The nature of the phasic and the tonic responses of the anterior byssal retractor muscle of Mytilus

Abstract

Since Winton (1934) first introduced the anterior byssal retractor muscle (ABRM) of Mytilus into muscle physiology, various workers have found that it provides a particularly suitable preparation for use in studying the physiology of lamellibranch muscle. Its virtues are, first, that it is made up of a homogeneous population of muscle fibres, each of which probably extends from one end of the muscle to the other; secondly, that it can easily be isolated intact for experiments in vitro. Various types of stimuli will make the muscle contract, but the time course of the relaxation that follows depends on the nature of the stimulus. This has provided a convenient basis for dividing the responses of the ABRM into two general categories; 'phasic' responses, in which the relaxation is complete within about 30 sec, and 'tonic' responses, in which the corresponding degree of relaxation may take from several minutes to several hours. In general, acetylcholine and direct-current stimulation produce tonic responses, and most other forms of electrical stimuli produce phasic responses.In the interpretations that have been given of the behaviour of the ABRM during phasic and tonic responses there has been an exacerbation of the traditional controversy that exists over the nature of the tonic contraction produced by many lamellibranch muscles. The controversy arose at the beginning of the century when there was disagreement over the suggestions made by certain workers (for references, see Griitzner, 1904;Marceau, 1909) that this type of muscle contains a special (passive) mechanism which enables it to maintain contractions economically for long periods. The concept of a 'catch' mechanism was first considered in detail by Griitzner (1904), and it was greatly strengthened by von Uexkiill's (1912) classical experiments on the adductor mechanism of Pecten. However, other workers rejected the idea that a special mechanism is necessary for the maintenance of a tonic contraction. It has been argued that in view of the intrinsic slowness of this type of muscle,

Invertebrate muscles: Thin and thick filament structure; molecular basis of contraction and its regulation, catch and asynchronous muscle

“…The work at the beginning of this third period used recognizably modern techniques and was initially devoted to well defining the contractile responses of the muscles. This work showed that the muscles indeed produce, as a function of stimulation protocol, rapidly or very slowly relaxing contractions; that ACh and serotonin are present in the nerves innervating the muscle; that ACh application induces very slowly relaxing contractions; that serotonin application causes these slow relaxations to become rapid but does not induce contractions when applied alone; and that the nerves innervating the muscle contain both substances (Lowy, 1953(Lowy, , 1954Twarog, 1954Twarog, , 1967aTwarog, , 1968Bandmann and Reichel, 1954;Hoyle and Lowy, 1956;Welsh, 1957;Holgate and Cambridge, 1958;Abbott and Lowy, 1958a,b;Jewell, 1959;Takahashi, 1960;Twarog, 1960a,b;Rudwick, 1961;Baguet et al, 1962;Millman, 1964;Baguet and Gillis, 1964;Bullard, 1967;Hidaka et al, 1967;Leenders, 1967;Salánki and Hiripi, 1970;Twarog and Cole, 1972;Lowy and Vibert, 1972;York and Twarog, 1973;Nagahama et al, 1974;Sugi and Suzuki, 1978;Satchell and Twarog, 1978;Muneoka et al, 1978aMuneoka et al, -c, 1979. The muscle's ability to produce both phasic and tonic contractions thus resulted from it having two innervations, one cholinergic and one serotonergic, with the differing stimulation protocols stimulating either only the cholinergic pathway or stimulating both pathways simultaneously.…”

“…By this time how nerve activity induces muscle contraction was beginning to be understood, which gave rise to the first of the controversies in this field: were the slow relaxations due to continuous activity in the innervating pathways (the 'tetanic' hypothesis), as had been shown to be the basis of a sustained contraction in isolated crustacean limbs (Barnes, 1930), or to a sustained change intrinsic to the muscle itself (the 'catch' hypothesis) (Lowy, 1953;Jewell, 1959). A series of papers before 1960 showed that in the animal and in some in vitro preparations infrequent electrical events were indeed present in the muscle during catch, supporting the tetanic idea (Lowy, 1954(Lowy, , 1955Hoyle and Lowy, 1956;Abbott and Lowy, 1958a,b).…”

“…That catch is not due to continuous high actomyosin activation was further supported by work showing that 1) catch expends much less energy than active shortening (Parnas, 1910;Brecht et al, 1955;Nauss and Davies, 1966;Baguet andGillis, 1967, 1968;Yernaux and Baguet, 1971;Schumacher, 1972;Sugi and Suzuki, 1978;Ebberink et al, 1979;Zange et al, 1989;Ishii et al, 1991), 2) when catch muscles are appropriately vibrated catch is abolished but force is not regenerated when the vibration ends (Ljung and Hallgren, 1975), and 3) the ability of muscles to shorten and then re-develop tension when loading force is decreased (quick release experiments) is much reduced after catch has developed (Jewell, 1959;Johnson and Twarog, 1960;Lowy et al, 1964;Baguet and Marchand-Dumont, 1975). It is precisely this property, that muscles in catch strongly resist being stretched, but do not contract further if their load is decreased, that most distinguishes catch from more commonly observed contractile states, and which is responsible for the fact that, if a piece of wood is inserted between the valves and the animal stimulated to close, when the wood is removed after catch has been induced the shells do not close further (Hoyle, 1983) These observations suggested that catch resulted from a process in the muscle that 'locked' it at whatever length it had when catch ensued.…”

31P-nuclear-magnetic-resonance study of muscles from Mytilus edulis

“…The anterior byssus retractor muscle was dissected according to the procedure described by Jewel1 [6]. 31P-NMR spectra were recorded from freshly excised and resting muscles: for obtaining relaxed muscles, we left them for several hours in aerated sea water.…”

The N-terminal Region of Twitchin Binds Thick and Thin Contractile Filaments

“…In the catch state, intracellular [Ca 2ϩ ] is close to basal concentration (1), and redevelopment of force following unloading of the muscle is absent (2). A hypothesis to explain the long term maintenance of catch force was based on a slowing of cycling of myosin attached to actin when activation waned (see Lowy and Millman (3)).…”