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.
Digital Object Identifier (DOI)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01 HD90642): Kenneth S Campbell, Timothy C Cope, Lena H Ting
National Cancer Institute (R01 CA221363): Timothy C Cope
National Institute of Neurological Disorders and Stroke (F31 NS093855): Kyle P Blum
Government of Canada (BPF-156622): Brian C Horslen
Code has been made available on GitHub: https://github.com/kylepblum/MechanisticSpindleManuscript (copy archived at https://archive.softwareheritage.org/swh:1:rev:da0ed89078a948167b4e2b511480787ddb681892/). Data have been made available on Dryad: https://doi.org/10.5061/dryad.vdncjsxsw.
The following data sets were generated.
Blum KP, Campbell KS, Horslen BC, Nardelli P, Housley SN, Cope TC, Ting LH (2020) Dryad Digital Repository Data from: Diverse and complex muscle spindle afferent firing properties emerge from multiscale muscle mechanics. https://doi.org/10.5061/dryad.vdncjsxsw
Blum, Kyle P.; Campbell, Kenneth S.; Horslen, Brian C.; Nardelli, Paul; Housley, Stephen N.; Cope, Timothy C.; and Ting, Lena H., "Diverse and Complex Muscle Spindle Afferent Firing Properties Emerge from Multiscale Muscle Mechanics" (2020). Physiology Faculty Publications. 172.
Supplementary file 1: Constant parameters used in both dynamic and static intrafusal muscle fiber models. These parameters did not change in any simulation presented in this study. When two val-ues are presented, they represent the respective values for the dynamic and static fibers.