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

• Type of Material: Article
• Authors: Kyle P. Blum, Northwestern University; Kenneth S. Campbell, University of Kentucky; Brian C. Horslen, Emory University; Paul Nardelli, Georgia Institute of Technology; Stephen N. Housley, Georgia Institute of Technology; Timothy Cope, Emory University; Lena Ting, Emory University
• Language: English
• Date: 2020-12-28
• Publisher: ELIFE SCIENCES PUBLICATIONS LTD
• Publication Version: Final Published Version
• Copyright Statement: © 2020, Blum et al.
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.7554/eLife.55177
• Title of Journal or Parent Work: ELIFE
• Volume: 9
• Start Page: 1
• End Page: 32
• Grant/Funding Information: This paper was supported by the following grants: Eunice Kennedy Shriver National Institute of Child Health and Human Development R01 HD90642 to Kenneth S Campbell, Timothy C Cope, Lena H Ting. National Cancer Institute R01 CA221363 to Timothy C Cope. National Institute of Neurological Disorders and Stroke F31 NS093855 to Kyle P Blum. Government of Canada BPF-156622 to Brian C Horslen.; The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
• Keywords: BAG FIBERS; DYNAMIC-RESPONSE; FUSIMOTOR STIMULATION; NORMAL LOCOMOTION; SECONDARY ENDINGS; Biology; INTRAFUSAL MUSCLE; MYOSIN HEADS; Life Sciences & Biomedicine; PRIMARY ENDINGS; INITIAL BURST; Science & Technology; Life Sciences & Biomedicine - Other Topics; NUCLEAR CHAIN FIBERS
• Research Categories: Biology, Anatomy; Biology, General

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 la 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.