journal article Open Access Sep 15, 2023

History-dependent muscle resistance to stretch remains high after small, posturally relevant pre-movements

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Abstract
ABSTRACT
The contributions of intrinsic muscle fiber resistance during mechanical perturbations to standing and other postural behaviors are unclear. Muscle short-range stiffness is known to vary depending on the current level and history of the muscle's activation, as well as the muscle's recent movement history; this property has been referred to as history dependence or muscle thixotropy. However, we currently lack sufficient data about the degree to which muscle stiffness is modulated across posturally relevant characteristics of muscle stretch and activation. We characterized the history dependence of muscle's resistance to stretch in single, permeabilized, activated, muscle fibers in posturally relevant stretch conditions and activation levels. We used a classic paired muscle stretch paradigm, varying the amplitude of a ‘conditioning’ triangular stretch–shorten cycle followed by a ‘test’ ramp-and-hold imposed after a variable inter-stretch interval. We tested low (<15%), intermediate (15–50%) and high (>50%) muscle fiber activation levels, evaluating short-range stiffness and total impulse in the test stretch. Muscle fiber resistance to stretch remained high at conditioning amplitudes of <1% optimal fiber length, L0, and inter-stretch intervals of >1 s, characteristic of healthy standing postural sway. An ∼70% attenuation of muscle resistance to stretch was reached at conditioning amplitudes of >3% L0 and inter-stretch intervals of <0.1 s, characteristic of larger, faster postural sway in balance-impaired individuals. The thixotropic changes cannot be predicted solely on muscle force at the time of stretch. Consistent with the disruption of muscle cross-bridges, muscle resistance to stretch during behavior can be substantially attenuated if the prior motion is large enough and/or frequent enough.
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References
48
[1]
Altman "Thixotropy and rheopexy of muscle fibers probed using sinusoidal oscillations" PLoS One (2015) 10.1371/journal.pone.0121726
[2]
Blum "Force encoding in muscle spindles during stretch of passive muscle" PLoS Comput. Biol. (2017) 10.1371/journal.pcbi.1005767
[3]
Blum "Diverse and complex muscle spindle afferent firing properties emerge from multiscale muscle mechanics" eLife (2020) 10.7554/elife.55177
[4]
Campbell "Tension recovery in permeabilized rat soleus muscle fibers after rapid shortening and restretch" Biophys. J. (2006) 10.1529/biophysj.105.067504
[5]
Campbell "A cross-bridge mechanism can explain the thixotropic short-range elastic component of relaxed frog skeletal muscle" J. Physiol. (1998) 10.1111/j.1469-7793.1998.941bj.x
[6]
Campbell "A thixotropic effect in contracting rabbit psoas muscle: prior movement reduces the initial tension response to stretch" J. Physiol. (2000) 10.1111/j.1469-7793.2000.00531.x
[7]
Campbell "History-dependent mechanical properties of permeabilized rat soleus muscle fibers" Biophys. J. (2002) 10.1016/s0006-3495(02)75454-4
[8]
Carpenter "The influence of postural threat on the control of upright stance" Exp. Brain Res. (2001) 10.1007/s002210100681
[9]
Carpenter "Deceleration affects anticipatory and reactive components of triggered postural responses" Exp. Brain Res. (2005) 10.1007/s00221-005-0049-3
[10]
Daley "Running over rough terrain reveals limb control for intrinsic stability" Proc. Natl. Acad. Sci. USA (2006) 10.1073/pnas.0601473103
[11]
Day "Tibialis anterior muscle fascicle dynamics adequately represent postural sway during standing balance" J. Appl. Physiol. (1985) (2013) 10.1152/japplphysiol.00517.2013
[12]
De Groote "Contribution of muscle short-range stiffness to initial changes in joint kinetics and kinematics during perturbations to standing balance: a simulation study" J. Biomech. (2017) 10.1016/j.jbiomech.2017.02.008
[13]
How Animals Move: An Integrative View

Michael H. Dickinson, Claire T. Farley, Robert J. Full et al.

Science 2000 10.1126/science.288.5463.100
[14]
Donaldson "Characterization of the effects of Mg2+ on Ca2+- and Sr2+-activated tension generation of skinned skeletal muscle fibers" J. Gen. Physiol. (1975) 10.1085/jgp.66.4.427
[15]
Geh "Assessed and distressed: white-coat effects on clinical balance performance" J. Psychosom. Res. (2011) 10.1016/j.jpsychores.2010.09.008
[16]
Herbst "Studies on the relation between latency relaxation and resting cross-bridges of frog skeletal muscle" Pflugers Arch. (1976) 10.1007/bf01062914
[17]
Hill "Tension due to interaction between the sliding filaments in resting striated muscle. The effect of stimulation" J. Physiol. (1968) 10.1113/jphysiol.1968.sp008672
[19]
Horak "Postural orientation and equilibrium" (2011) 10.1002/cphy.cp120107
[20]
Horslen "Arousal, valence and their relative effects on postural control" Exp. Brain Res. (2011) 10.1007/s00221-011-2867-9
[21]
Hu "Muscle short-range stiffness can be used to estimate the endpoint stiffness of the human arm" J. Neurophysiol. (2011) 10.1152/jn.00537.2010
[22]
Ivanenko "Human postural control" Front. Neurosci. (2018) 10.3389/fnins.2018.00171
[23]
Lakie "Muscle thixotropy-where are we now?" J. Appl. Physiol. (2019) 10.1152/japplphysiol.00788.2018
[24]
Lakie "Thixotropy: the effect of stretch size in relaxed frog muscle" Q. J. Exp. Physiol. (1988) 10.1113/expphysiol.1988.sp003110
[25]
Lännergren "The effect of low-level activation on the mechanical properties of isolated frog muscle fibers" J. Gen. Physiol. (1971) 10.1085/jgp.58.2.145
[26]
Larson "Transitional hybrid skeletal muscle fibers in rat soleus development" J. Histochem. Cytochem. (2019) 10.1369/0022155419876421
[27]
Lichtwark "Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running" J. Biomech. (2007) 10.1016/j.jbiomech.2005.10.035
[28]
Lockhart "Optimal sensorimotor transformations for balance" Nat. Neurosci. (2007) 10.1038/nn1986
[29]
Loram "Paradoxical muscle movement during postural control" Med. Sci. Sports Exerc. (2009) 10.1249/mss.0b013e318183c0ed
[30]
Lynch "Force deficits and breakage rates after single lengthening contractions of single fast fibers from unconditioned and conditioned muscles of young and old rats" Am. J. Physiol. Cell Physiol. (2008) 10.1152/ajpcell.90640.2007
[31]
Martino "Voluntary muscle coactivation in quiet standing elicits reciprocal rather than coactive agonist-antagonist control of reactive balance" J. Neurophysiol. (2023) 10.1152/jn.00458.2022
[32]
Mathew "Adaptive feedback control in human reaching adaptation to force fields" Front. Hum. Neurosci. (2021) 10.3389/fnhum.2021.742608
[33]
Maurer "Effect of chronic bilateral subthalamic nucleus (STN) stimulation on postural control in Parkinson's disease" Brain (2003) 10.1093/brain/awg100
[34]
Nichols "Reflex compensation for variations in the mechanical properties of a muscle" Science (1973) 10.1126/science.181.4095.182
[35]
Nichols "Improvement in linearity and regulation of stiffness that results from actions of stretch reflex" J. Neurophysiol. (1976) 10.1152/jn.1976.39.1.119
[36]
Sensorimotor Integration in Human Postural Control

R. J. Peterka

Journal of Neurophysiology 2002 10.1152/jn.2002.88.3.1097
[37]
Prieto "Measures of postural steadiness: differences between healthy young and elderly adults" IEEE Trans. Biomed. Eng. (1996) 10.1109/10.532130
[38]
Proske "The initial burst of impulses in responses of toad muscle spindles during stretch" J. Physiol. (1985) 10.1113/jphysiol.1985.sp015843
[39]
Proske "Thixotropy in skeletal muscle and in muscle spindles: a review" Prog. Neurobiol. (1993) 10.1016/0301-0082(93)90032-n
[40]
Rack "The short range stiffness of active mammalian muscle and its effect on mechanical properties" J. Physiol. (1974) 10.1113/jphysiol.1974.sp010613
[41]
Ramsey "Fiber-type dependence of stretch-induced force enhancement in rat skeletal muscle" Muscle Nerve (2010) 10.1002/mus.21744
[42]
Rassier "Effects of shortening on stretch-induced force enhancement in single skeletal muscle fibers" J. Biomech. (2004) 10.1016/j.jbiomech.2003.12.033
[43]
Rassier "Stretch-induced, steady-state force enhancement in single skeletal muscle fibers exceeds the isometric force at optimum fiber length" J. Biomech. (2003) 10.1016/s0021-9290(03)00155-6
[44]
Sakanaka "Sway-dependent changes in standing ankle stiffness caused by muscle thixotropy" J. Physiol. (2016) 10.1113/jp271137
[45]
Ting "Neuromechanical tuning of nonlinear postural control dynamics" Chaos (2009) 10.1063/1.3142245
[46]
Van Wouwe "Interactions between initial posture and task-level goal explain experimental variability in postural responses to perturbations of standing balance" J. Neurophysiol. (2021) 10.1152/jn.00476.2020
[47]
Warnica "The influence of ankle muscle activation on postural sway during quiet stance" Gait Posture (2014) 10.1016/j.gaitpost.2014.01.019
[48]
Welch "A feedback model explains the differential scaling of human postural responses to perturbation acceleration and velocity" J. Neurophysiol. (2009) 10.1152/jn.90775.2008
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Published
Sep 15, 2023
Vol/Issue
226(18)
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Funding
National Institutes of Health Award: R01 HD90642
Canadian Institutes of Health Research Award: BPF-156622
Georgia Institute of Technology
Cite This Article
Brian C. Horslen, Gregory N. Milburn, Kyle P. Blum, et al. (2023). History-dependent muscle resistance to stretch remains high after small, posturally relevant pre-movements. Journal of Experimental Biology, 226(18). https://doi.org/10.1242/jeb.245456