Muscle sensors and their (controversial) role
For about 100 years, since the time of the famous physiologist Sherrington and his many colleagues (e.g., Sherrington, 1910; Liddel and Sherrington, 1924), there has been an evolving debate on the role of reflexes and of muscle sensors in motor control. Indeed, for much of this century the field of motor control was intimately tied to the concept of reflexes (for an interesting historical perspective, see Granit 1975 or Matthews 1981). Reflexes can be elicited by many modes of sensory information, including temperature and pressure sensors just below the skin, within joint capsules and ligaments, and within muscles and tendon.
Despite a remarkable amount of research activity, our knowledge of how sensory information from sensors such as muscle spindles and Golgi tendon organs has remained illusive (Loeb 1984).
Several types of sensors are embedded within musculotendon tissue
The figure below provides an idealized view of the structural arrangement of the muscle spindles and Golgi tendon organs. All of the sensors essentially measure local tissue strain, and given that this local tissue is passive and somewhat spring-like, to a first approximation the sensors work like strain gages to (indirectly) estimate force. While the relative density of sensors within muscle tissue does vary (e.g., higher density for neck and hand muscles), the bottom line is that muscles are embedded with sensors.
For the Golgi tendon organs, due to the series arrangement, local strain would appear to be associated with muscle force, and to a reasonably good approximation this is indeed the case.
Simplified conceptual view of the key muscle structures: the muscle spindles are located structurally in parallel with the main (extrafusal) muscle fibers (driven by a MNs of various sizes, with idealized slow fatigue-resistant SR and fast fatiguing FF fibers shown here), while the Golgi tendon organs are structurally in series. Here idealized gdynamic and gstatic drives are displayed; in reality there are multiple types of both nuclear chain and bag fibers, with chain fibers receiving gstaticMN drive, and nuclear bag fibers receiving both types. The two classic types of muscle spindle afferents (SNs) are the secondary (group II) and primary (group 1a) sensory afferent endings, which tend to wrap around the fiber and measure local strain. While each type of intrafusal fiber may be innervated by both II and 1a fibers, in general it is useful to associate secondary afferents with chain fibers and primary afferents with bag fibers. Golgi tendon organ sensors (1b SN) essentially measure local strain in tendon near muscle-tendon junctions.
For the muscle spindles, the situation is quite a bit for involved. The traditional assumption is that the primary 1a afferents measure mostly velocity and the secondary II afferents positione. This is based primarily on various length perturbation studies in which the neural drive is constant, and the experiment involves either an isovelocity ramp (from one steady length to another) or a small sinusoidal oscillation.
For ramp-and-hold experiments, after an initial high-frequency transient, sensory action potentials are then reasonably well correlated to weighted linear sum of slightly smoothed length and velocity components. Furthermore, it is known that with increasing gstatic MN activation, the bias firing rate of the sensors (especially secondary) is increased, while with gdynamic MN activity, the dynamic sensitivity is increased (especially for 1a sensors). This suggests that the g drive just modulates the gain and a bias position, and that the process of sensing stretch and encoding this into action potentials is relatively linear.
However, it is not quite this simple – the overall response for a range of stretch is highly nonlinear even when the g drive is constant: there is a local region of high sensitivity to initial stretch which is followed by considerably less sensitivity, and additionally there is asymmetry between lengthening and shortening. This behavior can be conceptually captured by assuming that the sensing element is in series with intrafusal muscle contractile tissue that includes the muscle apparatus mentioned earlier – cross bridges, actin binding sites, etc. Measuring the actual force in these small muscle spindle units has proved quite challenging. Let’s assume that the spindle afferents measure stretch in what is essentially a SE-like element in series with the intrafusal contractile tissue, as in the figure, and that the “sticky” actomyosin bonds initially stretch but don’t yield and then tend to follow conventional shortening and lengthening muscle behavior as for a typical extrafusal muscle). One would then anticipate an initially high force (and thus strain) across the sensing region since the cross bridges initially “hold their ground,” followed by force levels that are consistent with transient behavior of a dynamic subsystem that is somewhat dominated by the CE force-velocity behavior for the intrafusal fibers. That’s about what we see. Thus spindle behavior is linked to intrafusal muscle mechanics as well as transducer-encoder dynamics, and its nonlinear behavior is likely more attributed to intrafusal muscle mechanics than to sensor dynamics.