Neural Adaptations to Resistance Training

Neural Adaptations to Resistance TrainingImplications for Movement Control

Timothy J. Carroll, Stephan Riek and Richard G. Carson

Perception and Motor Systems Laboratory, The School of Human Movement Studies, The University of Queensland, Brisbane, Queensland, Australia

Abstract It has long been believed that resistance training is accompanied by changeswithin the nervous system that play an important role in the development ofstrength. Many elements of the nervous system exhibit the potential for adaptationin response to resistance training, including supraspinal centres, descending neu-ral tracts, spinal circuitry and the motor end plate connections between motoneu-rons and muscle fibres. Yet the specific sites of adaptation along the neuraxis haveseldom been identified experimentally, and much of the evidence for neural ad-aptations following resistance training remains indirect. As a consequence of thiscurrent lack of knowledge, there exists uncertainty regarding the manner in whichresistance training impacts upon the control and execution of functional move-ments. We aim to demonstrate that resistance training is likely to cause adapta-tions to many neural elements that are involved in the control of movement, andis therefore likely to affect movement execution during a wide range of tasks.

We review a small number of experiments that provide evidence that resistancetraining affects the way in which muscles that have been engaged during trainingare recruited during related movement tasks. The concepts addressed in this ar-ticle represent an important new approach to research on the effects of resistancetraining. They are also of considerable practical importance, since most individ-uals perform resistance training in the expectation that it will enhance their per-formance in related functional tasks.

CURRENT OPINION Sports Med 2001; 31 (12): 829-8400112-1642/01/0012-0829/$22.00/0

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Muscular strength is fundamental to the suc-cessful and efficient performance of many tasksthat are encountered in daily living. Strength is de-fined as the capacity to exert force under a partic-ular set of biomechanical conditions. The amountof force that an isolated muscle can exert is influ-enced by factors such as: the number and size ofmuscle fibres, the orientation of fibres with respectto the line of muscle action, and the proportion ofmyosin heavy and light chain isoforms that are ex-

pressed within the muscle fibres.[1] However, in nat-ural tasks individual muscles are seldom requiredto generate force in isolation. Rather, most move-ments arise from the cooperation of a number ofmuscles acting together as functional synergists.The amount of force that can be generated in a par-ticular movement context is therefore determinednot only by intramuscular factors, but also by theeffectiveness of muscular coordination.

It is well documented in the literature that resis-

tance training can lead to increases in muscularstrength. There is a compelling body of evidencethat many of the physiological adaptations that un-derlie increments in strength occur within the mus-cles themselves.[1-3] It has long been believed thatresistance training is also accompanied by changeswithin the nervous system, that play an importantrole in the development of strength.[4,5-7] However,the specific sites of adaptation along the neuraxishave seldom been identified experimentally, andmuch of the evidence for neural adaptations fol-lowing resistance training remains indirect. For ex-ample, in a recent review, Enoka[5] identified phe-nomena such as strength changes in the absence ofsubstantial muscular adaptations, strength changesin the limb contralateral to the trained muscles (crosseducation), and specificity of strength adaptationsto the training movements, as the strongest evidencethat resistance training is accompanied by neuraladaptations.

While it is clear that intramuscular adaptationsinduced during a programme of resistance traininglead to strength increases by increasing the force-generating capacity of individual muscles, it is likelythat neural adaptations also contribute to strengthincrements by enhancing the effectiveness of mus-cular coordination.[8-10] That is, some of the adapta-tions associated with resistance training may be re-garded as motor learning, in so much as individualslearn to produce the specific patterns of muscle re-cruitment that are associated with optimal perfor-mance of the training tasks. At present, it is difficultto predict the impact that the physiological adapta-tions that underlie motor learning during resistancetraining will have upon the control and executionof functional tasks. However, in the present article,we aim to demonstrate that resistance training hasthe potential to alter the manner in which musclesthat have been recruited during training are con-trolled by the central nervous system (CNS). Wereview a small number of experiments that provideevidence that the changes that occur within the nerv-ous system in response to resistance training may

affect patterns of muscle recruitment within a va-riety of movement contexts.

1. Implications for Movement Control

It is well established that resistance training re-sults in greater increases in force-generating capac-ity in tasks that closely resemble the exercises per-formed during training than in novel tasks. That is,strength increases are somewhat specific to the tasksperformed during training.[11-13] Many researchershave inferred from this concept that some of theadaptations that cause strength increases have aneffect only on movements that are similar to thetraining tasks. However, while the principle of train-ing specificity suggests that the adaptations withinthe nervous system that underlie motor learning donot greatly contribute to increases in strength whennovel resistance training tasks are performed, it doesnot necessarily imply that the physiological changesassociated with motor learning do not affect themanner in which novel movements are controlledand executed.

When resistance training influences the execu-tion of another movement task the effect can be re-garded as a ‘transfer of learning’. Transfer occurswhen training for one task affects the performanceor learning of a subsequent task. Positive transfertakes place if training for the original task improvesperformance during a subsequent task, whereas trans-fer is negative if training causes a reduction in perfor-mance on the transfer task. The transfer of learninghas been extensively studied over the past cen-tury.[14] A number of researchers have also attemptedto understand the principles that govern transferwithin the context of motor learning, particularlyfrom a behavioural viewpoint.[14,15] Much of this‘motor learning’ research was concerned with trans-fer between tasks requiring considerable cognitive,as well as motor, processing.

In the present article, we attempt to understandthe impact of resistance training on the performanceof a wide range of transfer tasks in terms of thephysiological adaptations that accompany training.We argue that resistance training has the capacity

830 Carroll et al.

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to cause adaptations to many neuromuscular ele-ments that are involved in the control and execu-tion of movement, and is therefore likely to affectperformance during a wide range of movement tasks.Our reasoning is based on the classic work of Thorn-dike and Woodworth[16] who stated that ‘spreadof practice occurs only where identical elementsare concerned in the influencing and influencedfunction’ (page 249). The degree and direction (i.e.whether transfer is negative or positive) of transferfrom resistance training to other tasks is determinedby the interaction of the various neuromuscular ad-aptations associated with training, and the charac-teristics of the transfer tasks. Figure 1 depicts a sim-plified model that illustrates how 2 independent

neuromuscular adaptations could interact to affectthe performance of a particular movement task. Inreality, it is certain that transfer from resistancetraining to other movements will depend on theinteraction of more than 2 forms of adaptation. Thechallenge for future researchers is to determine theprecise nature of the neuromuscular adaptations thataccompany resistance training, and to identify pat-terns of interaction among these adaptations forvarious classes of movement.

1.1 Individual Muscles

In a recent experiment, we sought to establishwhether resistance training has the capacity to in-fluence the activation patterns of muscles that are

Performance ontransfer task

High

Low

Neuromuscularvariable 1

Neuromuscularvariable 2

State A

State A

State B

State B

Adaptation Adaptation

A

B

Fig. 1. A simplified model that illustrates how a linear interaction between 2 neuromuscular variables could affect performance on ahypothetical transfer task. The vertical coordinate of each point on the shaded surface specifies the level of performance on thetransfer task. The 2 neuromuscular variables can adapt independently, but performance is determined by the interaction betweentheir adaptive states. For example, the model depicts that adaptation of neuromuscular variable 1 in the direction from state A tostate B increases the level of performance on the transfer task when the state of neuromuscular variable 1 remains constant. Incontrast, an isolated adaptation of neuromuscular variable 2 in the direction from state A to state B reduces the level of performanceon the transfer task. In this hypothetical case, the overall influence on performance as the state of the system changes from stateA to state B is negative. Thus, transfer is negative despite that fact that neuromuscular variable 1 adapts in a manner that has apositive influence on the performance of the transfer task.

Resistance Training and Movement Control 831


recruited during training when they are engaged intasks requiring more complex muscular coordina-tion. We assessed the impact of resistance trainingfor the index finger extensor muscles on the perfor-mance of a difficult sensorimotor coordinationtask.[17] The task required participants to synchro-nise flexion and extension movements of the indexfinger with an auditory pacing signal. The frequencyof the pacing signal increased over time. Trainingthat increased isometric finger strength enhancedperformance on the finger coordination task. Theimprovements in performance were also accompa-nied by changes in the manner in which the trainedmuscles were recruited. More specifically, the fin-ger extensors were recruited in a more consistentfashion during the coordination task after the pro-gramme of resistance training. That is, the variabil-ity in the timing, amplitude and duration of muscleactivity was reduced.

These results confirm that the neuromuscular ad-aptations that are induced as a consequence of re-sistance training have the capacity to alter the man-ner in which trained muscles are activated by theCNS. In this particular case, resistance training wasassociated with neuromuscular adaptations that al-lowed the trained muscles to be controlled moreeffectively within the context of the coordinationtask. There was positive transfer from the resis-tance training to the functional task. To understandthe principles that govern whether there is positiveor negative transfer of performance from resistancetraining tasks to related functional tasks, it is nec-essary to consider the nature of the neuromuscu-lar adaptations that occur in response to resistancetraining.

1.1.1 Neural AdaptationsA candidate mechanism for an improvement

in the ability of resistance-trained muscles to becontrolled by the CNS is an increase in their force-generating capacity. Dettmers et al.[18] found thatneural activity increases in the primary motor cor-tex and caudal supplementary motor area as indi-viduals exert greater levels of isometric force. Ifeach motor unit within a muscle is capable of pro-

ducing more force after training, it follows that fewermotoneurons need to be recruited, and a reducedlevel of cortical activation is required to producean equivalent kinetic or kinematic outcome. It hasbeen proposed that the potential for interferencebetween functionally proximal areas of the cere-bral cortex increases with the degree to which theseare activated.[19] According to this hypothesis, in-creased spread of neural activation increases thepotential for the activation of neural elements thatinterfere with optimal task performance. In the con-text of movement control, the neural elements thatinterfere with performance may be any pathwaysor circuits that lead to the recruitment of motor unitsthat do not contribute effectively to an intendedmovement. Resistance training may enhance per-formance in related tasks by reducing the extent ofcortical activation and therefore the activation ofneural elements that interfere with the optimal ex-ecution of movement. Dettmers et al.[18] also foundthat when individuals increased the force that theyexerted in a simple key pressing task to levels above10% maximal voluntary contraction, muscle activ-ity was observed in a number of stabilising musclesthat did not directly contribute to force production inthe task. Thus, even in simple, low force tasks thereoccurs considerable spread of activation through-out the neuromuscular system. The observation ofsuch diffuse neural excitation clearly identifies thepotential for the activation of neural elements thatinterfere with optimal task performance.

It has also been consistently reported that coor-dination tasks that rely critically on the activationof the finger extensor muscles are performed lesseffectively than comparable tasks relying to a greaterdegree on flexor muscles.[20,21] Finger extensor mus-cles typically display a lower intrinsic capacity forforce generation than finger flexors and a greaterspread of cortical activation occurs during the re-cruitment of extensor muscles than flexors.[22,23]

Furthermore, cortical activity is greater during thumbextensor activity than flexor activity even when thelevel of force exerted is matched relative to themaximal voluntary contraction force in each direc-

832 Carroll et al.


tion.[23] That is, even when thumb flexors exert agreater absolute level of force than thumb exten-sors, a lower extent of cortical activity is requiredto produce thumb flexion. These observations pro-vide additional evidence for the hypothesis that anincrease in force-generating capacity may enhancemuscular coordination by reducing the extent ofneural activity within the motor centres of theCNS. It appears that muscles are controlled moreeffectively by the CNS when lower levels of neuralactivity are required to produce a given level ofmuscular force.

It is apparent that adaptations occurring distalto the motoneuron could underlie enhancements inmovement control via a reduction in the level ofcentral drive required to produce force. It is alsotrue, however, that adaptations to structures beforethe neuromuscular junction could act to increasethe efficiency of the central command. Changes insynaptic efficacy or in the organisation of neuralcircuitry within the spinal motoneuron pool or themotor cortex could serve to reduce the level of drivefrom other cortical or subcortical motor areas thatare involved in the control of movement. There isevidence that activity is reduced at a number ofsupraspinal sites, such as the dorsal pre-motor area,the parietal cortex and the lateral cerebellum, withthe acquisition of motor skill.[24-26] It is likely thatalterations of synaptic circuitry in the motor cortexunderlie some of the reductions in the level of neuralactivity within associated supraspinal motor centres.Rioult-Pedotti et al.[27,28] found that the synapticeffectiveness of layer II/III horizontal connectionswithin the primary motor cortex was modified whenrats learned to perform a difficult reaching move-ment. Furthermore, there is indirect evidence thatthe synaptic effectiveness of neural connections be-tween areas within the primary motor cortex canbe altered through motor training in humans.[29,30]

Thus, motor learning may be associated with phys-iological adaptations within the primary motor cor-tex that contribute to more efficient execution ofthe learned movements.

It is important to recognise that the evidencethat resistance training may enhance coordinationin come related tasks by reducing the level of cor-tical activity associated with the activation of trainedmuscles was drawn largely from experiments thathave focused on distal upper limb and hand mus-cles. Similarly, most of the studies that have dem-onstrated cortical adaptations following motor train-ing have involved hand muscles. The extent to whichthis evidence is applicable to more proximal limbmuscles, the control of which typically relies to alesser degree on direct cortico-spinal connections,is not clear.

Milner-Brown et al.[31] provided specific evi-dence that resistance training induces changes insynaptic effectiveness within the motoneuron pool.They found that resistance training caused an in-crease in the tendency of motor units to fire syn-chronously (motor unit short term synchronisation)and, in a cross sectional analysis, that the motor unitsof resistance-trained individuals fired with greatersynchrony than those of untrained individuals. Mo-tor unit short term synchronisation occurs when anumber of motoneurons receive input from axonalbranches of the same presynaptic neurons, therebyincreasing the probability of near-simultaneous dis-charge in the target motoneurons.[32-34] A changein the level of synchrony observed during a low-force isometric contraction therefore reflects an in-crease in the number or strength of common pre-synaptic inputs onto populations of motoneurons.There is also evidence that motor unit short termsynchronisation in hand muscles is brought aboutlargely via descending cortical-spinal tract neuronswith branched-stem axons.[32,35,36] The implicationof these findings is that resistance training may al-ter the connectivity between cortico-spinal cells andspinal motoneurons.

Although there remain caveats associated withthe original Milner-Brown et al.[37] study, Semmlerand Nordstrom[38] have provided converging evi-dence, based upon comparisons between resistance-trained individuals, untrained individuals and skilledmusicians. They found that the resistance-trained



individuals displayed greater motor unit short termsynchronisation than the musicians and untrainedpeople. Taken together, these experiments suggestthat resistance training is associated with an in-crease in motor unit short term synchrony, whichis caused by changes in synaptic efficacy within themotoneuron pool. This implies that the number orstrength of common connections onto the moto-neurons of trained muscles may increase followingresistance training.[32-34] Adaptations to basic neu-ral elements such as the synapses between moto-neurons and cortico-spinal cells, which play a fun-damental role in the execution of voluntarymovement, are likely to influence the manner inwhich trained muscles are recruited during a widerange of tasks.

1.1.2 Principles of TransferIt is not yet possible to identify a general set of

principles that govern the impact of resistance train-ing on the manner in which trained muscles arerecruited during related tasks. This is both becausethere exists insufficient information about the pre-cise nature of the neural adaptations that accom-pany training, and because few experiments havebeen conducted to investigate transfer between par-ticular resistance training and functional tasks. Forexample, there remains uncertainty regarding thebasic consequences for movement control of theneural adaptations that underlie changes in muscleactivation. On the one hand, if resistance trainingcauses increases in the force-generating capacity ofmuscle fibres or the strength of the connections be-tween motoneurons and cortico-spinal cells, fewerdescending fibres will be activated to execute anygiven task involving the trained muscles. These ef-fects would be expected to enhance the effective-ness of neuromuscular control in many movementtasks.[20,21]

Alternatively, we have argued that resistancetraining induces adaptations that lead to an increasein motor unit synchrony. There is evidence that in-creased synchrony of motor unit recruitment leadsto greater fluctuations in force during simple iso-metric tasks.[39,40] Decreases in the steadiness of

contraction may serve to reduce performance in cer-tain tasks. Furthermore, motor unit synchrony islower in musicians than in untrained individuals.[38]

Thus, in contrast to resistance training, the neuraladaptations associated with years of practice of skillsrequiring considerable fine control of force lead toreductions in motor unit synchrony. These findingsimply that resistance training induces some spe-cific adaptations that may reduce the effectivenessof neuromuscular control within some movementcontexts. However, in contrast to this expectation,resistance training has been found to cause reduc-tions in force variation in elderly individuals andpatients with essential tremor.[41-43] The discrepan-cies that are evident between the expected and ob-served functional consequences of the neuromus-cular adaptations that occur in response to resistancetraining confirm that a number of neuromuscularadaptations interact to determine the nature of trans-fer from resistance training to functional movements.

1.2 Groups of Muscles

Evidence that resistance training impacts uponmuscular coordination is provided by recent exper-iments that have focused on the activation of an-tagonist muscles during maximal contractions.[8-10]

The degree to which antagonist muscles are acti-vated during movement is of considerable impor-tance, since the resultant torque about a joint canbe increased by a reduction in the activation of mus-cles that oppose the prime movers. In these exper-iments, resistance training resulted in a lower levelof knee flexor electromyogram (EMG) activity dur-ing maximal isometric knee extension tasks. It ap-pears that the participants learned to reduce the levelof antagonist muscle activation during the periodof resistance training. It is likely that learning of asimilar nature occurs when individuals perform morecomplicated resistance training exercises, that re-quire the precise timing of muscle recruitment andcoordination of mono- and biarticular muscles. Inthis section, we discuss the influence that the phys-iological changes underlying enhancements in co-

834 Carroll et al.


ordination may have upon the control of functionalmovement tasks.

Carroll and co-workers[17] demonstrated that re-sistance training causes changes in the neuromus-cular system that can have a positive impact on theexecution of movements that are somewhat relatedto the training tasks. Specifically, resistance train-ing enhanced the performance during a difficult sen-sorimotor coordination task involving the musclesthat were engaged during training. However, Bar-rata et al.[44] reported that the adaptations associ-ated with resistance training had a negative impactupon the performance of a related movement task.The experiment of Barrata et al.[44] involved 2 in-dividuals who were drawn from a larger study in-volving cross-sectional analyses of hamstring/quad-riceps coactivation. The participants performed dailyresistance training involving dynamic knee flexionsfor 2 or 3 weeks. Following the short training pe-riod, both participants showed greater knee flexorEMG activity during maximal isometric knee ex-tension. That is, the activity of a muscle group thatwas recruited as a prime mover during training wasincreased when it acted as an antagonist followingtraining. This experiment provides direct evidencethat resistance training may cause changes in theway that groups of muscles are coordinated that aremaladaptive within some movement contexts, sinceincreases in knee flexor activity reduce the net kneeextension torque.

Experiments that have demonstrated the specificeffects of resistance training upon strength provideindirect evidence that resistance training causes ad-aptations that can either enhance or interfere withthe execution of related movements. For example,Carroll et al.[45] found that individuals who trained3 times per week showed greater strength increasesin a primary resistance training task, which involvedhip and knee extension, than those who trained twiceper week. In contrast, those who trained twice perweek showed a moderate strength increment in novelisometric and isokinetic knee extension tasks, where-as the isometric and isokinetic strength of individ-uals who trained 3 times per week did not change.

This pattern of results suggests that participantswho trained more frequently experienced a greaterdegree of neural adaptation than the individualswho trained twice per week. We have argued thatresistance training induces neural adaptations thatare associated with learning the optimal pattern ofmuscle recruitment for the training tasks. Thus, thegroup that trained more frequently may have showngreater increases in strength on the primary train-ing task than the low frequency group because ofa greater improvement in coordination.

However, the optimal pattern of muscle recruit-ment for the hip and knee extension task is inap-propriate for the pure knee extension tasks. Morespecifically, coactivation of the knee flexors andextensors contributes appropriately to force pro-duction in a hip and knee extension task but reducesforce in an open-chain knee extension task.[46] Thelack of an increase in knee extension strength shownby the high frequency training group can be ex-plained by a greater degree of knee flexor/extensorcoactivation in the pure knee extension task. Thatis, a greater degree of antagonist coactivation aftertraining could have resulted in a lack of change innet torque production, despite increases in the force-generating capacity of the prime movers. The impli-cation of these findings is that the nervous systemchanges associated with enhancements in coordi-nation on the training tasks may negatively influ-ence the patterns of muscle recruitment during somenovel strength tasks. The proposal that negativetransfer may occur between some resistance train-ing protocols and certain high force tasks is con-sistent with the results from Baratta et al.[44] Todetermine the general principles that govern thenature of transfer between resistance training andother related movements, however, it is necessaryto consider the neural mechanisms that may under-lie changes in coordination.

1.2.1 Neural AdaptationsThe coordination of muscle recruitment during

movement requires complex cooperative interac-tions between a number of spinal and supraspinalcentres. The architecture of the neural circuitry at



each of these sites influences patterns of muscleactivation. For example, considerable divergenceexists within the cortico-spinal pathway, such thatindividual cortico-spinal cells are connected withmany motoneurons that project to different mus-cles.[47-49] Thus, in most cases, output from the pri-mary motor cortex influences the activity of groupsof muscles rather than individual muscles. The pat-terns of muscular coordination that are ultimatelyexhibited during behaviour are therefore determinedby the extent to which cortico-spinal cell fibres di-verge within the motoneuron pool, and the efficacyof synapses between particular cortico-spinal cellsand the motoneurons that project to the musclesthat are engaged in the behaviour. Cortico-spinalcells also make a vast number of indirect connec-tions with motoneurons via oligosynaptic interneu-ronal pathways.[48,49] The organisation of the inter-neuronal circuitry that mediates indirect connectivitybetween cortico-spinal neurons and motoneuronstherefore plays an additional role in specifying theparticular patterns of muscle activity that are ex-hibited during movement.

Muscular coordination is also achieved via net-works of local connections between neurons thatreside at a number of sites in the CNS. Consider-able information exists regarding the synaptic cir-cuitry in the spinal cord that contributes to muscu-lar coordination. For example, the phenomenon ofreciprocal inhibition, which is the inhibition of an-tagonist muscles during activation of the ipsilateralagonist, is known to be at least partly mediated bydisynaptic inhibitory interneuronal pathways in thespinal cord.[50] However, there is recent evidencethat similar inhibitory connections exist betweenthe cortical areas that ultimately project to pairs ofantagonist muscles.[51] Furthermore, the existenceof horizontal connections between motor corticalzones that primarily represent antagonist muscleshas been confirmed anatomically in the cat.[52] Sub-cortical neural elements such as the cerebellum andbasal ganglia also appear to play an important rolein the coordination of synergist and antagonist mus-cles.[53,54] For example, there is evidence that cir-

cuitry within the globus pallidus may facilitate theactivity of prime mover and synergist muscles andinhibit the activity of antagonist muscles via cortico-putamino-pallidal-thalamo-cortical pathways.[55]

The basal ganglia have also been implicated in thecontrol of timing processes,[56] and may thereforeplay a role in the temporal coordination of musclesduring complicated movements that require pre-cise timing of muscle activation.

Future research may enable us to determine pre-cisely which of the many neural elements that playa role in generating coordinated movement undergoadaptation during resistance training and therebylead to changes in coordination. For example, thereis emerging evidence that plasticity within the mo-tor cortex plays an important role in motor learn-ing.[57-61] A number of recent reports indicate thatlong term potentiation (LTP) of synapses within themotor cortex may be an important mechanism of cor-tical adaptation that underlies motor learning.[27,28,62]

In this regard, Rioult-Pedotti et al.[27,28] found thatcortical adaptation and motor learning are attenu-ated when N-methyl-D-aspartate (NMDA) recep-tors, that are known to mediate LTP, are blocked.They also found that artificial LTP is more difficultto induce in motor cortical sections following learn-ing, and that long term depression (LTD) is exac-erbated. Since there is a limit to the extent of LTPthat can occur before the effect becomes saturated,[63]

the observation that learning reduces the capacityfor subsequent LTP suggests that skill learning in-volves a LTP-like mechanism. Although LTP is astrong candidate to underlie cortical plasticity, theimportance of other mechanisms of synaptic adapta-tion, such as LTD, should not be discounted. There isconsiderable evidence that LTD is the principle mech-anism of synaptic plasticity in the cerebellum.[54] Re-gardless of the mechanism, it is apparent that motorlearning arises, at least partly, from modifications inthe strength of connections between neurons withinsupraspinal motor centres. Thus, resistance train-ing that induces motor learning may cause changesin connectivity between the motor areas that are

836 Carroll et al.


involved in controlling the resistance training ex-ercises.

If improvements in coordination following re-sistance training arise as a consequence of changesin connectivity between the elements of the nerv-ous system that control the trained muscles, whatare the likely consequences for movements that arerelated to the movements performed during train-ing? At a simple level, it could be argued that changesin synaptic efficacy within the neural pathways as-sociated with producing particular movements arelikely to affect muscle activation whenever thesepathways are activated. Thus, if particular circuitsinvolved in coordinating resistance training move-ments are modified with training, alterations couldbe expected to the patterns of muscle activationexhibited during other movements that recruit someof the same circuits. However, this expectation doesnot account for the possibility that additional cir-cuits could be activated to counterbalance the ef-fect of the adaptations and thereby maintain an equiv-alent functional outcome. It also does not accountfor the ability of the CNS to facilitate or inhibitparticular neural pathways in a task-specific man-ner.

The considerable scope for flexibility in the mech-anisms employed by the CNS to generate muscleactivation is illustrated clearly by the nature of theinteractions that occur between neural circuits withinthe spinal cord during the control of voluntary move-ment.[48,49] Interneurons in the spinal cord receiveinput from afferent fibres, descending fibres andthe fibres of other interneurons, and ultimately in-fluence the activity of motoneurons. The interac-tion of these various inputs onto interneuronal cir-cuitry determines which motor units are recruitedduring movement. For example, afferent input al-ters the excitability of spinal interneurons that alsoreceive input from descending fibres, and can thusmodify the specific populations of motoneurons af-fected by the descending neural commands. How-ever, spinal interneuronal activity and the synapticeffectiveness of connections between afferent fi-bres and motoneurons and interneurons (i.e. via pre-

synaptic inhibition) are also greatly influenced bydescending output from supraspinal motor centres.Thus, the activation of motoneurons via both cortico-spinal cells and spinal reflex pathways is partlydetermined by the manner in which supraspinal andsegmental elements interact to set the excitabilitystates of interneuronal circuits. An important con-sequence of this arrangement is that the same cortico-spinal output can activate different populations ofmotoneurons depending on the state of circuitrywithin the spinal cord. The flexibility of this cir-cuitry suggests that, in many cases, the CNS maybe capable of selectively modulating the excitabil-ity of particular circuits that may have experiencedadaptation during motor learning. For example, theimpact of adaptations to spinal chord circuitry thatwould ordinarily serve to reduce performance in arelated task may be countered by the modulation ofdescending input from supra-spinal centres, therebyavoiding negative transfer.

1.2.2 Principles of TransferThe experiments cited in the previous sections

have shown that resistance training can induce ad-aptations that have the potential either to enhanceor interfere with the performance of related tasks.It is important to note that performance decrementshave only been demonstrated for high force tasksthat are relatively novel to the participants. It re-mains to be determined whether the neural adapta-tions that underlie refinements in coordination havea significant effect on patterns of muscle recruitmentduring tasks that have dissimilar force requirementsfrom the resistance training exercises. The impact ofneural adaptation on the coordination of well-learnedmovements and tasks that are practised concurrentlywith resistance training is also yet to be established.Martin and Morris[63] have speculated that consid-erable potential for interference exists when the sameneural elements are required for different types oflearning. However, the CNS has a high capacity forflexibility in the generation of muscle activationpatterns. It seems likely that, with appropriate train-ing, there exists the potential for a large number ofrelated movements to be executed with high effi-



ciency; even if conflicting patterns of coordinationare required for optimal performance of these tasks.

However, as a general principle, negative trans-fer may occur when a pattern of muscle recruitmentassociated with optimal performance on a resis-tance training task would serve to retard perfor-mance if it was expressed during a transfer task. Anexample would be if the training task required strongcoactivation of a particular set of muscles, and thetransfer task required strong activation of some ofthe muscles in the set, but inhibition of other mus-cles in the set. This situation occurs when the train-ing task involves simultaneous knee and hip exten-sion and the transfer task requires isolated kneeextension, since coactivation of knee flexors andextensors is necessary for optimal performance onthe training task, but reduces performance on thetransfer task. In this case, it is anticipated that anoverflow of activation may occur from the musclesthat are strongly activated in the transfer task (e.g.quadriceps muscles) to muscles that would best beinhibited (e.g. hamstring muscles). The mechanismof this overflow would be via the neural pathwaysresponsible for facilitating cocontraction in the train-ing task, since these pathways are likely to be rein-forced during training. In contrast, positive transfermay occur if the process of learning the optimalpatterns of muscle activity for the resistance train-ing exercises strengthens excitatory neural connec-tions between muscles that act as functional syner-gists in the context of the transfer task. Positivetransfer is also expected if learning reinforces in-hibitory circuits between muscles that, if activatedtogether, would degrade performance.

2. Conclusion

The evidence presented in this article indicatesthat resistance training induces adaptations that caninfluence the manner in which trained muscles arerecruited by the CNS during related functional tasks.Adaptations at a number of sites in the neuromus-cular system are likely to contribute to changes inmovement execution and control. There is directevidence that resistance training causes changes in

synaptic efficacy within the motoneuron pool,[31,38]

and evidence from a number of sources that adap-tations in various supraspinal motor centres under-lie motor learning. Furthermore, the physiologicaladaptations associated with resistance training mayinteract to produce either positive or negative transferof performance to functional tasks. Yet, the precisenature of many of the neuromuscular responses toresistance training and the principles that governthe transfer between resistance training and othermovements are still to be determined.

Research that seeks to identify these principleshas the potential to enhance our basic understandingof the neural basis of movement control and learn-ing, as well as provide important information toassist the design of resistance training programmesin practical settings such as rehabilitation and ath-letic training. The challenge for future researchersis to determine the precise nature of the neuromus-cular adaptations that accompany resistance train-ing, and to identify patterns of interaction amongthese adaptations for various classes of movement.

Acknowledgements

The authors would like to thank Benjamin Barry andAngus Ross for helpful comments on the manuscript.

This project was partly funded by the Australian ResearchCouncil.

References1. Abernethy PJ, Jurimae J, Logan P, et al. Acute and chronic

response of skeletal muscle to resistance exercise. Sports Med1994; 17 (1): 22-38

2. Baldwin KM, Haddad F. Effects of different activity and inac-tivity paradigms on myosin heavy chain gene expression instriated muscle. J Appl Physiol 2001; 90: 345-57

3. Timson BF. Evaluation of animal models for the study of exercise-induced muscle enlargement. J Appl Physiol 1990; 69:1935-45

4. Enoka RM. Neural adaptations with chronic physical activity. JBiomech 1997; 30 (5): 447-55

5. Enoka RM. Neural strategies in the control of muscle force.Muscle Nerve Suppl 1997; 5: S66-S69

6. Moritani T, deVries HA. Neural factors versus hypertrophy inthe time course of muscle strength gain. Am J Phys Med 1979;58 (3): 115-30

7. Sale DG. Neural adaptation to resistance training. Med SciSports Exerc 1988; 20 Suppl. 5: S135-S145

8. Carolan B, Carafelli E. Adaptations in coactivation after isomet-ric resistance training. J Appl Physiol 1992; 73 (3): 911-7

838 Carroll et al.


9. Hakkinen K, Kallinen M, Izquierdo M, et al. Changes in agonist-antagonist EMG, muscle CSA, and force during strengthtraining in middle-aged and older people. J Appl Physiol1998; 84 (4): 1341-9

10. Hakkinen K, Alen M, Kallinen M, et al. Neuromuscular adap-tation during prolonged strength training, detraining andre-strength-training in middle-aged and elderly people. Eur JAppl Physiol 2000; 83: 51-62

11. Abernethy PJ, Jurimae J. Cross-sectional and longitudinal usesof isoinertial, isometric, and isokinetic dynamometry. MedSci Sports Exerc 1996; 28: 1180-7

12. Pearson DR, Costill DL. The effects of constant external resis-tance exercise and isokinetic training on work-induced hyper-trophy. J Appl Sport Sci Res 1988; 2: 39-41

13. Sale DG, Martin JE, Moroz DE. Hypertrophy without increasedisometric strength after weight training. Eur J Appl Physiol1992; 64: 51-5

14. Cormier SM, Hagman JD, editors. Transfer of learning: con-temporary research and applications. New York (NY): Aca-demic Press, 1987

15. Adams JA. Historical review and appraisal of research on thelearning, retention, and transfer of human motor skills. Psy-chol Bull 1987; 101: 41-74

16. Thorndike EL, Woodworth RS. The influence of improvementin one mental function upon the efficiency of other functions.I. Psychol Rev 1901; 8: 247-61

17. Carroll TJ, Barry B, Riek S, et al. Resistance training enhancesthe stability of sensorimotor coordination. Proc R Soc LondB Biol Sci 2001; 268: 221-7

18. Dettmers C, Ridding MC, Stephan KM, et al. Comparison ofregional cerebral blood flow with transcranial magnetic stim-ulation at different forces. J Appl Physiol 1996; 81 (2):596-603

19. Kinsbourne M, Hicks RE. Mapping functional cerebral space:competition and collaboration in human performance. In:Kinsbourne M, editor. Asymmetrical function of the brain.Cambridge: Cambridge University Press, 1978: 267-73

20. Carson RG. Neuromuscular-skeletal constraints upon the dy-namics of perception-action coupling. Exp Brain Res 1996;110: 99-110

21. Carson RG, Riek S. The influence of joint position on the dy-namics of perception-action coupling. Exp Brain Res 1998;121: 103-14

22. Cheney PD, Fetz EE, Mewes K. Neural mechanisms underlyingcorticospinal and rubrospinal control of limb movements.Prog Brain Res 1991; 87: 213-52

23. Yue GH, Liu JZ, Siemionow V, et al. Brain activation duringhuman finger extension and flexion movements. Brain Res2000; 856: 291-300

24. Friston KJ, Frith CD, Passingham RE, et al. Motor practice andneurophysiological adaptation in the cerebellum: a positrontomography study. Proc R Soc Lond B Biol Sci 1992; 248:223-8

25. Hund-Georgiadis M, von Cramon DY. Motor-learning-relatedchanges in piano players and non-musicians revealed by func-tional magnetic-resonance signals. Exp Brain Res 1999; 125:417-25

26. van Mier H, Tempel LW, Perlmutter JS, et al. Changes in brainactivity during motor learning measured with PET: effects ofhand of performance and practice. J Neurophysiol 1998; 80:2177-99

27. Rioult-Pedotti MS, Friedman D, Donoghue JP. Learning-inducedLTP in neocortex. Science 2000; 290: 533-6

28. Rioult-Pedotti MS, Friedman D, Hess G, et al. Strengtheningof horizontal cortical connections following skill learning.Natl Neurosci 1998; 1: 230-4

29. Classen J, Liepert J, Wise SP, et al. Rapid plasticity of humancortical movement representation induced by practice. J Neuro-physiol 1998; 79: 1117-23

30. Cohen LG, Ziemann U, Chen R, et al. Studies of neuroplasticitywith transcranial magnetic stimulation. J Clin Neurophysiol1998; 15 (4): 305-24

31. Milner-Brown HS, Stein RB, Lee RG. Synchronization of hu-man motor units: possible roles of exercise and supraspinalreflexes. Electroencephalogr Clin Neurophysiol 1975; 38:245-54

32. Datta AK, Farmer SF, Stephens JA. Central nervous pathwaysunderlying synchronization of human motor unit firing stud-ied during voluntary contractions. J Physiol 1991; 432:401-25

33. Kirkwood PA, Sears TA. The synaptic connections to intercos-tal motoneurones as revealed by the average common excita-tion potential. J Physiol 1978; 275: 103-34

34. Sears TA, Stagg D. Short-term synchronization of intercostalmotoneurone activity. J Physiol 1976, 263: 357-81

35. Farmer SF, Ingram DA, Stephens JA. Mirror movements stud-ied in a patient with Klippel-Fiel syndrome. J Physiol 1990;428: 467-84

36. Farmer SF, Swash M, Ingram DA, et al. Changes in motor unitsynchronization following central nervous lesions in man. JPhysiol 1993; 463: 83-105

37. Yue G, Fuglevand AJ, Nordstrom MA, et al. Limitations of thesurface electromyography technique for estimating motorunit synchronization. Biol Cybern 1995; 73: 223-33

38. Semmler JG, Nordstrom MA. Motor unit discharge and forcetremor in skill- and strength-trained individuals. Exp BrainRes 1998; 119: 27-38

39. Halliday DM, Conway BA, Farmer SF, et al. Load-independentcontributions from motor-unit synchronization to humanphysiological tremor. J Neurophysiol 1999; 82: 664-75

40. Yao W, Fuglevand RJ, Enoka RM. Motor-unit synchronizationincreases EMG amplitude and decreases force steadiness ofsimulated contractions. J Neurophysiol 2000; 83: 441-52

41. Bilodeau M, Keen DA, Sweeney PJ, et al. Strength training canimprove steadiness in persons with essential tremor. MuscleNerve 2000; 23: 771-8

42. Keen DA, Yue GH, Enoka RM. Training related enhancementin the control of motor output in elderly humans. J Appl Phys-iol 1994; 77 (6): 2648-58

43. Laidlaw DH, Kornatz KW, Keen DA, et al. Strength trainingimproves the steadiness of slow lengthening contractions per-formed by old adults. J Appl Physiol 1999; 87: 1786-95

44. Barrata R, Solomonow M, Zhou BH, et al. Muscular coactiva-tion: the role of the antagonist musculature in maintainingknee stability. Am J Sports Med 1988; 16 (2): 113-22

45. Carroll TJ, Abernethy PJ, Logan PA, et al. Resistance trainingfrequency: strength and myosin heavy chain responses to twoand three bouts per week. Eur J Appl Physiol 1998; 78: 270-5

46. Wiemann K, Tidow G. Relative activity of hip and knee exten-sors in sprinting – implications for training. New Stud Athlet1995; 10: 29-49



47. Porter R, Lemon R. Corticospinal function and voluntary move-ment. Oxford: Clarendon Press, 1995

48. McCrea DA. Can sense be made of spinal interneuron circuits?Behav Brain Sci 1992; 15: 633-43

49. McCrea DA. Supraspinal and segmental interactions. Can JPhysiol Pharm 1996; 74: 513-57

50. Baldissera F, Hultoborn H, Illert M. Integration in spinal neu-ronal systems. I. In: Brookhart JM, Mountcastle VB, BrooksVB, et al., editors. Handbook of physiology: the nervous sys-tem II. Baltimore (MD): American Physiological Society, 1981

51. Bertolasi L, Priori A, Tinazzi M, et al. Inhibitory action of fore-arm flexor muscle afferents on corticospinal outputs to antag-onist muscles in humans. J Physiol 1998; 511: 947-56

52. Capaday C, Devanne H, Bertrand L, et al. Intracortical connec-tions between motor cortical zones controlling antagonisticmuscles in the cat: a combined anatomical and physiologicalstudy. Exp Brain Res 1998; 120: 223-32

53. Bloedel JR. Functional heterogeneity with structural homoge-neity: how does the cerebellum operate? Behav Brain Sci 1992;15: 666-78

54. Ito M. Mechanisms of motor learning in the cerebellum. BrainRes 2000; 886: 237-45

55. Marsden CD, Obeso JA. The functions of the basal ganglia andthe paradox of stereotaxic surgery in Parkinson’s disease. Brain1994; 117: 877-97

56. Rao SM, Mayer AR, Harrington DL. The evolution of brainactivation during temporal processing. Nat Neurosci 2001; 4:317-23

57. Jacobs KM, Donoghue JP. Reshaping the cortical motor map byunmasking latent intracortical connections. Science 1991;251: 944-7

58. Jenkins IH, Brooks DJ, Nixon PD, et al. Motor sequence learn-ing: a study with positron emission tomography. J Neurosci1994; 14 (6): 3775-90

59. Jones TA, Chu CJ, Grande LA, et al. Motor skills training en-hances lesion-induced structural plasticity in the motor cortexof adult rats. J Neurosci 1999; 19 (22): 10153-63

60. Karni A, Meyer G, Jezzard P, et al. Functional MRI evidencefor adult motor cortex plasticity during motor skill learning.Nature 1995; 377: 155-8

61. Petersen SE, van Mier H, Fiez JA, et al. The effects of practiceon the functional anatomy of task performance. Proc NatlAcad Sci U S A 1998; 95: 853-60

62. Butefisch CM, Davis BC, Wise SP, et al. Mechanisms of use-dependent plasticity in the human motor cortex. Proc NatlAcad Sci U S A 2000; 97: 3661-5

63. Martin SJ, Morris RG. Cortical plasticity: it’s all the rage! CurrBiol 2002; 11: R57-R59

Correspondence and offprints: Timothy J. Carroll, Perceptionand Motor Systems Laboratory, School of Human MovementStudies, The University of Queensland, Brisbane, Queens-land 4072, Australia.E-mail: [email protected]

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Neural Adaptations to Resistance Training

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