Diverse and Complex Muscle Spindle Afferent Firing Properties Emerge from Multiscale Muscle Mechanics

Despite decades of research, we lack a mechanistic framework capable of predicting how movement-related signals are transformed into the diversity of muscle spindle afferent firing patterns observed experimentally, particularly in naturalistic behaviors. Here, a biophysical model demonstrates that well-known firing characteristics of mammalian muscle spindle Ia afferents – including movement history dependence, and nonlinear scaling with muscle stretch velocity – emerge from first principles of muscle contractile mechanics. Further, mechanical interactions of the muscle spindle with muscle-tendon dynamics reveal how motor commands to the muscle (alpha drive) versus muscle spindle (gamma drive) can cause highly variable and complex activity during active muscle contraction and muscle stretch that defy simple explanation. Depending on the neuromechanical conditions, the muscle spindle model output appears to ‘encode’ aspects of muscle force, yank, length, stiffness, velocity, and/or acceleration, providing an extendable, multiscale, biophysical framework for understanding and predicting proprioceptive sensory signals in health and disease

Interaction between muscle tone, short-range stiffness and increased sensory feedback gains explains key kinematic features of the pendulum test in spastic cerebral palsy: A simulation study.

The pendulum test is a sensitive clinical assessment of spasticity where the lower leg is dropped from the horizontal position and features of limb motion are recorded. Three key kinematic features are associated with the degree of severity of spasticity in children with cerebral palsy: decreased initial limb excursion, reduced number of limb oscillations, and a non-vertical resting limb angle. While spasticity is attributed to increased velocity-dependent resistance to motion, prior models simulating increased sensorimotor feedback of muscle velocity fail to explain the key pendulum test kinematic outcomes in spastic individuals. Here we hypothesized that increased muscle tone, causing a transient increase in muscle force, i.e. short-range stiffness, could account for reduced first swing excursion and non-vertical resting limb angle. We further hypothesized that hyperreflexia modeled based on muscle fiber force, and not velocity, feedback would be necessary to reduce the number of oscillations because of its interaction with transiently increased muscle force due to short-range stiffness. We simulated the lower leg as a torque-driven single-link pendulum. Muscle tone was modeled as a constant baseline joint torque, short-range stiffness torque was dependent on the level of muscle tone, and delayed sensory feedback torque to simulate reflex activity was based on either muscle velocity or force. Muscle tone and transient short-range stiffness were necessary to simulate decreased initial swing excursion and non-vertical resting leg angle. Moreover, the reduction in the number of oscillations was best reproduced by simulating stretch reflex activity in terms of force, and not velocity, feedback. Varying only baseline muscle torque and reflex gain, we simulated a range of pendulum test kinematics observed across different levels of spasticity. Our model lends insight into physiological mechanisms of spasticity whose contributions can vary on an individual-specific basis, and potentially across different neurological disorders that manifest spasticity as a symptom