Thixotropy in skeletal muscle and in muscle spindles: A review

Abstract

UWE PROSKE,t DAVID L. MORGAN* and J. EDMUND GREGORY'} *Department of Electrical and Computer Systems Engineering, Monash University, Clayton, Victoria, 3168, Australia ~ Department of Physiology, Monash University, Clayton, Victoria, 3168, Australia CONTENTS 1. Extrafusal muscle 1.1. Introduction 1.2. Mechanism 1.2.1. Basic observation 1.2.2. The role of calcium 1.2.3. Relation to 'weakly attached state' 1.3. Slack in muscle fibers 1.4. Measurements using intact joints 1.5. Conclusions 2. Thixotropy in muscle spindles 2.1. Historical observations 2.2. Mechanism 2.3. Stretch excitation 2.4. Two forms of muscle conditioning 2.5. Time-course 2.6. Spindles and extrafusal thixotropy 2.7. Fusimotor after-effects 2.8. Human spindles 2.9. Thixotropy as a tool for studying spindle mechanisms 2.9.1. Two kinds of spindles 2.9.2. Selective conditioning with single fusimotor fibers 2.9.3. Secondary endings 2.10. Thixotropy and reflex action 2.11. Proprioception 2.12. Conclusions References 705 705 705 705 706 706 706 7O7 708 708 709 710 710 711 712 712 712 713 713 713 714 716 716 718 718 719 1. EXTRAFUSAL MUSCLE 1.1. INTRODUCTION The term thixotropy comes from the Greek words 'thixis' meaning touch and 'tropos' meaning trans- formation. It is applied to substances which change their physical properties as a result of being mechan- ically shaken. More formally, it applies to materials which behave as solids below a certain applied shear force and as fluids at higher forces. It is commonly applied to polymeric molecules which on mechanical agitation detach weak bonds. In biology it was first used by Peterfi (1927) who noted a reduction in viscosity of the cytoplasm of sea urchin eggs follow- ing disturbance with a needle. Thixotropy has been described for suspensions of red blood cell aggregates and for synovial fluid (quoted from Lackie et al., 1984). The term thixotropy has been used in striated muscle to describe the dry friction-like behavior of passive muscle to movement, as distinct from its elastic (length dependent) or viscous (velocity depen- dent) behavior. Thus the element described by Hill (1968) as a short range elastic component (SREC) could be classified as thixotropic, in that the tension did not vary directly with length or velocity, but increased with length up to a limit of about 0.2% of muscle length and then remained constant for the remainder of the movement. Manifestations of the same phenomenon, but ap- plied to whole animals, have also been called thixotropy. The term is used to describe the resistance of a muscle or limb to imposed motion which is high for small movements but less for larger movements. Transformation from the high resistance to the low resistance state is possible by giving a brief large amplitude 'stirring' movement. 1.2. MECHANISM 1.2.1. Basic observation The basic observations on skeletal muscle and the resulting hypothesis are both due to Hill (1968). He showed that the tension response of passive frog muscle to a slow stretch was biphasic, with an initial, stiff, elastic region at the onset of the movement, which gave way to a nearly constant tension due to motion over the remainder of the stretch. The prop- erty of the muscle responsible for this response was 705