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

Abstract

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...

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

“…Although only two catfish species were studied quantitatively, it is concluded that differences in the contraction frequency cannot be explained based on differences in the fine structural design of muscle fibers. Besides differences in the morphology of sonic organs, other differences between both families probably exist in the contraction kinetics of sonic muscle fibers, for example differences in speeds of calcium transients, crossbridge detachment rates, and probably kinetic off-rates of calcium from troponin (Rome et al, 1996).…”

“…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). Feher et al (1998) relate the extensive sarcoplasmic reticulum to calcium capacity, which allows the muscle to keep contracting even though calcium is not completely recycled.…”

High-speed video analysis of wing-snapping in two manakin clades(Pipridae: Aves)

“…These results thus provide independent support for the premise that 'sonic muscles', those used in sound production, are among the fastest vertebrate muscles known. Specifically, the shaker muscles of a rattlesnake's rattle contract at ~90·Hz, several times faster than more normal vertebrate locomotory muscles, which contract at 20-30·Hz (Rome et al, 1996). The piprids described herein can employ similarly rapid wing cycles of 75·Hz (P. mentalis, rub-snap) and 80·Hz (Manacus, snort), at least doubling the contraction rates used in normal flight.…”

Novel vocal repertoire and paired swimbladders of the three-spined toadfish,Batrachomoeus trispinosus: insights into the diversity of the Batrachoididae

“…Vocalizations are produced by the rapid contraction of paired striated muscles attached to the walls of the swimbladder (Fine et al, 2001;Fine et al, 2002), with ultrastructural traits divergent from trunk skeletal muscles (e.g. Bass and Marchaterre, 1989;Fawcett and Revel, 1961), that are adapted to contraction frequencies which are among the fastest of vertebrate skeletal muscles (Rome, 2006;Rome et al, 1996;Skoglund, 1961).…”