentially large enough to allow thick filaments (20 nm in diameter) to slide through and pass into the neighboring sarcomere thin filament zone (Fig. 4D
).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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. In Greek mythology, Tithonus, a mortal consort of the goddess of Dawn Eos, was granted immortality, but not external youth, by Zeus. The aging Tithonus was turned into a ceaselessly chirping cicada and was released into the world. The lifestyle of periodical cicadas is governed mainly by the muscles used to fly, to sing, and to mate. As mediocre flyers, Magicicada outnumbers, rather than evades, its predators. Cicadas are the world’s loudest insects (14)
, and Magicicada excels in this aspect. The orchestration of superfast and enduring tymbal muscles and the large mechanically resonating air sacs (15)
ensures the prelude for action.
Superfast muscles that rattle the tymbal
We seek to understand how specialized features enhance the performance and speed of superfast muscles, with the long-term goal of engineering and importing such designs into vertebrate muscles. Studies of other sonic muscles in nature such as those on the swimbladder of two species of toadfish have revealed unique speed-enhancing structural designs, including a single population of small diameter muscle fibers (2)
, an abundance of SR components to increase calcium handling ability (16)
, fast on-off cross-bridge kinetics (2)
, high mitochondrial content for production of ATP (1
, 17)
, low muscle specific forces (18)
, an intricate cytoskeleton system to organize and coordinate movements (4)
, and, in the midshipman sonic muscle, extraordinarily wide Z-bands in the sarcomere (3
, 4)
. These superfast muscles optimize speed and contraction efficiency and trigger the production of loud mating sounds by the mechanical resonance of the entire sonic organ (e.g., tymbals and swimbladder).
Our current studies have elaborated on the biology of the cicada and the structural features of the superfast cicada tymbal muscle that underlie the mechanism of muscle contraction and tymbal deflection during sound production. Micro-CT and MR imaging provided novel views of the tymbal muscle structure in vivo and illustrated the significant improvement in resolution of these imaging modalities over the past few decades. These modalities have only recently been applied to the study of insects, such as the internal structure of beetles (19)
, Drosophila neural structures (20
, 21)
, and woodlouse circulatory system (22)
. Further use of these modern imaging modalities will lead to a better understanding of internal structure in a wide variety of small organisms.
Tymbal muscles display the common attributes of superfast muscles, including a pure population of muscle fibers containing well-defined crystalline arrays of contractile filaments, high mitchondrial content, and elaborate SR. Physiological studies have shown that the specific force of sonic muscle is very low, which has been considered to be a tradeoff for their rapid contraction speeds (18)
. This tradeoff between force and speed has been demonstrated in other superfast muscles such as the rattlesnake tailshaker muscle (1
, 23)
and in the sonic muscles of the oyster toadfish (2)
.
The sarcomere proportions, i.e., filament length and geometric parameters of the tymbal muscle sarcomere, reflect additional aspects of design principles of a superfast muscle. The 30% shorter length of both thick and thin filaments (as compared with those in flight and leg skeletal muscles) indicates that tymbal muscle fibers contain more and shorter sarcomeres per fiber length. This feature would enhance shortening velocity and high frequency contraction, albeit with a shorter range of dynamic length change per sarcomere (24)
. Additionally, the constant relative length of thick and thin filaments between these muscles indicates that, at rest length, there is nearly a full overlap of the entire thin filaments with thick filament motors and would therefore display maximal isometric force at rest length.
The proportional filament length raises an important question as to how filament lengths are determined in the sarcomere of insects. In mammalian muscle, it is currently believed that two giant proteins, titin and nebulin, regulate the length of thick and thin filaments by serving as a scaffold for the assembly of myosin into the filament (25
26
27)
. The situation with insect muscles is more complex and uncertain. Current evidence indicates that thick filament length in invertebrates, varying widely in length from 0.5 µm in jellyfish swimming muscle up to 32 µm in the foregut muscle of the annelid worm (28)
, is regulated by additional proteins that are located either within the core of the filament or arranged periodically on the outside of the filament (29)
. Further studies that address the alternative splicing of myosin in Drosophila and the regulatory effects of accessory proteins such as paramyosin and myofilin found in the core of the invertebrate thick filament (29
30
31)
are shedding light on how thick filament lengths are determined. The mechanism of thin filament length regulation is more obscure in invertebrate muscles, despite the detection of nebulin-like proteins in several invertebrate muscles (32)
. In Drosophila, sanpodo, a homologue of the actin capping protein, tropomodulin, has been implicated in regulating tropomyosin-containing thin filament length during myofibril development (33)
.
The symmetry and perforation of the tymbal Z-bands have significant mechanical implications. Structurally, Z-bands of invertebrates present a different lattice arrangement, favoring a hexagonal pattern in most fibrillar muscles, and are in contrast to the tetragonal pattern in Z-bands of vertebrates (13)
. The tightly woven protein filaments in vertebrate muscle Z-bands create a physical barrier that prevents the passage of thick filaments through the Z-band. Supercontraction of hyperactivated vertebrate muscle therefore causes the crushing of the tips of thick filaments at the Z-bands in vertebrates (K. Wang, unpublished observations). Additionally, the tetragonal symmetry of the Z-bands and the associated thin filaments present a nagging question of how the tetragonal thin filaments slide into a hexagonal array of thick filaments without twisting and turning (34)
. In invertebrates, patterns of the Z-lattice vary widely, ranging from a near crystalline array in flight muscle to a highly disorganized array in some visceral and tubular muscles (13)
. The tymbal muscle showed a highly ordered Z-band hexagonal lattice with perforations that may allow the passage of thick filaments with identical symmetry and lattice spacings through the Z-band. Supercontraction in tymbal muscle, on induction by stimulation with caffeine, indeed caused the penentration of thick filaments through the Z-bands. Although it is not known whether supercontraction ensues in the normal functioning of the tymbal muscle, the intriguing possibility exists that this may be a mechanism to extend the force generating potential to a much shorter sarcomere length, by allowing the distal segment of thick filaments to interact and generate force with the thin filaments of the adjacent sarcomere (35)
. This would in turn enhance a broader range of travel of tymbals, for a given length of muscle fiber, and may subsequently amplify sound production.
The width of tymbal muscle Z-bands presents an additional example that challenges the generality of the reported relationship of Z-bandwidth with the speed of muscle. Correlative studies of various species of vertebrate striated muscle have led to the conclusion that the width of Z-bands is approximately inversely proportional to the intrinsic contraction speed, being narrowest for very fast muscle fibers and broadest for slow tonic ones (28
, 36)
. Whether such a relationship holds true for invertebrate muscles remains open. An obvious exception to this relationship is the superfast sonic muscle of the type 1 male midshipman, where Z-band width measures 1.2 µm, a width 20 times greater than those seen in typical vertebrate skeletal muscle (3
, 4)
and yet contracts at 100 Hz (37)
. In cicadas, Z-bands in the tymbal muscle were also wider (180 nm) than those in vertebrate muscles and vibrate at 50 Hz (5
,10)
. Thus, this relationship that was proposed based on a narrow range of Z-band widths from 30–120 nm of vertebrate muscles (38
, 39)
may require revisiting. The potential roles of Z-bands in enhancing the force transmission, the storing and releasing of elastic energy, the tensile strength, as well as the scaffolding capacity signaling proteins (40
, 41)
that are being studied in vertebrate muscle are increasingly attractive for invertebrate muscle as well.
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ACKNOWLEDGMENTS |
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Received for publication March 24, 2006. Accepted for publication May 15, 2006.
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