A model of the mammalian muscle spindle

Abstract

Proprioceptors such as muscle spindles and Golgi tendon organs provide the central nervous system with sensory feedback for motor control and kinesthesia. It is difficult to record afferent activity from such receptors during motor behavior, so theories of motor control usually depend on implicit or explicit assumptions about such activity. The muscle spindle is the most important proprioceptor, playing a dominant role in kinesthesia and in reflexive adjustments to perturbations. Each muscle spindle accurately senses and encodes length and velocity information of the extrafusal muscle fibers over a wide range of movements despite the relatively restricted dynamic range of firing rates for action potentials. It does this by shifting the relative importance and sensitivity to length and velocity in response to specialized fusimotor efferents (gamma motoneurons), at the cost of complicating the interpretation of their signals by the nervous system. We have constructed a physiologically realistic model of the spindle that is composed of mathematical elements closely related to the anatomical components found in the biological spindle. The spindle model consists of three nonlinear intrafusal fiber models: bag1, bag2 and chain. The bag1 fiber model is the only one that receives dynamic fusimotor control and is primarily responsible for velocity sensitivity of the spindle. The bag2 and chain receive ?static fusimotor control and contribute mainly to length sensitivity. All three fiber types give rise to primary afferent activity, while only bag2 and chain to secondary afferent activity. In the case of the primary afferent, the model incorporates the experimentally observed effect of partial occlusion, where primary afferent activity results from a competition between two impulse generator sites, one located on the bag1 and other on bag2 and chain fibers. When both sites are active, the dominant generator wins and suppresses all activity in the weaker generator by resetting its spike generator. While that results in total occlusion, the mechanism responsible for partial occlusion observed in the case of primary afferent is believed to include electrotonic current spread between the suppressed and dominant generator, resulting in increased impulse generation at the dominant site. The model also incorporates the appropriate temporal properties of three types of intrafusal fibers during static or dynamic fusimotor stimulation. The advantage of including these properties is demonstrated by comparing model simulations with and without these properties to data from recently published experiments in which both fusimotor efferent and spindle afferent activity were recorded simultaneously during decerebrate locomotion in the cat (Taylor et al., J Physiol 529.3: 825-836, 2000). We have inverted the spindle model in order to use it as a tool to better understand fusimotor control in natural tasks. By supplying the inverted model with records of afferent activity and kinematics during natural tasks, the inverted model can be used to infer the underlying fusimotor drive. Once the principles of fusimotor control are understood, it should be possible to apply the spindle model to predict more accurately the activity of spindle afferents and their role in control of motor tasks.