Functional morphology of toadfish sonic muscle fibers: relationship to possible fiber division

Fine, Michael L.; Bernard, Barbara; Harris, Thomas M.

doi:10.1139/z93-318

Cited by 51 publications

(55 citation statements)

References 37 publications

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“…(i) The duration of the calcium transient becomes shorter, which in turn requires more rapid calcium release and reuptake. Ultrastructural and biochemical studies suggest that this is achieved by a large increase in the density of SR calcium pumps (SERCAl isoform), an increased concentration of parvalbumin and a short diffusion distance for Ca2+ (-0.15 gm) in the narrow, lamellar-shaped myofibrils (5,7,21,33). There is also an increase in the density of SR Ca2+ release channels in swimbladder fibers (5) and it has been proposed that the channel isoform in this fiber type, the a-ryanodine receptor, abbreviates the time course of Ca2+ release (34).…”

Section: Resultsmentioning

confidence: 99%

The whistle and the rattle: the design of sound producing muscles.

Rome

Syme

Hollingworth

et al. 1996

Proc. Natl. Acad. Sci. U.S.A.

226

230

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Vertebrate sound producing muscles often operate at frequencies exceeding 100 Hz, making them the fastest vertebrate muscles. Like other vertebrate muscle, these sonic muscles are "synchronous," necessitating that calcium be released and resequestered by the sarcoplasmic reticulum during each contraction cycle. Thus to operate at such high frequencies, vertebrate sonic muscles require extreme adaptations. We have found that to generate the "boatwhistle" mating call , the swimbladder muscle fibers of toadfish have evolved (i) a large and very fast calcium transient, (ii) a fast crossbridge detachment rate, and (iii) probably a fast kinetic off-rate of Ca2+ from troponin. The fi'bers of the shaker muscle of rattlesnakes have independently evolved similar traits, permitting tail rattling at '90 Hz.sients-in fact the largest and fastest ever recorded. However, our results showed that a fast Ca2+ transient alone is not sufficient for high frequency operation. By measuring Vmax, an index of crossbridge detachment rate, and the force-pCa relationship in skinned fibers, a possible index of troponin kinetics, we found that rapid activation and relaxation likely also require a modification of the crossbridge kinetic rate, and probably a modification of the kinetics of Ca2+-troponin binding. In reaching these conclusions, we first compared the above measurements in three fiber types from toadfish, ranging from slow twitch swimming fibers to the superfast twitch swimbladder fibers. We then compared the properties of rattlesnake shaker fibers with those of swimbladder.Skeletal muscle fibers perform a wide range of activities, and different fiber types are accordingly designed to operate at different speeds and frequencies (1). A number of modifications appear to underlie this diversity. For example, in locomotory muscle, compared with slow twitch fibers, fast twitch fibers have a faster myosin with a higher maximum velocity of shortening (Vm,,) (2, 3), a greater content of sarcoplasmic reticulum (SR), and its associated Ca2+ pumps (4, 5), a different isoform of the SR Ca2+ pump (SERCAl in fast versus SERCA2 in slow) (6, 7) and a greater concentration of parvalbumin (a soluble protein that binds both calcium and magnesium) (5, 8). There is also evidence that fast fibers have a briefer myoplasmic free Ca2+ concentration ([Ca2+]) transient (9, 10) and less sensitive force-pCa relationship (11,12).To understand the physiological modifications that underlie very rapid contractions, we have studied two of the fastest vertebrate muscles known. Both of these "sonic" muscles are used to produce sounds at the frequency at which the muscle contracts. The "boatwhistle" mating call of the male toadfish (Opsanus tau) is generated by '200 Hz contractions (25°C) of the muscles encircling the fish's gas-filled swimbladder (13-15). The familiar "rattle" of the venomous western diamondback rattlesnake (Crotalus atrox) is generated by "90 Hz contractions (35°C) of the shaker muscles at the base of the tail (16-19). The operational frequ...

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Section: Resultsmentioning

confidence: 99%

The whistle and the rattle: the design of sound producing muscles.

Rome

Syme

Hollingworth

et al. 1996

Proc. Natl. Acad. Sci. U.S.A.

226

230

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“…A cylinder-like arrangement of myofibrils as found in the "doradoids," where mitochondria are arranged outside and inside but not within the contractile cylinder, appears to be a derived organizational pattern. The fine structural organization of organelles of the doradid Platydoras resembles that of sonic muscles in toadfishes (Bass and Marchaterre, 1989;Fine et al , 1993) and sciaenids (Ono and Poss, 1982). In both nonrelated groups, mitochondria are found outside and within the radially arranged ribbons of myofibrils.…”

Section: Evolutionary Considerationsmentioning

confidence: 93%

“…Josephson and Young (1985) argue that higher myofibril volume is associated with an increase in the muscle force per cross-sectional area and the mechanical power output per gram muscle in cicadas. In addition, Fine et al (1993) observed that muscle fibers were smaller in juvenile toadfish and that their grunts had a significantly lower SPL than those of adults. Both reports are in agreement with observations in catfishes.…”

Section: Fine Structure and Contraction Frequencymentioning

confidence: 95%

“…Contrary to locomotory muscles, drumming muscles possess thin myofibrils and an elaborate development of the sarcoplasmic reticulum (Fawcett and Revel, 1961;Eichelberg, 1977;Ono and Poss, 1981;Bass and Marchaterre, 1989;Fine et al, 1993;Loesser et al, 1997). These features are linked to an unusually rapid calcium cycling necessary for fibers to operate at such high frequencies (Appelt et al, 1991;Rome et al, 1996).…”

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confidence: 99%

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Sound‐generating and ‐detecting motor system in catfish: Design of swimbladder muscles in doradids and pimelodids

Ladich

2001

Anat. Rec.

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Catfishes have evolved a diversity of swimbladder muscles serving in the generation of different sounds and probably other acoustic functions. In order to find out if anatomical and acoustical differences are parallelled by fine structural differences, I examined the sonic muscles of the doradid Platydoras and the pimelodid Pimelodus by gross dissections and ultrastructural methods. In Platydoras, the sound-generating (drumming) muscle (DM) inserts on a dorsal bony plate that vibrates the swimbladder. In pimelodids, the large DM attaches directly on the ventral surface of the swimbladder, whereas the small tensor tripodis muscle (TT) inserts on the rostral surface near the tripus, the most caudal Weberian ossicle. Fibers of all three muscles possess an extensive development of sarcoplasmatic reticulum (SR) in association with very thin myofibrils (MF) but differed widely in their arrangement. In Platydoras, ribbons of MFs are arranged radially around a central core. Mitochondria were found within the core and the peripheral sarcoplasm. Pimelodus does not have a differentiated core and the cross-sectional area of DM-MFs is about 15% larger as determined by stereological measurements. The TT possesses shorter sarcomeres and more mitochondria than DMs, which were primarily found between MFs. This suggests faster contraction properties and greater resistence to fatigue compared with sonic muscles. Data indicate that the higher amount of DM-myofibrils in pimelodids might result in stronger muscle contractions and, presumably, in higher sound intensities. The fine structure of the TT reveals that contractions most likely prevent transmission of swimbladder vibrations to the inner ear via the Weberian ossicles during vocalization.

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“…Sections from a previous study [35,36] were used to measure developmental changes in bladder thickness. Sections came from the sides of the swimbladder, near the middle of the sonic muscle that were embedded in glycol methacrylate, sectioned at 2 mm and stained with haematoxylin and eosin.…”

Section: (B) Development Of Bladder Thicknessmentioning

confidence: 99%

Wall structure and material properties cause viscous damping of swimbladder sounds in the oyster toadfishOpsanus tau

et al. 2016

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Despite rapid damping, fish swimbladders have been modelled as underwater resonant bubbles. Recent data suggest that swimbladders of soundproducing fishes use a forced rather than a resonant response to produce sound. The reason for this discrepancy has not been formally addressed, and we demonstrate, for the first time, that the structure of the swimbladder wall will affect vibratory behaviour. Using the oyster toadfish Opsanus tau, we find regional differences in bladder thickness, directionality of collagen layers (anisotropic bladder wall structure), material properties that differ between circular and longitudinal directions (stress, strain and Young's modulus), high water content (80%) of the bladder wall and a 300-fold increase in the modulus of dried tissue. Therefore, the swimbladder wall is a viscoelastic structure that serves to damp vibrations and impart directionality, preventing the expression of resonance.

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Functional morphology of toadfish sonic muscle fibers: relationship to possible fiber division

Cited by 51 publications

References 37 publications

The whistle and the rattle: the design of sound producing muscles.

The whistle and the rattle: the design of sound producing muscles.

Sound‐generating and ‐detecting motor system in catfish: Design of swimbladder muscles in doradids and pimelodids

Wall structure and material properties cause viscous damping of swimbladder sounds in the oyster toadfishOpsanus tau

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