Role of cross‐bridge distortion in the small‐signal mechanical dynamics of insect and rabbit striated muscle.

Abstract

SUMMARY1. The mechanism of the active tension response of insect fibrillar muscle to step changes and small oscillations of length was re-investigated, following White's demonstration (1983) that the high relaxed stiffness evidently persists during activation and cannot be neglected as had previously been assumed. White's result makes earlier explanations of the small-signal response untenable; the experimental and theoretical studies described here lead to a new class of explanations at the cross-bridge level.2. The response of an activated muscle to a fast stretch consists of a synchronous tension increase that is followed first by a rapid decay oftension and then by a delayed rise ('stretch activation'). It was shown in glycerinated fibre preparations from the water bug and the bumblebee that subtraction of the relaxed tension response from the active response results in a prominent undershoot of the tension level preceding the step, before the delayed rise of tension.3. The responses ofthe same fibres to sinusoidal oscillations, in the frequency range 1-150 Hz, showed an equivalent behaviour, with the active locus circling the relaxed locus in a Nyquist plot, as described by Machin & Pringle (1960). 4. Stiffness was determined during the tension response to a large step (of 1 %) by recording the immediate change of tension to a small test step (0-2 %), applied at various times after the conditioning step. In the majority of preparations stiffness remained constant or increased during the undershoot of tension. 5.Step and sinusoidal responses with the above features cannot be explained at all by an active component resembling a simple exponential delay. We show, however, that such features are predicted if certain small-signal effects of cross-bridge distortion (previously and erroneously assumed negligible in insect flight muscle for the small-signal case) are incorporated in models of the cross-bridge cycle. Two alternative hypotheses for the effects ofdistortion are examined: (i) distortion-induced detachments and (ii) distortion-modulated transitions among multiple attached states (Huxley & Simmons, 1971). For the first we also show that the results do not differ qualitatively whether one assumes strain, interfilament displacement or 'bridge recruitment' as the physical correlate of stretch activation.

The elasticity of relaxed insect fibrillar flight muscle.

“…Abbott, 1973;Steiger & Abbott, 1981). In the following paper (Thorson & White, 1983) we discuss the implications of this conclusion.…”

“…On our singlefilaments model these values are equivalent to C-filament stiffnesses of 2-8 pN nm-1 and 13-1 pN nm-1 respectively. In the following paper (Thorson & White, 1983) we have used a figure of 10 pN nm-' for modelling purposes.…”

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

“…The strain sensor hypotheses argues that stress induced changes in thick or thin filament structure or regulatory molecule conformation (a molecular sensor) alters actomyosin attachment numbers or dynamics {Abbott, 1972 5059 /id; Chaplain, 1968 32694 /id;Chaplain, 1968 37435 /id;Granzier, 1993Granzier, 1360Güth, 1981 33259 /id;Pringle, 1978 35095 /id;Smith, 1991Smith, 2354Thomas, 1996 36667 /id;Thorson, 1969 7037 /id;Thorson, 1983 303 /id}. Because it is likely that sarcomere strain is signaled by the thick filaments (see below), and because cross-linking the myosin heads results in oscillatory power production in vertebrate myofibrils (Tawada and Kawai, 1990), a first speculation might be that strain directly alters myosin activity.…”

“…The difference between asynchronous and 'normal' muscle may thus be one of degree rather than kind. In particular, many actomyosin models predict stretch activation and oscillatory behavior for certain ranges of parameter values {Chaplain, 1975 5398 /id; Cheung, 1983 37501 /id;Guo, 2002 36662 /id;Julian, 1969 37415 /id;Jülicher, 1997 37272 /id;Sicilia, 1991 23522 /id;Smith, 1991Smith, 2354Steiger, 1981 37497 /id;Thomas, 1998 36664 /id;Thorson, 1969 7037 /id;Vilfan, 2003Vilfan, 2005 36680 /id}. Several of these models require high stiffness for oscillation {Julian, 1969 37415 /id; Sicilia, 1991 23522 /id;Smith, 1991Smith, 2354Thorson, 1983 303 /id}, and asynchronous muscles are extremely stiff (Machin and Pringle, 1959;Pringle, 1974;White, 1983;Peckham et al, 1990;Granzier and Wang, 1993;Josephson and Ellington, 1997;Josephson, 1997;Hao et al, 2004). This stiffness is appropriate both as a part of a high frequency resonator system and for coupling length changes to changes in force production.…”

Myosin light chain-2 mutation affects flight, wing beat frequency, and indirect flight muscle contraction kinetics in Drosophila.

“…In particular, we focused on that part of the active response that corresponds to the phenomenon of stretch induced delayed tension rise, generally referred to as "stretch activation" Stretch activation, common to many types of muscle, is responsible for powering the oscillatory wing movement in insects (Jewell and Ruegg, 1966;Pringle, 1978). This effect can be studied by examining force responses to sinusoidal length perturbations (oscillatory changes in fiber length) applied at different frequencies (Kawai and Brandt, 1980;Thorson and White, 1983). A useful parameter that combines both force and length information is muscle stiffness.…”