Intrafusal cross‐bridge dynamics shape history‐dependent muscle spindle responses to stretch

• Published in: Experimental physiology Vol. 109; no. 1; pp. 112 - 124
• Main Authors: Simha, Surabhi N., Ting, Lena H.
• Format: Journal Article
• Language: English
• Published: England John Wiley & Sons, Inc 01.01.2024; John Wiley and Sons Inc; Wiley
• Subjects: Actin; Behavior; Computational neuroscience; Firing rate; Force; Locomotion; Muscle Fibers, Skeletal; muscle spindle firing; Muscle spindles; Muscle Spindles - physiology; Myosin; Myosins - metabolism; Physiology; Posture; Roads & highways; Sarcomeres; Sense organs; sensory encoding; Sensory neurons; Sensory Receptor Cells; short‐range stiffness; short-range stiffness; sensory encoding; muscle spindle firing
• ISSN: 0958-0670; 1469-445X
• DOI: 10.1113/EP090767

Computational models can be critical to linking complex properties of muscle spindle organs to the sensory information that they encode during behaviours such as postural sway and locomotion where few muscle spindle recordings exist. Here, we augment a biophysical muscle spindle model to predict the muscle spindle sensory signal. Muscle spindles comprise several intrafusal muscle fibres with varied myosin expression and are innervated by sensory neurons that fire during muscle stretch. We demonstrate how cross‐bridge dynamics from thick and thin filament interactions affect the sensory receptor potential at the spike initiating region. Equivalent to the Ia afferent's instantaneous firing rate, the receptor potential is modelled as a linear sum of the force and rate change of force (yank) of a dynamic bag1 fibre and the force of a static bag2/chain fibre. We show the importance of inter‐filament interactions in (i) generating large changes in force at stretch onset that drive initial bursts and (ii) faster recovery of bag fibre force and receptor potential following a shortening. We show how myosin attachment and detachment rates qualitatively alter the receptor potential. Finally, we show the effect of faster recovery of receptor potential on cyclic stretch–shorten cycles. Specifically, the model predicts history‐dependence in muscle spindle receptor potentials as a function of inter‐stretch interval (ISI), pre‐stretch amplitude and the amplitude of sinusoidal stretches. This model provides a computational platform for predicting muscle spindle response in behaviourally relevant stretches and can link myosin expression seen in healthy and diseased intrafusal muscle fibres to muscle spindle function. What is the central question of the study? A computational biophysical muscle model was used to ask how muscle cross‐bridge dynamics shape the information that can be encoded by intrafusal muscle fibres within the muscle spindle. What is the main finding and its importance? Both actin and myosin dynamics and their interactions can shape muscle spindle sensory signals and are necessary to simulate history‐dependent muscle spindle firing properties to be more in line with experimental observations. The tuned muscle spindle model shows that non‐linear and history‐dependent muscle spindle firing properties to sinusoids reported previously emerge from intrafusal cross‐bridge dynamics.