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Published in: European Journal of Applied Physiology 3/2008

Open Access 01-10-2008 | Original Article

Effects of firing frequency on length-dependent myofascial force transmission between antagonistic and synergistic muscle groups

Authors: H. J. M. Meijer, J. M. Rijkelijkhuizen, P. A. Huijing

Published in: European Journal of Applied Physiology | Issue 3/2008

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Abstract

Effects of stimulation frequency on myofascial force transmission between rat peroneal and triceps surae and antagonistic anterior crural muscles, and between extensor digitorum longus (EDL) and tibialis anterior and extensor hallucis longus (TA + EHL) muscles were investigated for lengthening of all anterior crural muscles. Muscles contracted isometrically at firing rates of 10, 20, 30 and 100 Hz. EDL and TA + EHL were distally lengthened. Peroneal and triceps surae muscles attained a constant muscle-tendon complex length. Peroneal and triceps surae distal active force decreased significantly as a function of anterior crural muscle length, also at submaximal activation. The absolute decrease was highest for 100 Hz (peroneal muscles −0.87 N; triceps surae muscles −0.92 N), but the highest normalized decrease occurred at 10 Hz stimulation (peroneal muscles −34%; triceps surae muscles −18%). At all muscle lengths, a negative proximo-distal difference in EDL active force was present which decreased with lower firing frequencies (from −0.4 N at 100 Hz to −0.03 N at 10 Hz). The passive proximo-distal force difference attained positive values. EDL and TA + EHL length–force characteristics agree with effects of firing frequency, except for 10 Hz stimulation, where active force was higher than expected and optimum length shifted to lower muscle lengths. It is concluded that also at submaximal stimulation frequencies, extramuscular myofascial force transmission between peroneal and triceps surae muscles and antagonistic anterior crural muscles is substantial. Although lengthening of submaximally active anterior crural muscles decreases the net myofascially transmitted load on EDL, myofascial force transmission significantly alters effects of firing frequency on length–force characteristics.
Literature
go back to reference Bloch RJ, Gonzalez-Serratos H (2003) Lateral force transmission across costameres in skeletal muscle. Exerc Sport Sci Rev 31:73–78PubMedCrossRef Bloch RJ, Gonzalez-Serratos H (2003) Lateral force transmission across costameres in skeletal muscle. Exerc Sport Sci Rev 31:73–78PubMedCrossRef
go back to reference Brown IE, Cheng EJ, Loeb GE (1999) Measured and modeled properties of mammalian skeletal muscle II. The effects of stimulus frequency on force–length and force–velocity relationships. J Muscle Res Cell Motil 20:627–643PubMedCrossRef Brown IE, Cheng EJ, Loeb GE (1999) Measured and modeled properties of mammalian skeletal muscle II. The effects of stimulus frequency on force–length and force–velocity relationships. J Muscle Res Cell Motil 20:627–643PubMedCrossRef
go back to reference Huijing PA (2003) Muscular force transmission necessitates a multilevel integrative approach to the analysis of function of skeletal muscle. Exerc Sport Sci Rev 31:167–175PubMedCrossRef Huijing PA (2003) Muscular force transmission necessitates a multilevel integrative approach to the analysis of function of skeletal muscle. Exerc Sport Sci Rev 31:167–175PubMedCrossRef
go back to reference Huijing PA (2007) Epimuscular myofascial force transmission between antagonistic and synergistic muscles can explain movement limitation in spastic paresis. J Electromyogr Kinesiol 17:708–724PubMedCrossRef Huijing PA (2007) Epimuscular myofascial force transmission between antagonistic and synergistic muscles can explain movement limitation in spastic paresis. J Electromyogr Kinesiol 17:708–724PubMedCrossRef
go back to reference Huijing PA, Baan GC (2001a) Extramuscular myofascial force transmission within the rat anterior tibial compartment: proximo-distal differences in muscle force. Acta Physiol Scand 173:297–311PubMedCrossRef Huijing PA, Baan GC (2001a) Extramuscular myofascial force transmission within the rat anterior tibial compartment: proximo-distal differences in muscle force. Acta Physiol Scand 173:297–311PubMedCrossRef
go back to reference Huijing PA, Baan GC (2001b) Myofascial force transmission causes interaction between adjacent muscles and connective tissue: effects of blunt dissection and compartmental fasciotomy on length–force characteristics of rat extensor digitorum longus muscle. Arch Physiol Biochem 109:97–109PubMedCrossRef Huijing PA, Baan GC (2001b) Myofascial force transmission causes interaction between adjacent muscles and connective tissue: effects of blunt dissection and compartmental fasciotomy on length–force characteristics of rat extensor digitorum longus muscle. Arch Physiol Biochem 109:97–109PubMedCrossRef
go back to reference Huijing PA, Baan GC (2003) Myofascial force transmission: muscle relative position and length determine agonist and synergist muscle force. J Appl Physiol 94:1092–1107PubMed Huijing PA, Baan GC (2003) Myofascial force transmission: muscle relative position and length determine agonist and synergist muscle force. J Appl Physiol 94:1092–1107PubMed
go back to reference Huijing PA, Baan GC, Rebel GT (1998) Non-myotendinous force transmission in rat extensor digitorum longus muscle. J Exp Biol 201:682–691 Huijing PA, Baan GC, Rebel GT (1998) Non-myotendinous force transmission in rat extensor digitorum longus muscle. J Exp Biol 201:682–691
go back to reference Huijing PA, Jaspers RT (2005) Adaptation of muscle size and myofascial force transmission: a review and some new experimental results. Scand J Med Sci Sports 15:349–380PubMedCrossRef Huijing PA, Jaspers RT (2005) Adaptation of muscle size and myofascial force transmission: a review and some new experimental results. Scand J Med Sci Sports 15:349–380PubMedCrossRef
go back to reference Huijing PA, van de Langenberg RW, Meesters J, Baan GC (2007) Extramuscular myofascial force transmission also occurs between synergistic muscles and antagonistic muscles. J Electromyogr Kinesiol 17:680–689PubMedCrossRef Huijing PA, van de Langenberg RW, Meesters J, Baan GC (2007) Extramuscular myofascial force transmission also occurs between synergistic muscles and antagonistic muscles. J Electromyogr Kinesiol 17:680–689PubMedCrossRef
go back to reference Kreulen M, Smeulders MJ, Hage JJ, Huijing PA (2003) Biomechanical effects of dissecting flexor carpi ulnaris. J Bone Joint Surg Br 85:856–859PubMed Kreulen M, Smeulders MJ, Hage JJ, Huijing PA (2003) Biomechanical effects of dissecting flexor carpi ulnaris. J Bone Joint Surg Br 85:856–859PubMed
go back to reference Maas H, Baan GC, Huijing PA (2001) Intermuscular interaction via myofascial force transmission: effects of tibialis anterior and extensor hallucis longus length on force transmission from rat extensor digitorum longus muscle. J Biomech 34:927–940PubMedCrossRef Maas H, Baan GC, Huijing PA (2001) Intermuscular interaction via myofascial force transmission: effects of tibialis anterior and extensor hallucis longus length on force transmission from rat extensor digitorum longus muscle. J Biomech 34:927–940PubMedCrossRef
go back to reference Maas H, Baan GC, Huijing PA, Yucesoy CA, Koopman BH, Grootenboer HJ (2003a) The relative position of EDL muscle affects the length of sarcomeres within muscle fibers: experimental results and finite-element modeling. J Biomech Eng 125:745–753PubMedCrossRef Maas H, Baan GC, Huijing PA, Yucesoy CA, Koopman BH, Grootenboer HJ (2003a) The relative position of EDL muscle affects the length of sarcomeres within muscle fibers: experimental results and finite-element modeling. J Biomech Eng 125:745–753PubMedCrossRef
go back to reference Maas H, Yucesoy CA, Baan GC, Huijing PA (2003b) Implications of muscle relative position as a co-determinant of isometric muscle force: a review and some experimental results. J Mech Med Biol 3:145–168CrossRef Maas H, Yucesoy CA, Baan GC, Huijing PA (2003b) Implications of muscle relative position as a co-determinant of isometric muscle force: a review and some experimental results. J Mech Med Biol 3:145–168CrossRef
go back to reference Maas H, Meijer HJM, Huijing P (2005) Intermuscular interaction between synergists in rat originates from both intermuscular and extramuscular myofascial force transmission. Cells Tissues Organs 181:38–50PubMedCrossRef Maas H, Meijer HJM, Huijing P (2005) Intermuscular interaction between synergists in rat originates from both intermuscular and extramuscular myofascial force transmission. Cells Tissues Organs 181:38–50PubMedCrossRef
go back to reference MacIntosh BR, MacNaughton MB (2005) The length-dependence of muscle active force: considerations for parallel elastic properties. J Appl Physiol 98:1666–1673PubMedCrossRef MacIntosh BR, MacNaughton MB (2005) The length-dependence of muscle active force: considerations for parallel elastic properties. J Appl Physiol 98:1666–1673PubMedCrossRef
go back to reference Meijer HJM, Baan GC, Huijing PA (2006) Myofascial force transmission is increasingly important at lower forces: firing frequency-related length–force characteristics of rat extensor digitorum longus. Acta Physiol (Oxf) 186:185–195 Meijer HJM, Baan GC, Huijing PA (2006) Myofascial force transmission is increasingly important at lower forces: firing frequency-related length–force characteristics of rat extensor digitorum longus. Acta Physiol (Oxf) 186:185–195
go back to reference Meijer HJM, Rijkelijkhuizen JM, Huijing PA (2007) Myofascial force transmission between antagonistic rat lower limb muscles: effects of single muscle or muscle group lengthening. J Electromyogr Kinesiol 17:698–707PubMedCrossRef Meijer HJM, Rijkelijkhuizen JM, Huijing PA (2007) Myofascial force transmission between antagonistic rat lower limb muscles: effects of single muscle or muscle group lengthening. J Electromyogr Kinesiol 17:698–707PubMedCrossRef
go back to reference Monti RJ, Roy RR, Hodgson JA, Edgerton VR (1999) Transmission of forces within mammalian skeletal muscles. J Biomech 32:371–380PubMedCrossRef Monti RJ, Roy RR, Hodgson JA, Edgerton VR (1999) Transmission of forces within mammalian skeletal muscles. J Biomech 32:371–380PubMedCrossRef
go back to reference Neter J, Wasserman W, Kutner ME (1990) Applied linear statistic models: regression. analysis of variance and experimental design, Irwin, Homewood Neter J, Wasserman W, Kutner ME (1990) Applied linear statistic models: regression. analysis of variance and experimental design, Irwin, Homewood
go back to reference Pasternak C, Wong S, Elson E (1995) Mechanical function of dystrophin in muscle cells. J Cell Biol 128:355–361PubMedCrossRef Pasternak C, Wong S, Elson E (1995) Mechanical function of dystrophin in muscle cells. J Cell Biol 128:355–361PubMedCrossRef
go back to reference Rack PM, Westbury DR (1969) The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J Physiol (Lond) 204:443–460 Rack PM, Westbury DR (1969) The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J Physiol (Lond) 204:443–460
go back to reference Rijkelijkhuizen JM, Baan GC, de Haan A, de Ruiter CJ, Huijing PA (2005) Extramuscular myofascial force transmission for in situ rat medial gastrocnemius and plantaris muscles in progressive stages of dissection. J Exp Biol 208:129–140PubMedCrossRef Rijkelijkhuizen JM, Baan GC, de Haan A, de Ruiter CJ, Huijing PA (2005) Extramuscular myofascial force transmission for in situ rat medial gastrocnemius and plantaris muscles in progressive stages of dissection. J Exp Biol 208:129–140PubMedCrossRef
go back to reference Rijkelijkhuizen JM, Meijer HJM, Baan GC, Huijing PA (2007) Myofascial force transmission also occurs between antagonistic muscles located within opposite compartments of the rat lower hind limb. J Electromyogr Kinesiol 17:690–697PubMedCrossRef Rijkelijkhuizen JM, Meijer HJM, Baan GC, Huijing PA (2007) Myofascial force transmission also occurs between antagonistic muscles located within opposite compartments of the rat lower hind limb. J Electromyogr Kinesiol 17:690–697PubMedCrossRef
go back to reference Roszek B, Huijing PA (1997) Stimulation frequency history alters length–force characteristics of fully recruited rat muscle. J Electromyogr Kinesiol 7:161–177CrossRef Roszek B, Huijing PA (1997) Stimulation frequency history alters length–force characteristics of fully recruited rat muscle. J Electromyogr Kinesiol 7:161–177CrossRef
go back to reference Smeulders MJ, Kreulen M (2007) Myofascial force transmission and tendon transfer for patients suffering from spastic paresis: A review and some new observations. J Electromyogr Kinesiol 17:644–656PubMedCrossRef Smeulders MJ, Kreulen M (2007) Myofascial force transmission and tendon transfer for patients suffering from spastic paresis: A review and some new observations. J Electromyogr Kinesiol 17:644–656PubMedCrossRef
go back to reference Stephenson DG, Wendt IR (1984) Length dependence of changes in sarcoplasmic calcium concentration and myofibrillar calcium sensitivity in striated muscle fibers. J Muscle Res Cell Motil 5:243–272PubMedCrossRef Stephenson DG, Wendt IR (1984) Length dependence of changes in sarcoplasmic calcium concentration and myofibrillar calcium sensitivity in striated muscle fibers. J Muscle Res Cell Motil 5:243–272PubMedCrossRef
go back to reference Street SF (1983) Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol 114:346–364PubMedCrossRef Street SF (1983) Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol 114:346–364PubMedCrossRef
go back to reference Street SF, Ramsey RW (1965) Sarcolemma: transmitter of active tension in frog skeletal muscle. Science 149:1379–1380PubMedCrossRef Street SF, Ramsey RW (1965) Sarcolemma: transmitter of active tension in frog skeletal muscle. Science 149:1379–1380PubMedCrossRef
go back to reference Sheard P, Paul A, Duxson M (2002) Intramuscular force transmission. Adv Exp Med Biol 508:495–499PubMed Sheard P, Paul A, Duxson M (2002) Intramuscular force transmission. Adv Exp Med Biol 508:495–499PubMed
go back to reference Trotter JA, Hsi K, Samora A, Wofsy C (1985) A morphometric analysis of the muscle-tendon junction. Anat Rec 213:26–32PubMedCrossRef Trotter JA, Hsi K, Samora A, Wofsy C (1985) A morphometric analysis of the muscle-tendon junction. Anat Rec 213:26–32PubMedCrossRef
go back to reference Yucesoy CA, Koopman BH, Baan GC, Grootenboer HJ, Huijing PA (2003) Effects of inter- and extramuscular myofascial force transmission on adjacent synergistic muscles: assessment by experiments and finite-element modeling. J Biomech 36:1797–1811PubMedCrossRef Yucesoy CA, Koopman BH, Baan GC, Grootenboer HJ, Huijing PA (2003) Effects of inter- and extramuscular myofascial force transmission on adjacent synergistic muscles: assessment by experiments and finite-element modeling. J Biomech 36:1797–1811PubMedCrossRef
go back to reference Yucesoy CA, Maas H, Koopman BH, Grootenboer HJ, Huijing PA (2006) Mechanisms causing effects of muscle position on proximo-distal muscle force differences in extra-muscular myofascial force transmission. Med Eng Phys 28:214–226PubMedCrossRef Yucesoy CA, Maas H, Koopman BH, Grootenboer HJ, Huijing PA (2006) Mechanisms causing effects of muscle position on proximo-distal muscle force differences in extra-muscular myofascial force transmission. Med Eng Phys 28:214–226PubMedCrossRef
Metadata
Title
Effects of firing frequency on length-dependent myofascial force transmission between antagonistic and synergistic muscle groups
Authors
H. J. M. Meijer
J. M. Rijkelijkhuizen
P. A. Huijing
Publication date
01-10-2008
Publisher
Springer-Verlag
Published in
European Journal of Applied Physiology / Issue 3/2008
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-008-0788-5

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