The role of static and dynamic fusimotor activity during locomotion

In mammals, two basic types of motoneurone (α and γ) are activated during movement. A lot is known about the activity patterns, control and function of α-motoneurones since direct effects are produced on muscle that are easy to record (e.g. EMG). In contrast, even the basic rules that govern the activity of the γ (fusimotor) system are not fully understood, due largely to the complete lack of direct recordings from identified γ-efferents, for technical reasons, in intact animals. These neurones exert their effects indirectly via the muscle spindle, a stretch receptor that makes important contributions to proprioception and, reflexly, to muscle activity.

Through the two types of functionally distinct γ-efferent (static and dynamic), the CNS is capable of powerfully influencing muscle spindle feedback during normal movement (Prochazka, 1996). Spindle afferent recordings from man indicate that the α and γ systems are generally activated together (α-γ coactivation) while there is strong evidence for α-γ independence in animals. This apparent conflict might, however, simply reflect the different ranges of movement that have been studied.

A major, unresolved problem in the fusimotor system concerns the nature of the γ drive to different muscles during the same movement. Does it vary in timing or degree? Is the balance between the two γ types altered? What are the governing rules and functional significance? In this context, animal locomotion is currently the best understood behaviour with recordings available from spindle afferents and, in reduced preparations, γ-efferents. The paper by Taylor et al. in this issue of The Journal of Physiology introduces an elegantly simple method to the field. In these experiments multiple single spindle afferents were recorded from dorsal root filaments during locomotion in a decerebrate cat preparation. Afferents from the medial gastrocnemius (MG) and tibialis anterior (TA) muscles, antagonists at the ankle, were studied simultaneously and the accompanying joint movements recorded. Subsequently the ankle joint signal was replayed through a servo mechanism to reproduce muscle length changes passively, after suppression of α and γ activity using barbiturate anaesthesia. The essential feature of the method lies in the subtraction of spindle discharge during the locomotor and passive states to produce a difference signal that can be interpreted simply in terms of important features of the γ drive to the parent muscle. A potential complication may arise, however, where γ action alters spindle rate and sensitivity together.

The principal results indicate that both static and dynamic γ-motoneurones are active during locomotion in MG and TA. The pattern of dynamic γ firing could not be deduced but static activity to these muscles showed a significant phasic component that could be related to their length changes. This feature is discussed in terms of the ‘temporal template’ hypothesis of fusimotor control. Differences in the timing and profile of static γ drive to MG and TA were, however, apparent (cf. Figs 4A and 9D in Taylor etal., this issue). Static action in MG was phase advanced compared with TA. Furthermore, MG appears to receive a stronger tonic, but weaker phasic, static drive during locomotion than its antagonist. These observations are similar to those reported previously for ankle flexor and extensor muscles using different experimental approaches (Taylor et al. 1985; Murphy & Hammond, 1993). The paper by Taylor et al. (this issue) therefore adds to the growing body of evidence that fusimotor activity during locomotion may vary in different muscles (Cabelguen, 1981; Bessou et al. 1990; Murphy & Hammond, 1993).

The functional significance of such muscle-specific γ drive, in terms of the ‘dual’ role of spindles in proprioception and motor control, is still unresolved and will require more data, from different muscles in a range of tasks, to be fully appreciated. The chief importance of the report by Taylor and colleagues lies in the clarity of illustration of the effect of γ firing on muscle spindle afferents using a simple method. Suitably adapted, this approach should prove useful, with both reduced preparations and intact animals, for gaining new insights into the rules that govern the fusimotor system during posture and movement, and how these become disturbed in pathological conditions.