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Introduction

he effects of contractile strengthtraining have been investigated alarge variety of training designs. The

purpose of the studies has been to betterunderstand the adaptive mechanisms of thehuman movement system to physical activity.In principle, two modalities of functional

adaptations can be substantiated for classicalstrength training: strength training can eitherlead to enhancements in the contractile mus-cular properties of the protein structuresthemselves or it can lead to improvements inthe neural supply to the contracting muscleor muscle group. The two types of adaptationcan be addressed specifically by the design ofthe training programme using variations inthe level of the training load, the volume oftraining session and the duration.

Evidence has been produced that trainingwith a relatively high number of repetitionswithin one set (i.e. 6-15 RM (maximum rep-etition) load), which is associated with anextensive exhaustion of the trained musclegroup, is followed by an enhancement instrength and power. Athletes working withthis method show adaptations in the mus-cular tissue, enhanced cross-sectional areas,altered pinnation angles and high endocrineinvolvement (RUTHERFORD, JONES 1992;WALKER ET AL 1998). However, many stud-ies also report improvements in strength and

by IAAF

22:1; 23-30, 2007Adaptive responses of the neuromuscular system to trainingBy Albert Gollhofer

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The author is head of the Instituteof Sport Science at the Universityof Freiburg in Germany. He is apast president of the GermanySociety of Biomechanics and since2005 is the president of the Euro-pean College of Sport Science.

Strength training leads to func-tional adaptations of the muscu-lo-skeletal and the neuromuscularsystems. The properties of muscu-lar activation can be changed to alarge extent depending on thetype of strength training. For ath-letic performance the power ofmuscular action is often muchmore important than the maxi-mum force capacity. Recognizingthis aspect is necessary in order tofind the best training parameters. Sensorimotor training has provento be highly effective, with respectto considerable improvements inmuscle power, as well as toenhanced postural control. Forteam sports the improvement inpostural control is very effectivefor the reduction of injuries to thelower extremities. In the present paper, the focus ison the physiological pathwaysthat explain the functional adap-tations of power strength training,in order to give coaches and ath-letes explanations why sensori-motor training can be beneficialfor enhanced rate of force devel-opment capabilities.

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power capabilities after strength trainingwithout a substantial adaptation of the mus-cular profile. Thus, an alternative functionalresponse modality must be considered.Recent publications have given evidence thata specific type of training can enhance spinaland supraspinal mechanisms. In contrast tothe muscular adaptations after training witha high number of RMs, neuronal adaptation isassociated with training using a low numberof repetitions (1-8 RM load), high loads, in-tensive or explosive types of contraction andsufficiently long periods between sets(AAGAARD ET AL 2001).

The present paper focuses on the neuro-muscular adaptive mechanisms that mayresult from intensive strength training andsensorimotor training.

The motoneurons in the spinal cord is inlatest consequence directly linked to themuscle fibres. Due to the fact that the func-tional properties of the motor units (MU) aredirectly dependent on the discharge charac-teristics of the activating spinal motoneu-rons, it appears logical to separate the vari-ous adaptive responses of the neuromuscularsystem to training in accordance to the dif-ferent modalities of training.

Increased muscle activation

Increased muscle activation can beachieved by a) alterations in the recruitment

properties of activated motoneurons or b) thefiring frequency or the motor synchronisationor c) a combination of these three modalities.

EMG (electromyography) studies clearlydemonstrate that vigorous intensive strengthtraining is quite often associated with anenhanced EMG input to the trained muscle.Despite the methodological limitation of thisapproach, a number of studies have consis-tently shown that neural adaptation canaccount for the observed gains in strength(NARICI ET AL 1989; MORITANI, DEVRIES,1979; HAKKINEN ET AL 1985A; HAKKINEN ETAL 1985B; HAKKINEN ET AL 1987)

From a functional point of view, the adap-tation in the RFD (rate of force development)is much more often required after strengthtraining than enhanced MVC (maximumforces). From the dynamic, explosive type ofstrength training in particular it is knownthat an increase in RFD is closely related toimprovements in the neural drive of thetrained muscles (JANSSON ET AL 1990; GRU-BER, GOLLHOFER 2004). It has been shownthat neural adaptations caused by an explo-sive type of training are primarily responsiblefor an increase in the speed of voluntarymuscle contraction. By analysing singlemotor unit recordings, the authors were ableto demonstrate the preservation of an order-ly motor unit recruitment pattern. However,MUs were activated earlier and showedincreased firing frequencies after training.

Figure 1: Neuronal adaptations to strength training can be achieved either by enhanced activation of the agonistic mus-cles, by appropriate coordination of the synergists or by functional decreased activation of the antagonistic muscles(modified from SALE 2002).

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From intramuscular EMG recordings, there issupport for the idea that the explosive type oftraining is associated with high frequencydischarges occurring at the onset of muscu-lar action (VAN CUTSEM ET AL 1998). In thelatter study, the subjects trained ballistic dor-

siflexion actions with 30 to 40% of 1 RMover a period of 12 weeks. After training theRFD was drastically (+80%) enhanced, main-ly due to increased firing rates at the begin-ning of the isometric test action. From singlemotor recordings, the authors could demon-

Figure 2: Isometric strength training over four weeks of training was associated with a substantial enhancement of strengthand a muscle specific neural adaptation, obtained from surface EMG recordings. (modified from RABITA ET AL 2000)

Figure 3: Isometric strength (% MVC) and recruitment of individual MUs in small and in large muscles. It is importantto note that both types of muscle are nearly fully activated at a level of 50% MVC (modified from ENOKA and FUGLE-VAND 2001)

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strate that the frequency of discharge at theearly onset was nearly doubled after thetraining. Functionally, the MUs learned toactivate with higher starting frequencies andthis led to enhanced rates of force develop-ment on the MU level.

Observations of a changed discharge fre-quency are mainly obtained from studiesinvestigating only a small number of singleMUs. Therefore, it is not clear if this type oftraining also alters the recruitment level oreven the recruitment order of the motoneu-rons involved. PATTEN ET AL (2000) demon-strated that ballistic training caused a slightshift in the recruitment threshold to the left,leading to an earlier recruitment of the MUs.However, the authors clearly state that theorder of recruitment was preserved, which isin accordance to findings from GARLAND ETAL (1996).

It is important to note that generally a nor-mal healthy subject should be able to recruit

all the MUs of a muscle during maximal iso-metric actions. Therefore, the only explana-tion of neural adaptation can be seen in theimproved firing rates after training. It is wellknown that in large muscles the recruitmentof MUs occurs up to 80% of MVC (ENOKA,FUGLEVAND 2001) whereas in small musclesthe recruitment is finished at 50% MVC.Thus, a large variety of force output can beaddressed by alterations in the firing patternof the MUs.

Spinal mechanisms activating themotoneurons

In Figure 4 the various inputs of the centralnervous system to the motoneuron of a dis-tinct muscle group are illustrated. Not onlydo motoneurons receive signals through thecentral pathways from brain structures, theyare also largely influenced by selective inputsfrom peripheral feedback afferents. Afferentinput from sensors in the skin, capsules, liga-ments, tendons and muscle are mediated

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Proprioceptive Feedback

Figure 4: Various sources of afferent influence of the spinal MU. Note that most of the feedbacks are inhibitory, reduc-ing the activation level of the motoneuron.

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either directly to the motoneuron or they areconnected via interneuronal structures. It isnoteworthy that most of the peripheral affer-ents are looped back, either facilitating orinhibiting the spinal motoneuron.

One of the most important feedback-loopsis the Ia-afferent from the muscle spindles.This reflex pathway directly facilitates thehomonymous MUs (i.e. extensors) and inhibitsthe antagonist muscle (i.e. flexors) of the ipsi-lateral side. On the contralateral side, theafferents are connected in the opposite man-ner, facilitating the flexors and inhibiting theextensors. On the other side, afferents fromIb-Golgi-Tendon-Units (GTO) generally inhibithomonymeous and facilitate antagonisticMUs. Influences from skin- and joint-recep-tors converge together with the Ia and Ibafferents into the Ib-interneuron pool. How-ever, in humans it has been shown that, espe-cially in stance and locomotion, the Ib-inhibi-tion is reversed into facilitation. This reflexpathway is dependent on the load acting onthe lower limb (GOLLHOFER ET AL 1989).Functionally this Ib-mechanism has beenaddressed as the load-receptor modulation.

From a functional point of view, the spinalnetwork of feedback represents the backboneof the neural adaptations resulting fromlearning and training. By modulations origi-nating from changed inputs from the brain aswell as from the sensors of the proprioceptivesystem, the input from the interneuron poolto the motoneurons, i.e. the activation of thelast common path to the muscle, can bedrastically adjusted to either the mechanicalneeds of a distinct movement or to the levelof experience and training of the individual.

Sensorimotor training

For rehabilitation of injuries to the locomo-tor system, sensorimotor training is widelybelieved to restore neuromuscular functions.The various receptors in the joint complexes,in the tendons and ligaments, in the musculerand skin structures are trained in order toenhance proprioceptive contributions infunctional situations. The aim is to improve

the efficacy of the afferent feedback in orderto attain functional limb control and achieveappropriate neuromuscular access to themuscles encompassing joint complexes. KON-RADSEN ET AL (1993) and TROPP (1986) com-pared postural stability of healthy subjectsand with individuals with chronic ankleinstability. Other approaches have investigat-ed the sensory angular reproduction of differ-ent joint dynamics under active or passiveconditions (FREEMAN ET AL 1965; GLICK ETAL 1976; LOFVENBERG ET AL 1995; TROPP,1986). These studies demonstrate a proprio-ceptive deficit during reproduction of distinctangular dynamics in cases of chronic ankleinstability.

Enhancement of proprioceptive generatedmuscle activation has been assumed fromexperiments of the knee (PERLAU ET AL 1995)and ankle joint (JEROSCH, BISCHOF 1994).However, only a few controlled studies areavailable demonstrating an improved afferentsupply to the muscles after training.

In a series of experiments, GOLLHOFERinvestigated the neuromuscular adaptationsfollowing sensorimotor training interven-tions. Based on longitudinal studies, theauthor presents experimental data thatdemonstrate the adaptability of the afferentand efferent contributions. In those studies,the hypothesis that a specifically designedsensorimotor training will have a positiveimpact on the neural activation and strengthduring a maximal isometric leg extension wasverified. GRUBER and GOLLHOFER (2004)investigated 12 female subjects before andafter a 4-week training programme with atotal of 8 training sessions. Each session (60min in duration) comprised various exercisesfor balance and body stabilisation. No classi-cal strength training exercises were allowedduring the entire training period. EMGs of theshank muscles as well as force parameters ofthe isometric maximum strength measure-ments revealed significantly increased neuro-muscular activation and isometric powerafter the training period. The sensorimotortraining produced the best neuromuscularadaptations at the initiation of the force pro-

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duction. Explosive strength and neuromuscu-lar activation at the onset of voluntaryactions seemed to be efficiently enhanced(see figure 5).

Increments in strength and in neural activa-tion reflect adaptive processes on themotoneuron level. From walking (SINKJAER ETAL 2000) and from voluntary ramp contrac-tions (MACEFIELD ET AL 1993) it has beenshown that afferent feedback is providedespecially at the onset of muscular action.MEUNIER and PIERROT-DESEILLIGNY (1989)

indicated that both homonymous and het-eronymous contributions of Ia afferents facili-tate muscular actions. From a functional pointof view, it must be pointed out that enhancedgain in neuromuscular control is of vitalimportance for stiffening of muscles encom-passing joint systems. Thus, it may be suggest-ed that sensorimotor training has a greatimpact on the proprioceptive supply of thetrained muscle. The enhancement has been in-terpreted as a modulation of the presynapticinhibition of the motoneuron. In contrast toclassical strength training, the increased RFD

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Figure 5: (A) Rate of force development (RFD) (means (SE)) in the time intervals of early force production before(open bars) and after (filled bars) the four-week sensorimotor training programme. (B) Mean activation amplitudes(MAV) (means (SE)) of the muscles vastus medialis (VM) and vastus lateralis (VL) before (open bars) and after (filledbars) the sensorimotor training. * P

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values were not associated with increasedmaximum strength (HAKKINEN ET AL 1998;AAGAARD ET AL 2002). Thus it may be assu-med, that sensorimotor training is beneficialfor an enhanced access of the neuromuscularsystem to the motoneuronpool, but not for anenhanced contractile force under maximumconditions.

The gain in neuromuscular activation mayarise from enhanced reflex contributions act-ing on a spinal level, induced by the training.

Conclusion

Neuromuscular adaptation is neitherunique in occurrence nor easy to identify.There are numerous possibilities for the neu-ral system to either facilitate or inhibit the

final motoneuron. On the basis of a largenumber of electromyographic studies, evi-dence has been produced indicating a highspecifity of the neural adaptation seen afterdifferent training regimen. Recently, addi-tional techniques have revealed detailedinsights into the mechanisms on the spinallevel. By means of H-reflex techniques, thedegree of presynaptic influences on themotoneuron excitability can be addressed. Bymeans of additional transcranial magneticstimulation (TMS), the central and peripheraladaptations following training can be distin-guished. In future, the various tools of elec-trophysiological methods need to be com-bined in order to examine changes in themotor cortex and spinal reflex pathways aswell as to explain changes in the motoneurondischarge properties.

AAGAARD, P.; ANDERSEN, J.L.; DYHRE-POULSEN, P.; LEFFERS, A.M.; WAGNER,A.; MAGNUSSON, S.P.; HALKJAER-KRIS-TENSEN, J.; SIMONSEN, E.B. (2001): Amechanism for increased contractilestrength of human pennate muscle inresponse to strength training: changes inmuscle architecture. J Physiol 534, 613-623.

AAGAARD, P.; SIMONSEN, E.B.; ANDERSEN,J.L.; MAGNUSSON, P.; DYHRE-POULSEN,P. (2002): Increased rate of force devel-opment and neural drive of human skele-tal muscle following resistance training.J Appl Physiol 93, 1318-1326.

ENOKA, R.M.; FUGLEVAND, A.J. (2001):Motor unit physiology: some unresolvedissues. Muscle Nerve 24, 4-17.

FREEMAN, M.A.; DEAN, M.R.; HANHAM, I.W.(1965): The etiology and prevention offunctional instability of the foot. J BoneJoint Surg Br 47, 678-685.

GARLAND, S.J.; COOKE, J.D.; MILLER, K.J.;OHTSUKI, T.; IVANOVA, T. (1996): Motorunit activity during human single jointmovements. J Neurophysiol 76, 1982-1990.

GLICK, J.M.; GORDON, R.B.; NISHIMOTO, D.(1976): The prevention and treatment ofankle injuries. Am J Sports Med 4, 136-141.

GOLLHOFER, A.; HORSTMANN, G.A.; BERGER,W.; DIETZ, V. (1989): Compensation oftranslational and rotational perturba-tions in human posture: stabilization ofthe center of gravity. Neuroscience let-ters105, 73-78.

GRUBER, M.; GOLLHOFER, A. (2004): Impactof sensorimotor training on the rate offorce development and neural activation.Eur J Appl Physiol 92, 98-105.

HAKKINEN, K.; ALEN, M.; KOMI, P.V. (1985a):Changes in isometric force- and relax-ation-time, electromyographic and mus-cle fibre characteristics of human skele-tal muscle during strength training anddetraining. Acta Physiol Scand 125, 573-585.

HAKKINEN, K.; KOMI, P.V.; ALEN, M. (1985b):Effect of explosive type strength trainingon isometric force- and relaxation-time,electromyographic and muscle fibrecharacteristics of leg extensor muscles.Acta Physiol Scand 125, 587-600.

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