Is there inhibition during eccentric muscle contractions?
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1 Biomechanics of Human Movement: Mechanisms and Methods position 17th International Symposium Neuromuscular Research Center (NMRC) University of Jyväskylä Moment EMG VL EMG VM EMG RF Is there inhibition during eccentric muscle contractions? Functional implications and effects of resistance training Per Aagaard Institute of Sports Science and Clinical Biomechanics, University of Southern Denmark Aagaard et al., J. Appl. Physiol. 2 Types of muscle Types contraction of muscle contraction Eccentric Eccentric muscle muscle contraction contraction muscle muscle generating generating contractile contractile force force while while lengthening lengthening Concentric Concentric muscle muscle contraction muscle muscle generating generating contractile force force while while shortening Isometric muscle contraction muscle muscle generating contractile force force while while maintaining constant length length Eccentric Concentric Isometric Why is ECC strength important? In some sports very high eccentric muscle strength is a prerequisite for superior athletic performance... 1
2 Why is neural modulation important? Human skeletal muscles may contract eccentrically to slowly decelerate movement: 'dampening' function low muscle stiffness However, skeletal muscles can also contract eccentrically very rapidly to decelerate-accelerate movement (SSC): 'rebound' function high muscle stiffness Why is neural modulation important? Cat soleus, ventral nerve root stimulation in situ Joyce, Rack, Westbury, J Physiol 24, 1969 Why is neural modulation important? Cat soleus, ventral nerve root stimulation in situ Joyce, Rack, Westbury, J Physiol 24,
3 ntric contraction Why is neural modulation important? Neural drive m. quadriceps slow eccentric contraction Neural input from the CNS to myofibers determines the stiffness behavior pre trainingof the muscle: high-stiffness 'rebound' profile position or compliant 'dampening' profile Moment EMG VL 3
4 Knee Extensor torque Knee Extensor torque isometric rectus femoris Expression of maximal ECC muscle strength in vivo Moment of Force (Nm) vastus EMG ( Knee joint angle ( o ) -24 ECC CONC Angular velocity ( o s -1 ) Knee joint Muscle Force (isometric = %) Contractile characteristics of skeletal muscle during maximal ECC and CON contraction Katz B, J. Physiol. 96, Edman KAP, J. Physiol. 44, 1988 Katz B, J. Physiol. 96, 1939 Edman KAP, J. Physiol. 44, eccentric concentric 2 2 eccentric eccentric concentric concentric concentric percent of V 2 4 max percent of V max Contraction Speed Contraction percent Speed of V max Contraction Speed 1 Human quadriceps muscle, 12 electrical muscle stimulation superimposed onto maximal voluntary contraction (Westing et al 199) Arbitrary Units Contractile Force / Strength Arbitrary Units Muscle Force Arbitrary (isometric Units = %) Contractile Force / Strength From Aagaard & Thorstensson. Neuromuscular aspects of exercise: Adaptive responses evoked by strength training, Textbook of Sports Medicine (Eds. Kjær et al) 23 Contractile Force / Strength Increased electrically superimposed muscle torques only observed in untrained individuals, not in strength trained athletes... SEDENTARY subjects STRENGTH TRAINED subjects eccentric concentric eccentric concentric Knee Angular Velocity ( o /s) Knee Angular Velocity ( o /s) Amiridis, Martin, Van Hoecke et al, Eur J Appl Physiol
5 (Nm) Expression of maximal ECCentric and CONcentric muscle strength in vivo Maximal ECC and CONC quadriceps contraction strength (elite alpine skier) based on peak Moment highly strength trained athlete 5 (alpine skiier) based on peak Moment Moment of Force sedentary subject of similar age and body mass max ECC strength eccentric concentric Angular velocity ( o /sec) Aagaard, unpubl. data Team Danmark Testcenter centric contraction g pre training Surface EMG recording position Moment slow eccentric contraction EMG VL EMG VM EMG RF File: I15mn1L.1-15% MVC 4 2 Neuromuscular activity during ECC contractions Bic Fem -2-4 Segmented EMG patterns (burst behavior) typically 1 is observed during slow submaximal ECC muscle contraction Rect Fem Vast Lat -4 - degrees concentric phase Vast Med knee angle eccentric phase Time (miliseconds) 5
6 Neuromuscular activity during ECC contractions Segmented EMG patterns (burst behavior) typically is observed during slow submaximal ECC muscle contraction position Moment EMG VL How is it possible to evaluate neuromuscular activity during maximal ECC muscle contractions? EMG VM EMG RF nt VL Isokinetic dynamometry and muscle electromyography (EMG) recording VM RF Aagaard et al., J. Appl. Physiol. 2 Nm position Moment EMG VL EMG VM EMG RF Time ( Reduced neuromuscular activity ( EMG amplitude) during maximal ECC versus CON quadriceps contraction position Nm Moment EMG VL EMG VM EMG RF Westing et al
7 Reduced neuromuscular activity ( EMG amplitude) during maximal ECC versus CON quadriceps contraction Komi et al, Med Sci Sports Exerc 32, 2 Neuromuscular activity m. quadriceps slow CONC contraction pre training slow ECC contraction pre training 1 o position 1 o Nm 9 o Moment 9 o Calculating mean filtered EMG amplitude (iemg) EMG VL EMG VM Calculating mean filtered EMG amplitude (iemg) EMG RF Aagaard et al, J Appl Physiol 2 Suppressed quadriceps EMG activity during maximal ECC contraction Percent Percent Percent Percent eccentric -3 3 Knee angular velocity concentric ( o s -1 ) 24 quadriceps force moment percent EMG VL percent EMG VM percent EMG RF percent Percent Percent Average quadriceps EMG and strength Quadriceps force moment (percent) mean EMG Quadriceps (percent) fast ECC slow slow CONC fast -24 eccentric -3 3 concentric 24 Knee angular velocity ( o s -1 ) Aagaard et al, J Appl Physiol 2 7
8 femoris -25 Quadriceps 2 3 muscle 4 5 activity (EMG amplitude) 2 3varies 4 with 5 contraction mode (CON vs ECC) and Time knee (msec) joint angle Moment of Force (Nm) vastus lateralis EMG ( V) Knee joint angle ( o ) -24 ECC CONC Angular velocity ( o s -1 ) (n=14) Knee joint angle ( o ) -24 ECC CONC Angular velocity ( o s -1 ) Aagaard et al, J Appl Physiol 2 femoris -25 Quadriceps muscle 5 activity (EMG) is 2 reduced 3 4 in 5 Time the (msec) high-force region of the F-V relationship Moment of Force (Nm) vastus lateralis EMG ( V) Knee joint angle ( o ) -24 ECC CONC Angular velocity ( o s -1 ) (n=14) Knee joint angle ( o ) -24 ECC CONC Angular velocity ( o s -1 ) Aagaard et al, J Appl Physiol 2 femoris -25 In 2 contrast, 3 4 quadriceps 5 muscle activity 2 is 3 not 4 reduced 5 Time in (msec) the low-force region of the F-V Time relationship (msec) Moment of Force (Nm) vastus lateralis EMG ( V) Knee joint angle ( o ) -24 ECC CONC Angular velocity ( o s -1 ) (n=14) Knee joint angle ( o ) -24 ECC CONC Angular velocity ( o s -1 ) Aagaard et al, J Appl Physiol 2 8
9 femoris -25 In 2 contrast, 3 4 quadriceps 5 muscle activity 2 is 3 not 4 reduced 5 Time in (msec) the low-force region of the F-V Time relationship (msec) Moment of Force (Nm) vastus lateralis EMG ( V) Indicating that neuromuscular activity during maximal ECC 4 muscle force production in vivo 3 is mainly influenced 2 by negative force-feedback mechanism(s) Knee joint angle ( o ) -24 ECC CONC Angular velocity ( o s -1 ) (n=14) Knee joint angle ( o ) -24 ECC CONC Angular velocity ( o s -1 ) Aagaard et al, J Appl Physiol 2 Central activation - interpolated twitch analysis Isometric ECC CONcentric CONC ECCentric Reduced central activation during maximal eccentric muscle contraction in vivo? Isometric CONcentric ECCentric m. quadriceps femoris, maximal voluntary contraction efforts superimposed stimulation (triplet, 3 Hz) femoral nerve Regularly active subjects ~6 h per wk (28±8 yrs, n=1) Beltman, De Haan et al, J Appl Physiol 24 9
10 Reduced central activation during maximal eccentric muscle contraction in vivo? A: yes! Isometric CONcentric ECCentric ± 5 % 92 ± 5 % 79 ± 8 % Isometric Con Ecc m. quadriceps femoris, maximal voluntary contraction efforts Regularly active subjects ~6 h per wk (28±8 yrs, n=1) Beltman, De Haan et al, J Appl Physiol 24 Spinal motorneuron excitability assessed by evoked spinal motorneuron recording Brain motor cortex cerebellum Spinal cord spinal motor neurons Muscle EMG amplifier M H Stimulator The H-reflex Hoffmann reflex Sensory Ia afferent axon EMG recording electrodes Spinal cord -motorneuron Spinal motor neurons Muscle -motoneuron axon Stimulus electrode The H-reflex: electric stimulus is applied to Ia afferent axons evoked efferent motoneuron response (H-reflex) M 2 mv M H H 1 ms Aagaard et al, J Appl Physiol 92, 22 1
11 EMG amplifier M H Stimulator The H-reflex Hoffmann reflex Sensory Ia afferent axon -motorneuron EMG recording electrodes Spinal cord Spinal motor neurons Muscle -motoneuron axon Stimulus electrode Reduced H-reflex amplitude indicates altered spinal circuitry state: - excitability of spinal motoneurons and/or - presynaptic inhibition of Ia afferents - postsynaptic inhibition of spinal motoneurons 2 mv M M H 1 ms Aagaard et al, J Appl Physiol 92, 22 H-reflex recording during maximal ECC contraction isometric CONcentric ECCentric H max H max M max M max M max H max The H-reflex appears to be markedly suppressed during maximal voluntary ECC muscle contraction in vivo Indicating excitability of spinal motor neurons during maximal ECC contraction and/or presynaptic inhibition Maximal plantarflexor contractions Soleus muscle, ankle joint angular velocity: 3 o /sec Duclay & Martin, J Neurophysiol 25 H-reflex recording during maximal ECC contraction isometric CONcentric ECCentric H max H max M max M max M max H max The H-reflex appears to be markedly suppressed during maximal voluntary ECC muscle contraction in vivo In contrast, the V-wave (H-reflex induced by maximal nerve stimulation) was not different between maximal ECC, CON and ISO contraction Maximal plantarflexor contractions Soleus muscle, ankle joint angular velocity: 3 o /sec Duclay & Martin, J Neurophysiol 25 11
12 H-reflex recording during maximal ECC contraction isometric CONcentric ECCentric H max H max H max Suggesting that maximal ECC contraction M max M max M... does not involve reduced descending max cortical drive [ V-wave responses ]... but may involve spinal inhibition via via preferential presynaptic inhibition of small sized motor neurons (typically innervating type I fibers) [ V vs H responses ] The H-reflex appears to be markedly suppressed during maximal voluntary ECC muscle contraction in vivo In contrast, the V-wave (H-reflex induced by maximal nerve stimulation) was not different between maximal ECC, CON and ISO contraction Maximal plantarflexor contractions Soleus muscle, ankle joint angular velocity: 3 o /sec Duclay & Martin, J Neurophysiol 25 Modulations in corticospinal excitability TMS Transcranial Magnetic Stimulation (TMS) MEP Duclay, Duchateau et al, J Physiol
13 ECC ISO CON Duclay, Duchateau et al, J Physiol 211 Evoked TMS (MEP) and H-reflex responses ECCentric ISOmetric CONcentric SOLEUS SOL MEP SOL H-reflex 3% MVC % MVC MG MEP MEDIAL GASTROCNEMIUS MG H-reflex 3% MVC % MVC Duclay, Duchateau et al, J Physiol 211 Evoked TMS responses (3% MVC) Duclay, Duchateau et al, J Physiol 211 from Duchateau & Baudry, J Appl Physiol
14 M M H Evoked H-reflex responses (% MVC) SOLEUS MEDIAL GASTROCNEMIUS CON ISO ECC Duclay, Duchateau et al, J Physiol 211 Taylor & Gandevia, J Appl Physiol 24 Gruber, Avela et al, J Neurophysiol 29 Evoked motor potential (MEP or CMEP) Gruber, Avela et al, J Neurophysiol 29 14
15 Maximal M wave (M max) ISOMETRIC ECCENTRIC Gruber et al, J Neurophysiol 29 CMEP Cervicomedullary stimulation (CMS) ECC vs ISO contractions: MEP MEP, CMEP responses Transcranial stimulation (TMS) ECC contractions: MEP and CMEP responses but MEP / CMEP ratio... ISO ECC ISO ECC MEP/CMEP: ECC > ISO (p <.5) Gruber, Avela et al, J Neurophysiol 29 "... In conclusion... the responsiveness of [spinal] motoneurons was reduced [...] in lengthening compared with isometric contractions, indicating inhibition of spinal motoneurons..." "... The observed reduction in CMEPs indicates that spinal excitability was considerably lower in lengthening than isometric contractions, whereas a moderate increase in MEP/CMEP ratio indicates that cortical excitability was slightly higher..." "... We suggest that increased cortical excitability results in extra excitatory descending drive during muscle lengthening to compensate for spinal inhibition..." "... This indicates changes in neural control of muscle activity for both spinal and cortical sites in lengthening compared with isometric contractions..." Gruber et al, J Neurophysiol 29 15
16 n nt Neuromuscular activity during maximal eccentric muscle contraction L surface EMG amplitude (iemg, aemg) H-reflex response M MEP, CMEP responses (TMS, CMS) [unchanged or elevated MEP/CMEP ratio] F Neuromuscular activation appears to be reduced during maximal voluntary ECCentric muscle contraction, indicating that motoneuron activation is suppressed (untrained subjects) Aagaard 2, Andersen 25, McHugh 22, Komi 2, Kellis & Baltzopoulos 1998, Higbie 1996, Amiridis 1996, Seger & Thorstensson 1994, Bobbert & Harlaard 1992, Westing 1991, Tesch 199, Eloranta & Komi 19, Duclay & Martin 25, Duclay et al 28, Gruber 29, Abbruzzese 1994, Sekiguchi 21, 23 Effects of training? Heavy-resistance strength training (14 wks) Reduced suppression in quadriceps EMG amplitude during ECC contraction Reflecting downregulated quadriceps motoneuron inhibition Percent quadriceps force moment percent 2 Average quadriceps EMG and strength Percent Percent Percent EMG VL percent EMG VM percent EMG RF percent Percent Percent Quadriceps force moment (percent) mean EMG Quadriceps (percent) -24 eccentric -3 3 concentric 24 Knee angular velocity ( o s -1 ) -24 eccentric -3 3 concentric 24 Knee angular velocity ( o s -1 ) Aagaard et al, J Appl Physiol 2 16
17 Neuromuscular activity during maximal ECCentric muscle contraction - effects of resistance training R 2 =.77, p<.1 % slow ECC ecc Torque moment at of 3 o force /s r =.89, p< % ECC slow norm ecc norm EMG EMG at 3 o /s The gain in maximal ECC muscle strength evoked by months of heavy resistance training is positively related to the concurrent improvement in neuromuscular activity (r=.89, p <.1) Andersen, Aagaard et al. 25 tion ment G VL G VM pre training Neuromuscular activity during maximal ECCentric muscle contraction Effects of heavy-resistance strength training - increased neuromuscular activity during max ECC contraction ( iemg for VL,VM,RF; H,V waves for SOL,GM) - reduced suppression in neuromuscular activity during maximal ECC vs CON contraction increased maximal ECC muscle strength G RF Aagaard et al 2, Andersen et al 25 Effects of heavy-resistance strength training on maximal ECC muscle strength Quadriceps muscle strength, Elite Soccer Players Before and after 12 weeks strength training Moment of Force (Nm) eccentric velocity of training knee angular velocity ( o s -1 ) Heavy-resistance HR group (n=7) strength training (8 RM loads) 5 o concentric peak Aagaard et al, Acta Physiol Scand
18 Effects of strength/resistance training on maximal ECC muscle strength Heavy-resistance strength training CONC strength, ECC strength Andersen 25, Aagaard 2, Seger 1998, Aagaard 1996, Hortobagyi 1996, Higbie 1996, Colliander & Tesch 199, Narici 1989, Komi & Buskirk 1972 No or only minor changes in maximal eccentric muscle strength following low-resistance strength training Aagaard 1996, Duncan 1989, Takarada 2, Holm Aagaard et al 28 Neuromuscular activity during maximal ECCentric muscle contraction Effects of heavy-resistance strength training - increased neuromuscular activity during max ECC contraction ( iemg for VL,VM,RF; H,V waves for SOL,GM) - reduced suppression in neuromuscular activity during maximal ECC vs CON contraction increased maximal ECC muscle strength Functional consequences??? Neuromuscular activity during maximal ECCentric muscle contraction Effects of heavy-resistance strength training - increased neuromuscular activity during max ECC contraction ( iemg for VL,VM,RF; H,V waves for SOL,GM) - reduced suppression in neuromuscular activity during maximal ECC vs CON contraction increased maximal ECC muscle strength Functional consequences - faster SSC muscle actions - faster decelerations (side cutting etc) - ECC antagonist muscle strength: (joint protection, reduced risk of injury) 18
19 Neuromuscular activity during maximal ECCentric muscle contraction Effects of heavy-resistance strength training - increased neuromuscular activity during max ECC contraction ( iemg for VL,VM,RF; H,V waves for SOL,GM) - reduced suppression in neuromuscular activity during maximal ECC vs CON contraction increased maximal ECC muscle strength Functional consequences - faster SSC muscle actions - faster decelerations (side cutting etc) - ECC antagonist muscle strength: (joint protection, reduced risk of injury) Neuromuscular activity during maximal ECCentric muscle contraction Effects of heavy-resistance strength training - increased neuromuscular activity during max ECC contraction ( iemg for VL,VM,RF; H,V waves for SOL,GM) - reduced suppression in neuromuscular activity during maximal ECC vs CON contraction increased maximal ECC muscle strength Possible adaptation mechanisms??? Spinal neurocircuitry plasticity potential role in maximal ECCentric muscle contraction Potential adaptation with resistance training... Bawa, Exercise Sports Science Reviews 22 19
20 Altered inhibitory force feedback? Golgi organs potential role in maximal ECCentric muscle contraction Potential adaptation with resistance training... Inhibitory Ib interneuron activity may be downregulated... is under inhibitory control from reticulospinal pathways descending from the brain Bawa, Exercise Sports Science Reviews 22 Altered excitatory force feedback? Muscle spindles potential role in maximal ECCentric muscle contraction Potential adaptation with resistance training... Ia afferent input Pre-synaptic inhibition of spinal MN s may be down-regulated... by means of reduced presynaptic inhibition of primary muscle spindle Ia afferents Muscle spindles Bawa, Exercise Sports Science Reviews 22 Altered autogenic inhibition? Renshaw cells potential role in maximal ECCentric muscle contraction Potential adaptation with resistance training... Reccurent inhibition via Renshaw cells may be down-regulated... receives inhibitory and excitatory descending inputs from cortical centers Bawa, Exercise Sports Science Reviews 22 2
21 Elevated H-reflex and V-wave amplitudes during max ECC contraction following 7 wks of eccentric (ECC) plantar flexor strength training H max at rest Soleus H max at rest Gastroc med ECC < ISO, CON # PRE < MID, POST PRE < POST PRE MID POST ECC ISO CON H-reflex amplitude at MVC ECC ISO CON H-reflex amplitude at MVC ECC ISO CON ECC ISO CON V-wave amplitude at MVC ECC ISO CON ECC ISO CON V-wave amplitude at MVC Duclay, Martin et al, Med Sci Sports Exerc 28 Neural adaptation to ECC resistance training Elevated H-reflex and V-wave amplitudes during maximal ECC contraction following 7 wks of eccentric (ECC) plantar flexor strength training Substantial depression in Soleus and Gastrocnemius medialis H- reflex (but not and V-wave) amplitudes were present during maximal ECC contraction prior to training. This depression ('inhibition') was removed by 7 wks of ECC strength training, since elevated H and V responses were observed during ECC contraction after training. Conclusion: max ECC muscle strength caused by elevated volitional descending neural drive from cortical centers + neural adaptation mechanisms acting at the spinal level (increased MN excitability, reduced presynaptic inhibition)... Duclay, Martin et al, Med Sci Sports Exerc 28 SUMMARY Main spinal networks likely to modulate motorneurone excitability during ECC muscle contractions Duchateau & Enoka J Exp Biol 216 Muscle 21
22 SUMMARY Main spinal networks likely to modulate motorneurone excitability during ECC muscle contractions Potential adaptative mechanisms evoked by resistance training: - presynaptic inhibition - recurrent inhibition - inflow Ib inhibitory interneurons Duchateau & Enoka J Exp Biol 216 Muscle VM position Moment OVERALL CONCLUSIONS EMG VL RF EMG VM position Nm EMG RF Moment 'dampening' function low muscle stiffness EMG VL Heavy-resistance -3 strength training EMG VM ECC muscle strength Enhanced Time 'rebound' (msec) function Increased muscle stiffness EMG RF VM OVERALL CONCLUSIONS RF Distinct activation patterns exists in the brain for ECC vs CONC contractions Neural inhibition/suppression exists in the CNS in ECC vs CONC contraction Time MU (msec) firing frequency is reduced in ECC vs CONC contractions (submax, max) Central Activation during MVC estimated by superimposed twitch interpolation appears reduced in ECC vs CONC contractions Sites of inhibition: spinal rather than cortical, likely involving post-synaptic as well as pre-synaptic inhibitory mechanisms Motorneuron inhibition/suppression during ECC contractions can be modified (reduced/removed) by means of heavy-resistance strength training Functional consequences: muscular stiffness SCC Force/Power/RFD 22
23 G VL G VM Acknowledgements Coworkers at Institute of Sports Medicine Copenhagen, University of Copenhagen; Institute of Sports Science and Clinical Biomechanics, University of Southern Denmark: G RF Poul Dyhre-Poulsen Erik B. Simonsen Paolo Caserotti Lars L. Andersen Jens Bojsen-Møller Peter Magnusson Jesper L. Andersen Michael Kjær Charlotte Suetta Jonas Thorlund Aagaard et al., J. Appl. Physiol. 2 23
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