1 Neural control of eccentric contractions Why is neural modulation - - PDF document

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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 Biomechanics of Human Movement: Mechanisms and Methods 17th International Symposium  Neuromuscular Research Center (NMRC)  University of Jyväskylä

Types of muscle contraction

Eccentric muscle contraction

muscle generating contractile force while lengthening

Concentric muscle contraction

muscle generating contractile force while shortening

Isometric muscle contraction

muscle generating contractile force while maintaining constant length

Eccentric Concentric Isometric

Neural control of eccentric contractions

Why is ECC strength important?

In some sports very high eccentric muscle strength is a prerequisite for superior athletic performance...

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Neural control of eccentric contractions

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

Joyce, Rack, Westbury, J Physiol 204, 1969 Cat soleus, ventral nerve root stimulation in situ

Neural control of eccentric contractions

Why is neural modulation important?

Joyce, Rack, Westbury, J Physiol 204, 1969 Cat soleus, ventral nerve root stimulation in situ

Neural control of eccentric contractions

Why is neural modulation important?

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Neural input from the CNS to myofibers determines the stiffness behavior of the muscle: ► high-stiffness 'rebound' profile

• r

► compliant 'dampening' profile Neural control of eccentric contractions

Why is neural modulation important?

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Neural control of eccentric contractions

Expression of maximal ECC muscle strength in vivo

50 100 150 200 250 300 350 10 20 30 40 50 60 70 80

Moment of Force (Nm) K n e e j

• i

n t a n g l e

(

• )

Angular velocity ( o s-1 )

• 240
• 30 30

240

C O N C E C C



Contraction Speed

percent of Vmax

• 40
• 20

20 40 60 80 100 20 40 60 80 100 120 140 160 180 20 40 60 80 100 120 140 160 180 concentric eccentric

Contraction Speed

isometric concentric eccentric

Katz B, J. Physiol. 96, 1939 Edman KAP, J. Physiol. 404, 1988

Human quadriceps muscle, electrical muscle stimulation superimposed onto maximal voluntary contraction

(Westing et al 1990)

Muscle Force (isometric = 100%) Muscle Force (isometric = 100%)

Contractile characteristics of skeletal muscle during maximal ECC and CON contraction

From Aagaard & Thorstensson. Neuromuscular aspects of exercise: Adaptive responses evoked by strength training, Textbook of Sports Medicine (Eds. Kjær et al) 2003 Knee Angular Velocity (o/s) SEDENTARY subjects Knee Angular Velocity (o/s) eccentric concentric eccentric concentric STRENGTH TRAINED subjects

Knee Extensor torque Knee Extensor torque

Increased electrically superimposed muscle torques only observed in untrained individuals, not in strength trained athletes...

Amiridis, Martin, Van Hoecke et al, Eur J Appl Physiol 1996

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( o/sec) concentric eccentric

Moment of Force 240

Angular velocity

30

• 30
• 240

100 200 300 400 500

based on peak Moment based on peak Moment highly strength trained athlete (alpine skiier) sedentary subject of similar age and body mass max ECC strength

(Nm)

Expression of maximal ECCentric and CONcentric muscle strength in vivo

Aagaard, unpubl. data Team Danmark Testcenter

Maximal ECC and CONC quadriceps contraction strength (elite alpine skier)

Neural control of eccentric contractions

Surface EMG recording

Segmented EMG patterns (burst behavior) typically is observed during slow submaximal ECC muscle contraction

• 600
• 300

Vast Med knee angle Time (miliseconds) degrees uVolt

• 800
• 400

Vast Lat

eccentric phase

Neuromuscular activity during ECC contractions

concentric phase

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Segmented EMG patterns (burst behavior) typically is observed during slow submaximal ECC muscle contraction

Neuromuscular activity during ECC contractions How is it possible to evaluate neuromuscular activity during maximal ECC muscle contractions? Isokinetic dynamometry and muscle electromyography (EMG) recording

100 Nm

• 2500

2500 3000

• 3000
• 4000

4000

position Moment EMG VL EMG VM EMG RF

Time (msec)

1000 2000 3000 4000 5000 uVolt uVolt uVolt

Reduced neuromuscular activity ( EMG amplitude) during maximal ECC versus CON quadriceps contraction

Westing et al 1991

• 2500

2500 3000

• 3000
• 4000

4000

EMG VL EMG VM EMG RF

Time (msec)

1000 2000 3000 4000 5000 uVolt uVolt uVolt

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Komi et al, Med Sci Sports Exerc 32, 2000

Reduced neuromuscular activity ( EMG amplitude) during maximal ECC versus CON quadriceps contraction

100 Nm

• 2500

2500 3000

• 3000
• 4000

4000

position Moment EMG VL EMG VM EMG RF

Time (msec)

1000 2000 3000 4000 5000 uVolt uVolt uVolt

Time (msec)

1000 2000 3000 4000 5000 Aagaard et al, J Appl Physiol 2000 90o 10o 90o 10o

Neuromuscular activity m. quadriceps

Calculating mean filtered EMG amplitude (iEMG) Calculating mean filtered EMG amplitude (iEMG)

slow CONC contraction

pre training

slow ECC contraction

pre training

Suppressed quadriceps EMG activity during maximal ECC contraction

* * * * * * * * * *

percent EMG RF EMG VM EMG VL Knee angular velocity

Percent

Percent

Percent

concentric eccentric 100 120 140 160 180 200 240

Percent

• 30
• 240

force moment quadriceps percent percent percent

Average quadriceps EMG and strength

* * * * * *

mean EMG Quadriceps Knee angular velocity

Percent concentric eccentric

240

Percent

( o s-1 ) 30

• 30
• 240

Quadriceps force moment (percent) (percent)

* * *

fast ECC slow slow CONC fast

Aagaard et al, J Appl Physiol 2000

8

50 100 150 200 250 300 350 10 20 30 40 50 60 70 80

Moment of Force (Nm) Knee joint angle

(

• )

Angular velocity ( o s-1 )

• 240
• 30 30

240

CONC ECC

100 200 300 400 500 600 700 10 20 30 40 50 60 70 80

vastus lateralis EMG (V) Knee joint angle

(

• )

Angular velocity ( o s-1 )

• 240
• 30 30

240

CONC ECC

Quadriceps muscle activity (EMG amplitude) varies with contraction mode (CON vs ECC) and knee joint angle

(n=14) Aagaard et al, J Appl Physiol 2000

50 100 150 200 250 300 350 10 20 30 40 50 60 70 80

Moment of Force (Nm) Knee joint angle ( o ) Angular velocity ( o s-1 )

• 240
• 30 30

240

C O N C E C C

100 200 300 400 500 600 700 10 20 30 40 50 60 70 80

vastus lateralis EMG (V) Knee joint angle ( o ) Angular velocity ( o s-1 )

• 240
• 30 30

240

C O N C E C C (n=14)

Quadriceps muscle activity (EMG) is reduced in the high-force region of the F-V relationship

Aagaard et al, J Appl Physiol 2000

50 100 150 200 250 300 350 10 20 30 40 50 60 70 80

Moment of Force (Nm) K n e e j

• i

n t a n g l e ( o ) Angular velocity ( o s-1 )

• 240
• 30 30

240

C O N C E C C

100 200 300 400 500 600 700 10 20 30 40 50 60 70 80

vastus lateralis EMG (V) K n e e j

• i

n t a n g l e ( o ) Angular velocity ( o s-1 )

• 240
• 30 30

240

C O N C E C C (n=14)

In contrast, quadriceps muscle activity is not reduced in the low-force region of the F-V relationship

Aagaard et al, J Appl Physiol 2000

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50 100 150 200 250 300 350 10 20 30 40 50 60 70 80

Moment of Force (Nm) K n e e j

• i

n t a n g l e ( o ) Angular velocity ( o s-1 )

• 240
• 30 30

240

C O N C E C C

100 200 300 400 500 600 700 10 20 30 40 50 60 70 80

vastus lateralis EMG (V) K n e e j

• i

n t a n g l e ( o ) Angular velocity ( o s-1 )

• 240
• 30 30

240

C O N C E C C (n=14)

In contrast, quadriceps muscle activity is not reduced in the low-force region of the F-V relationship

Aagaard et al, J Appl Physiol 2000

Indicating that neuromuscular activity during maximal ECC muscle force production in vivo is mainly influenced by negative force-feedback mechanism(s) Neural control of eccentric contractions

Central activation - interpolated twitch analysis

ECC CONC Isometric CONcentric ECCentric

Reduced central activation during maximal eccentric muscle contraction in vivo?

Beltman, De Haan et al, J Appl Physiol 2004

• m. quadriceps femoris, maximal voluntary contraction efforts

superimposed stimulation (triplet, 300 Hz) femoral nerve Regularly active subjects ~6 h per wk (28±8 yrs, n=10)

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ECCentric Beltman, De Haan et al, J Appl Physiol 2004

• m. quadriceps femoris, maximal voluntary contraction efforts

Regularly active subjects ~6 h per wk (28±8 yrs, n=10)

100 90 80 70 60 Isometric Con Ecc

*

79 ± 8 % 92 ± 5 % 93 ± 5 %

Reduced central activation during maximal eccentric muscle contraction in vivo? A: yes!

Neural control of eccentric contractions

Spinal motorneuron excitability assessed by evoked spinal motorneuron recording

Brain motor cortex cerebellum Spinal cord Muscle

spinal motor neurons

The H-reflex: electric stimulus is applied to Ia afferent axons  evoked efferent motoneuron response (H-reflex)

The H-reflex

Hoffmann reflex

EMG amplifier Stimulator

Muscle Spinal cord

EMG recording electrodes Stimulus electrode

Sensory Ia afferent axon -motoneuron axon -motorneuron

Spinal motor neurons

Aagaard et al, J Appl Physiol 92, 2002 H M

10 ms 2 mV

H

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The H-reflex

Hoffmann reflex

EMG amplifier Stimulator

Muscle Spinal cord

EMG recording electrodes Stimulus electrode

Sensory Ia afferent axon -motoneuron axon -motorneuron

Spinal motor neurons

Aagaard et al, J Appl Physiol 92, 2002

H

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

H

H M

10 ms 2 mV

H-reflex recording during maximal ECC contraction

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 Hmax Hmax Hmax isometric CONcentric ECCentric Mmax Mmax Mmax Maximal plantarflexor contractions Soleus muscle, ankle joint angular velocity: 30 o/sec Duclay & Martin, J Neurophysiol 2005

H-reflex recording during maximal ECC contraction

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

Hmax Hmax Hmax isometric CONcentric ECCentric Mmax Mmax Mmax Maximal plantarflexor contractions Soleus muscle, ankle joint angular velocity: 30 o/sec Duclay & Martin, J Neurophysiol 2005

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H-reflex recording during maximal ECC contraction

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

Hmax Hmax Hmax isometric CONcentric ECCentric Mmax Mmax Mmax Maximal plantarflexor contractions Soleus muscle, ankle joint angular velocity: 30 o/sec Duclay & Martin, J Neurophysiol 2005

Suggesting that maximal ECC contraction ... does not involve reduced descending cortical drive [ V-wave responses ] ... but may involve spinal inhibition via via preferential presynaptic inhibition

• f small sized motor neurons (typically

innervating type I fibers) [ V vs H responses ]

Neural control of eccentric contractions

Modulations in corticospinal excitability

TMS MEP

Transcranial Magnetic Stimulation (TMS)

Duclay, Duchateau et al, J Physiol 2011

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Duclay, Duchateau et al, J Physiol 2011 ECC ISO CON

Evoked TMS (MEP) and H-reflex responses

↓ ↓

ECCentric ISOmetric CONcentric

SOL MEP SOL H-reflex MG MEP MG H-reflex

30% MVC 30% MVC 100% MVC 100% MVC SOLEUS MEDIAL GASTROCNEMIUS Duclay, Duchateau et al, J Physiol 2011 from Duchateau & Baudry, J Appl Physiol 2013

Evoked TMS responses (30% MVC)

Duclay, Duchateau et al, J Physiol 2011

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Evoked H-reflex responses (100% MVC)

SOLEUS MEDIAL GASTROCNEMIUS Duclay, Duchateau et al, J Physiol 2011

CON ISO ECC

H M

Gruber, Avela et al, J Neurophysiol 2009 Taylor & Gandevia, J Appl Physiol 2004 Evoked motor potential

(MEP or CMEP)

Gruber, Avela et al, J Neurophysiol 2009

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Gruber et al, J Neurophysiol 2009 CMEP MEP Cervicomedullary stimulation (CMS) Transcranial stimulation (TMS) Maximal M wave (Mmax) ISOMETRIC ECCENTRIC

ECC vs ISO contractions: ↓ MEP, ↓ CMEP responses ↓ ↓

ISO ECC ISO ECC

ECC contractions:  MEP and CMEP responses but  MEP / CMEP ratio...

* MEP/CMEP: ECC > ISO (p < 0.05)

* *

Gruber, Avela et al, J Neurophysiol 2009

" ... 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 2009

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Neuromuscular activation appears to be reduced during maximal voluntary ECCentric muscle contraction, indicating that motoneuron activation is suppressed (untrained subjects)

Aagaard 2000, Andersen 2005, McHugh 2002, Komi 2000, Kellis & Baltzopoulos 1998, Higbie 1996, Amiridis 1996, Seger & Thorstensson 1994, Bobbert & Harlaard 1992, Westing 1991, Tesch 1990, Eloranta & Komi 1980, Duclay & Martin 2005, Duclay et al 2008, Gruber 2009, Abbruzzese 1994, Sekiguchi 2001, 2003

Neuromuscular activity during maximal eccentric muscle contraction  surface EMG amplitude (iEMG, aEMG)  H-reflex response  MEP,  CMEP responses (TMS, CMS)

[unchanged or elevated MEP/CMEP ratio]

Neural control of eccentric contractions

Effects of training?

* * * * * * * * * *

percent EMG RF EMG VM EMG VL Knee angular velocity

Percent

Percent

Percent

concentric eccentric 100 120 140 160 180 200 240

Percent

• 30
• 240

force moment quadriceps percent percent percent

* * * * * *

mean EMG Quadriceps Knee angular velocity

Percent concentric eccentric

240

Percent

( o s-1 ) 30

• 30
• 240

Quadriceps force moment (percent) (percent)

* * *

Average quadriceps EMG and strength

Reflecting down- regulated quadriceps motoneuron inhibition

Aagaard et al, J Appl Physiol 2000

Heavy-resistance strength training (14 wks)  Reduced suppression in quadriceps EMG amplitude during ECC contraction

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Neuromuscular activity during maximal ECCentric muscle contraction

• effects of resistance training

 slow ecc norm EMG

20 40 60 80 100 120 140

 slow ecc moment of force

20 40 60 80 100 120 R2 = 0.77, p<0.001

 % ECC norm EMG at 30o/s  % ECC Torque at 30o/s

r = 0.89, p<0.001

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=0.89, p < 0.001)

Andersen, Aagaard et al. 2005

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

Neuromuscular activity during maximal ECCentric muscle contraction

Aagaard et al 2000, Andersen et al 2005

Moment of Force (Nm)

knee angular velocity ( o

• 120

240 120 30

• 30
• 240

100 200 300 400

velocity of training

50o peak * * * * ** ** **

eccentric concentric

HR group (n=7)

*

Quadriceps muscle strength, Elite Soccer Players Before and after 12 weeks strength training

Aagaard et al, Acta Physiol Scand 1996

Heavy-resistance strength training

(8 RM loads)

Effects of heavy-resistance strength training

• n maximal ECC muscle strength



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Effects of strength/resistance training

• n maximal ECC muscle strength

Heavy-resistance strength training   CONC strength,  ECC strength

Andersen 2005, Aagaard 2000, Seger 1998, Aagaard 1996, Hortobagyi 1996, Higbie 1996, Colliander & Tesch 1990, 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 2000, Holm Aagaard et al 2008



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

Neuromuscular activity during maximal ECCentric muscle contraction

???

Functional consequences 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

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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

Neuromuscular activity during maximal ECCentric muscle contraction

Functional consequences

• faster SSC muscle actions
• faster decelerations (side cutting etc)
•  ECC antagonist muscle strength:

(joint protection, reduced risk of injury)

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

Neuromuscular activity during maximal ECCentric muscle contraction

???

Possible adaptation mechanisms

Bawa, Exercise Sports Science Reviews 2002

Spinal neurocircuitry plasticity

potential role in maximal ECCentric muscle contraction



Potential adaptation with resistance training...

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Bawa, Exercise Sports Science Reviews 2002

Altered inhibitory force feedback? Golgi organs

potential role in maximal ECCentric muscle contraction

Inhibitory Ib interneuron activity may be down- regulated

... is under inhibitory control from reticulospinal pathways descending from the brain



Potential adaptation with resistance training...

Pre-synaptic inhibition

• f spinal MN’s may be

down-regulated

... by means of reduced presynaptic inhibition

• f primary muscle spindle Ia

afferents

Muscle spindles Ia afferent input Bawa, Exercise Sports Science Reviews 2002

Altered excitatory force feedback? Muscle spindles

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 2002

Altered autogenic inhibition? Renshaw cells

potential role in maximal ECCentric muscle contraction



Potential adaptation with resistance training...

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Soleus Gastroc med

Hmax at rest Hmax at rest H-reflex amplitude at MVC H-reflex amplitude at MVC V-wave amplitude at MVC V-wave amplitude at MVC ECC ISO CON ECC ISO CON ECC ISO CON ECC ISO CON ECC ISO CON ECC ISO CON Duclay, Martin et al, Med Sci Sports Exerc 2008

* ECC < ISO, CON # PRE < MID, POST § PRE < POST PRE MID POST

Elevated H-reflex and V-wave amplitudes during max 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

• bserved 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 2008

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

SUMMARY Main spinal networks likely to modulate motorneurone excitability during ECC muscle contractions

Muscle Duchateau & Enoka J Exp Biol 2016

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Muscle Duchateau & Enoka J Exp Biol 2016

Potential adaptative mechanisms evoked by resistance training:

•  presynaptic inhibition
•  recurrent inhibition
•  inflow Ib inhibitory

interneurons

SUMMARY Main spinal networks likely to modulate motorneurone excitability during ECC muscle contractions Neural control of eccentric contractions

OVERALL CONCLUSIONS

'dampening' function low muscle stiffness  ECC muscle strength Enhanced 'rebound' function Increased muscle stiffness

Heavy-resistance strength training

Neural control of eccentric contractions

OVERALL CONCLUSIONS

► Distinct activation patterns exists in the brain for ECC vs CONC contractions ► Neural inhibition/suppression exists in the CNS in ECC vs CONC contraction ► MU 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

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Acknowledgements

Coworkers at Institute of Sports Medicine Copenhagen, University of Copenhagen; Institute of Sports Science and Clinical Biomechanics, University of Southern Denmark: 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