Diverse and complex muscle spindle afferent firing properties emerge from multiscale muscle mechanics

Abstract

1 Sensory information about the body's mechanical interactions with the environment are critical for neural 2 control of movement. Muscle spindle sensory neurons richly innervate muscles in vertebrates; their firing 3 patterns as muscles stretch have been well-characterized experimentally, but have not been fully explained 4 mechanistically. Here, we show that a diverse range of muscle spindle firing characteristics are emergent 5 from first principles of muscle contractile mechanics. We develop a mechanistic muscle spindle model that 6 predicts well-known phenomena such as variations in muscle spindle sensitivity due to prior movement 7 history and nonlinear scaling with muscle stretch velocity. The model further predicts how central 8 commands to muscle spindles-fusimotor drive-alters their firing responses, and shows how seemingly 9 paradoxical muscle spindle firing during voluntary force production in humans can arise. Our multiscale 10 muscle spindle model provides a unifying biophysical framework that may broadly explain and predict 11 movement-related sensory signals in health and disease. 13Precise movements depend on sensory information from throughout the body. Vertebrates have specialized 14 sensors called muscle spindles that are widely distributed throughout skeletal muscles, providing critical 15 information for all movements-from basic knee-jerk reflexes to playing musical instruments. Muscle 16 spindles are all the more remarkable because they are not simply passive sensors: muscle spindles contain 17 specialized muscle fibers that, when activated by central motor commands, alter the sensory information 18 received by the nervous system. Despite decades of research, we still lack a mechanistic framework capable 19 of explaining and predicting how movement-related biomechanical signals are transformed into the broad 20 diversity of muscle spindle firing patterns observed experimentally, particularly in naturalistic behaviors. 21Developing a mechanistic framework for understanding how muscle spindle organs generate the complex 22 sensory signals observed during movement will be critical for understanding not only the functional role of 23 muscle spindles as proprioceptive sensors, but also neural control of movement and how it is affected by 24 neurological disorders. 25We recently demonstrated that a combination of muscle fiber force and yank, i.e. the first time 26 derivative of force 1 , matches the profile of muscle spindle firing throughout the stretch of a relaxed 27 muscle 2,3 . The role of muscle mechanics and force in muscle spindle function has long been discussed 4,5 , 28 but not integrated into a mechanistic framework. We first used a phenomenological approach to 29 demonstrate the parallel dependence of muscle spindle firing and muscle mechanics on prior movement of 30 the muscle. Muscle spindle firing rates, together with muscle force and yank are high when the muscle is 31 stretched after being held at a constant length, and lower if the muscle was moving prior to stretch 6 . In both ...

Skeletal muscle function underpins muscle spindle abundance

“…Skeletal muscle is functionally diverse, simultaneously operating as a motor to drive locomotion while also as a sensory organ to detect limb positions and modulate posture [1]. Activation of extrafusal muscle fibres and changes in fascial length enable muscles to produce power.…”

“…Activation of extrafusal muscle fibres and changes in fascial length enable muscles to produce power. The coordination of activation and fibre length change across multiple muscle groups is a complex process, where the successful execution of a motor command relies on constant proprioceptive feedback to modulate central drivers of movement [1,2]. These proprioceptive signals are detected through two peripherally located sensory apparatuses: muscle spindles and Golgi tendon organs (GTOs) [3].…”

Abnormal center of mass control during balance: a new biomarker of falls in people with Parkinson’s disease

“…Importantly, these signals could not have originated within TA, which is shortened during the initial portion of this perturbation. Instead, they likely arise from muscle spindle proprioceptive signals 2,22 within the MG and within other muscles within the limbs -and potentially torso and other areas -that are stretched due to the perturbations and which exhibit similar feedback-mediated responses.…”

“…For example, PD is associated with additional coactivation during walking, but the presence of coactivation is weakly related to gait quality. 23 The sensorimotor processing underlying motor signals to antagonist muscles during balance are not understood, but may arise from similar CoM sensorimotor feedback signals driving agonist muscles. An antagonist activation pathway based on CoM feedback analogous to that of agonist muscles seems plausible, as antagonist muscles are frequently activated during motor tasks in uncertain environments.…”

“…For example, PD is associated with additional coactivation during walking, but the presence of coactivation is weakly related to gait quality. 23…”