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

Abstract

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.

Computational Modeling: Human Dynamic Model

“…Several possibilities were debated at the Neural Control of Movement conference in 2013 without definitive results. We have emphasized that the motor cortex communicates a coded kinematic plan together with stiffness settings that play an essential role in shaping the dynamics in muscle spindles (Blum et al, 2020).…”

Abnormal center of mass feedback responses during balance: A potential biomarker of falls in Parkinson’s disease

“…Importantly, these signals could not have originated within TA, which is slack during the initial portion of this perturbation. Instead, they likely arise from muscle spindle proprioceptive signals [2,52] 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.…”

Disentangling acceleration-, velocity-, and duration-dependency of the short- and medium-latency stretch reflexes in the ankle plantarflexors

“…13393724) (16,17). Therefore, the muscle spindle model ( 26) was replaced with a multiscale muscle mechanics model in which this burst does emerge (19).…”

“…Similarly, studies on muscle spindle firing dynamics are subject to the same interdependence. For example, Blum et al (19) observed a relationship of the Ia afferent response's dynamic index with stretch velocity and initial burst with stretch acceleration. However, the simulated stretch velocity and acceleration were varied with a perfect correlation, thus the observed relations cannot conclusively be linked to either velocity or acceleration.…”

“…To disentangle the perturbation parameters under investigation, 49 unique perturbation profiles are used. In addition, a biophysical simulation model of the muscle spindle Ia afferents (19) coupled to a motoneuron pool (20) was implemented. This simulation model was used to corroborate the experimental findings, investigate stretch reflex dependencies across an extended set of perturbation parameters and gain a physiological understanding of the observed dependencies.…”