Advertisement

Contribution of stroke-related changes in neuromuscular factors to gear ratio during isometric contraction of medial gastrocnemius muscle: A simulation study

  • Jongsang Son
    Correspondence
    Corresponding author at: 323 Dr Martin Luther King Jr Blvd, Newark, NJ 07102, United States.
    Affiliations
    Department of Biomedical Engineering, Newark College of Engineering, New Jersey Institute of Technology, Newark, NJ, United States
    Search for articles by this author
  • William Z. Rymer
    Affiliations
    Shirley Ryan AbilityLab (formerly the Rehabilitation Institute of Chicago), Chicago, IL, United States

    Department of Physical Medicine and Rehabilitation, Feinberg School of Medicine, Northwestern University, Chicago, IL, United States
    Search for articles by this author

      Highlights

      • Gear ratio decreases significantly with smaller pennation angle and shorter optimal fiber length.
      • Gear ratio may be primarily determined by initial pennation angle and fiber rotationshortening ratio.
      • Pennation angle may play an important role for efficient muscular contraction.

      Abstract

      Background

      It is not clear which neuromuscular factors are most closely associated with the loss of variable fascicle gearing after chronic stroke. The purpose of this simulation study is to determine the effects of stroke-related changes in key neuromuscular factors on the gear ratio.

      Methods

      A modified Hill-type model of the medial gastrocnemius was developed to determine the gear ratio for a given muscle activation level and musculotendon length. Model parameters were then systematically adjusted to simulate known stroke-related changes in neuromuscular factors, and the gear ratio was computed for each change in the parameters. A Monte Carlo simulation was performed to understand which neuromuscular factors and fiber behavior-related parameters are most relevant to the loss of variable gearing. Dominance analyses were also conducted to quantify the relative importance of fiber behavior-related parameters on the gear ratio.

      Findings

      The gear ratio decreases significantly with smaller pennation angle and with shorter optimal fiber length. In addition, muscle thickness and pennation angle at optimal fiber length appear to be the most important muscle architectural parameters. Dominance analyses further suggest that primary determinants of gear ratio include initial pennation angle, fiber rotation-shortening ratio, initial muscle thickness, and fiber rotation.

      Interpretation

      Our findings provide insight that the pennation angle may play an important role for efficient muscular contraction, implying that maintaining muscle architecture and/or improving fiber/fascicle rotation could a key goal in rehabilitation interventions. Our findings will help us to better interpret altered gearing behavior in aging and pathological muscles.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Clinical Biomechanics
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Adkins A.N.
        • Dewald J.P.A.
        • Garmirian L.P.
        • Nelson C.M.
        • Murray W.M.
        Serial sarcomere number is substantially decreased within the paretic biceps brachii in individuals with chronic hemiparetic stroke.
        Proc. Natl. Acad. Sci. U. S. A. 2021; 118e2008597118
        • Andreassen S.
        • Rosenfalck A.
        Impaired regulation of the firing pattern of single motor units.
        Muscle Nerve. 1978; 1: 416-418
        • Azen R.
        • Budescu D.V.
        The dominance analysis approach for comparing predictors in multiple regression.
        Psychol. Methods. 2003; 8: 129-148
        • Azizi E.
        • Brainerd E.L.
        • Roberts T.J.
        Variable gearing in pennate muscles.
        Proc. Natl. Acad. Sci. U. S. A. 2008; 105: 1745-1750
        • Azizi E.
        • Deslauriers A.R.
        • Holt N.C.
        • Eaton C.E.
        Resistance to radial expansion limits muscle strain and work.
        Biomech. Model. Mechanobiol. 2017; 16: 1633-1643
        • Benjamini Y.
        • Hochberg Y.
        Controlling the false discovery rate: a practical and powerful approach to multiple testing.
        J. R. Stat. Soc. Ser. B Methodol. 1995; 57: 289-300
        • Bohannon R.W.
        Relative decreases in knee extension torque with increased knee extension velocities in stroke patients with hemiparesis.
        Phys. Ther. 1987; 67: 1218-1220
        • Clark D.J.
        • Condliffe E.G.
        • Patten C.
        Activation impairment alters muscle torque–velocity in the knee extensors of persons with post-stroke hemiparesis.
        Clin. Neurophysiol. 2006; 117: 2328-2337
        • Dias C.P.
        • Freire B.
        • Goulart N.B.A.
        • Onzi E.S.
        • Becker J.
        • Gomes I.
        • et al.
        Muscle architecture and torque production in stroke survivors: an observational study.
        Top. Stroke Rehabil. 2017; 24: 206-213
        • Dick T.J.M.
        • Wakeling J.M.
        Shifting gears: dynamic muscle shape changes and force-velocity behavior in the medial gastrocnemius.
        J. Appl. Physiol. 2017; 123: 1433-1442
        • D'Souza A.
        • Bolsterlee B.
        • Herbert R.D.
        Intramuscular Fat in the Medial Gastrocnemius Muscle of People who have had a Stroke.
        Frontiers in Bioengineering and Biotechnology. vol. 8. 2020
        • Eng C.M.
        • Roberts T.J.
        Aponeurosis influences the relationship between muscle gearing and force.
        J. Appl. Physiol. 2018; 125: 513-519
        • Frontera W.R.
        • Grimby L.
        • Larsson L.
        Firing rate of the lower motoneuron and contractile properties of its muscle fibers after upper motoneuron lesion in man.
        Muscle Nerve. 1997; 20: 938-947
        • Gao F.
        • Zhang L.-Q.
        Altered contractile properties of the gastrocnemius muscle poststroke.
        J. Appl. Physiol. 2008; 105: 1802-1808
        • Gao F.
        • Grant T.H.
        • Roth E.J.
        • Zhang L.-Q.
        Changes in passive mechanical properties of the gastrocnemius muscle at the muscle fascicle and joint levels in stroke survivors.
        Arch. Phys. Med. Rehabil. 2009; 90: 819-826
        • Gemperline J.J.
        • Allen S.
        • Walk D.
        • Rymer W.Z.
        Characteristics of motor unit discharge in subjects with hemiparesis.
        Muscle Nerve. 1995; 18: 1101-1114
        • Gindre J.
        • Takaza M.
        • Moerman K.M.
        • Simms C.K.
        A structural model of passive skeletal muscle shows two reinforcement processes in resisting deformation.
        J. Mech. Behav. Biomed. Mater. 2013; 22: 84-94
        • Gray V.
        • Rice C.L.
        • Garland S.J.
        Factors that influence muscle weakness following stroke and their clinical implications: a critical review.
        Physiother. Can. 2012; 64: 415-426
        • Hill A.V.
        The heat of shortening and the dynamic constants of muscle.
        Proc. R. Soc. B. 1938; 126: 612-745
        • Hodgson J.A.
        • Chi S.-W.
        • Yang J.P.
        • Chen J.-S.
        • Edgerton V.R.
        • Sinha S.
        Finite element modeling of passive material influence on the deformation and force output of skeletal muscle.
        J. Mech. Behav. Biomed. Mater. 2012; 9: 163-183
        • Holt N.C.
        • Danos N.
        • Roberts T.J.
        • Azizi E.
        Stuck in gear: age-related loss of variable gearing in skeletal muscle.
        J. Exp. Biol. 2016; 219: 998-1003
        • Hu X.
        • Suresh A.K.
        • Rymer W.Z.
        • Suresh N.L.
        Assessing altered motor unit recruitment patterns in paretic muscles of stroke survivors using surface electromyography.
        J. Neural Eng. 2015; 12066001
        • Hu X.
        • Suresh A.K.
        • Rymer W.Z.
        • Suresh N.L.
        Altered motor unit discharge patterns in paretic muscles of stroke survivors assessed using surface electromyography.
        J. Neural Eng. 2016; 13046025
        • Jakubowski K.L.
        • Terman A.
        • Santana R.V.C.
        • Lee S.S.M.
        Passive material properties of stroke-impaired plantarflexor and dorsiflexor muscles.
        Clin. Biomech. 2017; 49: 48-55
        • Kawakami Y.
        • Ichinose Y.
        • Fukunaga T.
        Architectural and functional features of human triceps surae muscles during contraction.
        J. Appl. Physiol. 1998; 85: 398-404
        • Knarr B.A.
        • Ramsay J.W.
        • Buchanan T.S.
        • Higginson J.S.
        • Binder-Macleod S.A.
        Muscle volume as a predictor of maximum force generating ability in the plantar flexors post-stroke.
        Muscle Nerve. 2013; 48: 971-976
        • Lee S.S.M.
        • Spear S.
        • Rymer W.Z.
        Quantifying changes in material properties of stroke-impaired muscle.
        Clin. Biomech. 2015; 30: 269-275
        • Lee S.S.M.
        • Jakubowski K.L.
        • Spear S.C.
        • Rymer W.Z.
        Muscle material properties in passive and active stroke-impaired muscle.
        J. Biomech. 2019; 83: 197-204
        • Lieber R.L.
        • Fridén J.
        Muscle contracture and passive mechanics in cerebral palsy.
        J. Appl. Physiol. 2018; 126: 1492-1501
        • Maganaris C.N.
        • Baltzopoulos V.
        • Sargeant A.J.
        In vivo measurements of the triceps surae complex architecture in man: implications for muscle function.
        J. Physiol. 1998; 512: 603-614
        • Mathewson M.A.
        • Lieber R.L.
        Pathophysiology of muscle contractures in cerebral palsy.
        Phys. Med. Rehabil. Clin. N. Am. 2015; 26: 57-67
        • Monte A.
        In vivo manipulation of muscle shape and tendinous stiffness affects the human ability to generate torque rapidly.
        Exp. Physiol. 2020; 106: 486-495
        • Monte A.
        • Bertucco M.
        • Magris R.
        • Zamparo P.
        Muscle belly gearing positively affects the force–velocity and power–velocity relationships during explosive dynamic contractions.
        Front. Physiol. 2021; 12
        • Mottram C.J.
        • Heckman C.J.
        • Powers R.K.
        • Rymer W.Z.
        • Suresh N.L.
        Disturbances of motor unit rate modulation are prevalent in muscles of spastic-paretic stroke survivors.
        J. Neurophysiol. 2014; 111: 2017-2028
        • Narici M.V.
        • Binzoni T.
        • Hiltbrand E.
        • Fasel J.
        • Terrier F.
        • Cerretelli P.
        In vivo human gastrocnemius architecture with changing joint angle at rest and during graded isometric contraction.
        J. Physiol. 1996; 496: 287-297
        • Otten E.
        Concepts and models of functional architecture in skeletal muscle.
        Exerc. Sport Sci. Rev. 1988; 16: 89-137
        • Patten C.
        • Lexell J.
        • Brown H.E.
        Weakness and strength training in persons with poststroke hemiplegia: rationale, method, and efficacy.
        J. Rehabil. Res. Dev. 2004; 41: 293-312
        • Rahemi H.
        • Nigam N.
        • Wakeling J.M.
        The effect of intramuscular fat on skeletal muscle mechanics: implications for the elderly and obese.
        J. R. Soc. Interface. 2015; 12: 20150365
        • Ramsay J.W.
        • Barrance P.J.
        • Buchanan T.S.
        • Higginson J.S.
        Paretic muscle atrophy and non-contractile tissue content in individual muscles of the post-stroke lower extremity.
        J. Biomech. 2011; 44: 2741-2746
        • Ramsay J.W.
        • Buchanan T.S.
        • Higginson J.S.
        Differences in plantar flexor fascicle length and pennation angle between healthy and poststroke individuals and implications for poststroke plantar flexor force contributions.
        Stroke Res. Treat. 2014; 2014: 6
        • Randhawa A.
        • Jackman M.E.
        • Wakeling J.M.
        Muscle gearing during isotonic and isokinetic movements in the ankle plantarflexors.
        Euro. J. Appl. Physio. 2013; 113: 437-447
        • Ryan A.S.
        • Dobrovolny C.L.
        • Smith G.V.
        • Silver K.H.
        • Macko R.F.
        Hemiparetic muscle atrophy and increased intramuscular fat in stroke patients.
        Arch. Phys. Med. Rehabil. 2002; 83: 1703-1707
        • Siebert T.
        • Eb M.
        • Ryan D.S.
        • Wakeling J.M.
        • Stutzig N.
        Impact of multidirectional transverse calf muscle loading on calf muscle force in young adults.
        Front. Physiol. 2018; 9
        • Son J.
        • Rymer W.Z.
        Loss of variable fascicle gearing during voluntary isometric contractions of paretic medial gastrocnemius muscles in male chronic stroke survivors.
        J. Physiol. 2020; 598: 5183-5194
        • Son J.
        • Rymer W.Z.
        • Lee S.S.M.
        Limited fascicle shortening and fascicle rotation may be associated with impaired voluntary force-generating capacity in pennate muscles of chronic stroke survivors.
        Clin. Biomech. 2020; 75105007
        • Svantesson U.
        • Takahashi H.
        • Carlsson U.
        • Danielsson A.
        • Stibrant Sunnerhagen K.
        Muscle and tendon stiffness in patients with upper motor neuron lesion following a stroke.
        Euro. J. Appl. Physio. 2000; 82: 275-279
        • Thelen D.G.
        Adjustment of muscle mechanics model parameters to simulate dynamic contractions in older adults.
        J. Biomech. Eng. 2003; 125: 70-77
        • Wakeling J.M.
        • Jackman M.
        • Namburete A.I.
        The effect of external compression on the mechanics of muscle contraction.
        J. Appl. Biomech. 2013; 29: 360-364
        • Zhao H.
        • Ren Y.
        • Wu Y.-N.
        • Liu S.Q.
        • Zhang L.-Q.
        Ultrasonic evaluations of achilles tendon mechanical properties poststroke.
        J. Appl. Physiol. 2009; 106: 843-849
        • Zhao H.
        • Ren Y.
        • Roth E.J.
        • Harvey R.L.
        • Zhang L.-Q.
        Concurrent deficits of soleus and gastrocnemius muscle fascicles and achilles tendon post stroke.
        J. Appl. Physiol. 2015; 118: 863-871