A thixotropic effect in contracting rabbit psoas muscle: prior movement reduces the initial tension response to stretch.

Striated muscles in vivo are frequently subjected to repeated patterns of lengthening and shortening movements. In humans, for example, skeletal muscles in the limbs undergo cyclic changes in length during locomotion while the ventricular walls of the beating heart stretch and shorten approximately once per second throughout life. A thorough knowledge of the behaviour of striated muscles during repeated length changes is thus important for a complete understanding of muscle function in physiologically relevant conditions. Previous studies have shown that the mechanical properties of relaxed skeletal muscles are dramatically influenced by the history of movement. Specifically, the apparent stiffness of the initial phase of the tension response is reduced in the second of two stretches. This phenomenon was first described by Denny-Brown in 1929 and has since been confirmed in both whole body (Lakie et al. 1984) and isolated muscle (Lannergren, 1971; Lakie & Robson, 1990) experiments. The precise mechanism underlying this history-dependent behaviour remains unclear. Several reports (Herbst, 1976; Lakie & Robson, 1988) have suggested that the myofilaments of relaxed intact muscles are linked by a small number of slowly cycling cross-bridges and that the decreased stiffness reflects a temporary reduction in the number of attached cross-bridges following movement. Recent simulations (Campbell & Lakie, 1998) support this hypothesis but the theory remains controversial (Lannergren, 1971; Hufschmidt & Schwaller, 1987; reviewed by Proske & Morgan, 1999). The present experiments were designed to investigate whether contracting skeletal muscles also possess history-dependent mechanical properties. We subjected permeabilised skeletal muscle preparations (in which the activity of the contractile apparatus could be varied by immersing the fibres in solutions with different free Ca2+ concentrations) to repeated length changes imposed under sarcomere length control and measured the resulting tension responses. Our results reveal qualitatively similar history-dependent behaviour to that previously observed in relaxed intact muscles; two identical length changes produce different tension responses in contracting skeletal muscles if they are separated by intervals of less than a few seconds. Following the nomenclature introduced to muscle physiology by Buchthal & Kaiser (1951), we have chosen to describe this history-dependent reduction in the muscle's stiffness as a thixotropic effect. Thixotropy is a term used in the field of rheology to describe an isothermal system in which there is a ‘decrease in the apparent viscosity under shear stress, followed by a gradual recovery when the stress is removed’ (Harris, 1977). This strict definition has unfortunate implications in the present context of muscle mechanics since it might suggest that the non-linear tension response of contracting skeletal muscle arises from a passive viscosity within the contractile apparatus. We do not believe this to be the case. Our results would best be described by a term which defines a history-dependent stiffness but unfortunately, at least as far as we are aware, no such word exists. Rather than inventing a new term, we have chosen to apply Buchthal & Kaiser's original term thixotropy to maintain consistency with previous reports in the physiological literature. However, we wish to stress that in the present work we intend thixotropy to describe a time-dependent reduction in a muscle's resistance to stretch following movement, irrespective of whether the resistance is entirely proportional to velocity. Brief accounts of preliminary experiments and simulations have previously been presented to the Biophysical Society (Campbell & Moss, 1999, 2000).