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Sports Med 2009; 39 (11): 903-921

REVIEW ARTICLE 0112-1642/09/0011-0903/$49.95/0

ª 2009 Adis Data Information BV. All rights reserved.

Neuromuscular Adaptations to Training,


Injury and Passive Interventions
Implications for Running Economy
Jason Bonacci,1,2 Andrew Chapman,1,3,4,5 Peter Blanch2 and Bill Vicenzino1
1 Musculoskeletal Pain and Injury Research Unit, University of Queensland, Brisbane,
Queensland, Australia
2 Department of Physical Therapies, Australian Institute of Sport, Canberra, Australian Capital Territory,
Australia
3 School of Kinesiology, Simon Fraser University, Vancouver, British Columbia, Canada
4 Applied Research Centre, Australian Institute of Sport, Canberra, Australian Capital Territory, Australia
5 Department of Kinesiology and Physical Education, McGill University, Montreal, Quebec, Canada

Contents
Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 903
1. Literature Search . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 905
2. Adaptations of Muscle Recruitment to Single-Discipline Endurance Training . . . . . . . . . . . . . . . . . . . . 906
3. Adaptation of Muscle Recruitment to Multidiscipline Endurance Training . . . . . . . . . . . . . . . . . . . . . . . 907
4. Neuromuscular Characteristics and Running Economy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 907
5. Training, Shoes, In-Shoe Orthoses, Musculoskeletal Injury and Running Economy. . . . . . . . . . . . . . . . . 909
5.1 Resistance Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 909
5.2 Plyometric Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 910
5.3 Stretching . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 911
5.4 Multidiscipline Sports and Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 912
5.5 Shoes and In-Shoe Orthoses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 914
5.6 Musculoskeletal Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 915
6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 916
7. Future Directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 916

Abstract Performance in endurance sports such as running, cycling and triathlon


has long been investigated from a physiological perspective. A strong
relationship between running economy and distance running performance is
well established in the literature. From this established base, improvements in
running economy have traditionally been achieved through endurance
training. More recently, research has demonstrated short-term resistance and
plyometric training has resulted in enhanced running economy. This
improvement in running economy has been hypothesized to be a result of
enhanced neuromuscular characteristics such as improved muscle power
development and more efficient use of stored elastic energy during running.
Changes in indirect measures of neuromuscular control (i.e. stance phase
contact times, maximal forward jumps) have been used to support this
hypothesis. These results suggest that neuromuscular adaptations in response
904 Bonacci et al.

to training (i.e. neuromuscular learning effects) are an important contributor


to enhancements in running economy. However, there is no direct evidence to
suggest that these adaptations translate into more efficient muscle recruit-
ment patterns during running. Optimization of training and run performance
may be facilitated through direct investigation of muscle recruitment patterns
before and after training interventions.
There is emerging evidence that demonstrates neuromuscular adaptations
during running and cycling vary with training status. Highly trained runners
and cyclists display more refined patterns of muscle recruitment than their
novice counterparts. In contrast, interference with motor learning and neuro-
muscular adaptation may occur as a result of ongoing multidiscipline training
(e.g. triathlon). In the sport of triathlon, impairments in running economy
are frequently observed after cycling. This impairment is related mainly to
physiological stress, but an alteration in lower limb muscle coordination
during running after cycling has also been observed. Muscle activity during
running after cycling has yet to be fully investigated, and to date, the effect of
alterations in muscle coordination on running economy is largely unknown.
Stretching, which is another mode of training, may induce acute neuromus-
cular effects but does not appear to alter running economy.
There are also factors other than training structure that may influence
running economy and neuromuscular adaptations. For example, passive
interventions such as shoes and in-shoe orthoses, as well as the presence of
musculoskeletal injury, may be considered important modulators of neuro-
muscular control and run performance. Alterations in muscle activity and
running economy have been reported with different shoes and in-shoe
orthoses; however, these changes appear to be subject-specific and non-
systematic. Musculoskeletal injury has been associated with modifications in
lower limb neuromuscular control, which may persist well after an athlete has
returned to activity. The influence of changes in neuromuscular control as a
result of injury on running economy has yet to be examined thoroughly, and
should be considered in future experimental design and training analysis.

Endurance sports such as running, cycling and The steady-state oxygen consumption at a given
triathlon are performed by many people at the running velocity is defined as running economy,[2,3]
recreational and competitive levels. At competi- and reflects the metabolic cost or metabolic de-
tion level, each of these sports requires extensive mand of running. A strong relationship has been
training. Triathlon is unique in that it is a multi- demonstrated between running economy and
discipline sport requiring athletes to balance the endurance running performance.[2,4-7] These mea-
training demands of three separate disciplines sures highlight the relationship between the cardio-
(i.e. swimming, cycling, running). The physiolo- respiratory system and performance; however,
gical and metabolic adaptations that occur in they do not reflect the contribution of the neural
response to training have been extensively investi- system, which controls and coordinates human
gated. Oxygen consumption, blood lactate movement. The interaction between the neural and
threshold, heart rate intensity, respiratory ex- muscle systems (i.e. neuromuscular system) is
change ratio and the pulmonary ventilation fundamental to all movement, and effectively
threshold are common measures used to reflect translates cardiorespiratory capacity into efficient
endurance performance or adaptation to training.[1] movement and therefore into performance.

ª 2009 Adis Data Information BV. All rights reserved. Sports Med 2009; 39 (11)
Neuromuscular Adaptations and Running Economy 905

The neuromuscular system has the capability times and leg strength during isolated tasks as
to adapt to training, not unlike the cardio- evidence for neuromuscular adaptations. If
respiratory system. Studies over the past two neuromuscular adaptations are responsible for
decades have provided strong evidence that con- the changes in running economy then it would be
tinued practice of a task (i.e. training) facilitates reasonable to suggest that there would be altera-
neuromuscular adaptations, which are charac- tions in motor recruitment during running fol-
terized by more skilled control of movement and lowing training.
muscle recruitment patterns.[8-11] Training- It is important to appreciate that adaptations
induced adaptations of descending motor com- in motor recruitment as a result of training re-
mands reflect learning within the CNS and can be present a learning effect. Positive adaptations
represented by changes in muscle electro- infer that an individual learns to produce specific
myography (EMG) function (i.e. motor recruit- patterns of muscle recruitment that are asso-
ment).[11] Like training, musculoskeletal pain and ciated with optimal performance of the task. This
injury[12,13] – and passive interventions such as is inherently different to the alterations in neuro-
shoes and in-shoe orthoses[14-17] (which are often muscular function that occur with fatigue during
prescribed for pain and/or injury) – have been prolonged exercise.[28] Fatigue in itself is a com-
shown to induce acute adaptations in motor plex phenomenon and much attention has
recruitment. Musculoskeletal overuse injury is a already been directed toward better under-
significant adverse effect of training that con- standing the mechanisms of fatigue and regula-
stitutes a major impediment to training and ulti- tion of output during endurance exercise.[29-32]
mately performance, through missed training Accordingly, the intent of this review is not to
and/or diminished training quality. The pre- revisit this information nor discount the impor-
valence of lower extremity injury in recreational tance of fatigue in modulating exercise perfor-
and competitive athletes ranges from 19.4% to mance but rather to discuss the adaptations in
79.3% in running athletes[18] and 37–91% in ath- motor recruitment (i.e. learning effects) that
letes participating in triathlons.[19] An injury- occur with different modes of training, injury and
induced restriction in training can result in passive interventions and the implications this
detraining, which may negatively affect perfor- may have for running economy. Therefore,
mance, cardiorespiratory health and neuro- the aims of this review are to: (i) examine the
muscular control.[20,21] adaptations of lower limb muscle recruitment
It is apparent within the literature that training (i.e. neuromuscular adaptations) to different
can induce positive changes in running econo- modes of training (i.e. running, cycling, multi-
my.[22,23] Training also appears to induce adap- discipline); (ii) examine what aspects of neuro-
tations in motor recruitment.[8,9,11] Less well muscular control are associated with running
known are the neuromuscular adaptations that economy; and (iii) investigate whether neuro-
occur with different modes of training (i.e. run- muscular adaptations induced by training, pas-
ning, cycling, multidiscipline training, resistance sive interventions and injury can be coupled with
training) and how these changes in neuromus- changes in running economy.
cular control can be coupled with running econ-
omy. It has recently been hypothesized that
improvements in running economy following 1. Literature Search
strength and resistance training were due to
neuromuscular adaptations.[24-26] Inferences have The databases Cinahl, MEDLINE, PubMed,
also been made that optimal lower limb muscle SportDiscus and Web of Science were searched
recruitment is critical for superior running eco- using the following combination of terms: (‘run-
nomy.[27] However, these hypotheses have been ning
. economy‘ or ‘oxygen consumption’ or
based on indirect measures of neuromuscular ‘VO2’) and (‘EMG’ or ‘muscle activity’ or ‘neuro-
control such as stance phase ground contact muscular’) or (‘EMG’ or ‘neuromuscular’ or

ª 2009 Adis Data Information BV. All rights reserved. Sports Med 2009; 39 (11)
906 Bonacci et al.

‘running economy’ or ‘oxygen consumption’) and strokes for individual cyclists), greater popula-
(‘orthoses’ or ‘orthotics’ or ‘shoes’ or ‘resistance tion variance (i.e. variability of muscle recruit-
training’ or ‘plyometrics’ or ‘injury’ or ‘cycling’ ment between athletes), more extensive and more
or ‘triathlon’). The reference lists of the articles variable muscle co-activation and longer dura-
obtained were searched manually to obtain tions of muscle activity than highly trained
further studies not identified electronically. All cyclists with 10.2 – 1.4 years’ experience, cycling
relevant studies in the English language were 393.9 – 32.5 km/wk[39] (figure 1[40]). A similar
included. finding emerged when moderately trained run-
ners (6.6 – 1.3 years’ experience, 61.4 – 8.8 km/wk)
were compared with novice runners (3.4 – 2.8
2. Adaptations of Muscle Recruitment to km/wk).[41] Specifically, novice runners were char-
Single-Discipline Endurance Training acterized by greater individual variance (i.e. varia-
bility between strides) and greater population
Motor learning studies have demonstrated variance. These findings are consistent with pre-
that continued practice of a task results in more vious short-term training studies of arm and hand
skilled control of movement, characterized by movements,[8,9,33] suggesting that ongoing neuro-
decreased amplitude and duration of muscle acti- muscular adaptations occur as a result of con-
vity,[8-10] decreased muscle co-activation[9,11,33] tinued training. The cross-sectional nature of the
and less variability of movement.[9,11,34] How- cycling and running studies is a clear limitation.
ever, these studies examined novel hand and arm However, given the limitations of the aforemen-
movements over a short training period (e.g. 1–2 tioned studies, and the difficulties of tracking
days), and their results provide little insight into athletes over many years of training, this is the
the adaptations of muscle recruitment that may strongest evidence of continuing neuromuscular
occur in response to years of continued training adaptations to endurance training available at
by athletes. Furthermore, there is very little present.
research that has directly measured the neuro-
muscular adaptations that occur in response to
Trained triathlete Trained cyclist Novice cyclist
endurance training such as cycling and running,
which involve repetitive, rhythmical actions. TA
Initial studies comparing muscle recruitment
patterns of trained cyclists to their novice coun-
TP
terparts presented conflicting findings and are
limited by small sample sizes, EMG methodo-
logical limitations, and inadequate regard for PL
kinematics (i.e. kinematics were not controlled or
measured and any difference in EMG activity GL
may have been due to kinematic changes).[35,36]
Similarly, running studies[37,38] are hindered by
SOL
the heterogeneity of participants and inadequate
inclusion criteria, making it difficult to determine 0° 180° 360° 0° 180° 360° 0° 180° 360°
the specific training status of included athletes. Crank angle Crank angle Crank angle
Only recently has evidence emerged that
Fig. 1. Rectified electromyogram (EMG) of tibialis anterior (TA),
trained cyclists and runners display different tibialis posterior (TP), peroneus longus (PL), lateral gastrocnemius
patterns of muscle recruitment to their novice (GL), and soleus (SOL) muscles during cycling at 77.5 rpm. Data for
ten non-contiguous pedal strokes from a representative highly
counterparts. Novice cyclists with 1.4 – 0.4 years trained triathlete, highly trained cyclist and novice cyclist are shown.
of cycling experience, who cycled 36.1 – 10.3 EMG amplitude is shown as a percentage of the maximum measured
amplitude (0–100%). Muscle activity is plotted for each complete
km/wk, exhibited greater individual variance (i.e. pedal stroke from upper vertical position of the crank (0) through to a
variability of muscle activity between pedal range of 360 (reproduced from Chapman et al.,[40] with permission).

ª 2009 Adis Data Information BV. All rights reserved. Sports Med 2009; 39 (11)
Neuromuscular Adaptations and Running Economy 907

3. Adaptation of Muscle Recruitment to activity similar to that of novice cyclists (figure 1).
Multidiscipline Endurance Training The authors suggested that the similarity of leg
muscle recruitment during cycling between highly
Multidiscipline endurance sports such as trained triathletes and novice cyclists may reflect
triathlon carry high training demands and are ongoing interference with motor learning and
likely to provide an immense challenge to the neuromuscular adaptation as a result of multi-
human motor control system. Triathlon com- discipline training.[40] Unlike cycling, multi-
prises sequential swimming, cycling and running, discipline training does not appear to adversely
and triathletes often practice two or more of these affect adaptation of running muscle activity in
disciplines in the one training session or practice highly trained triathletes.[41] The difference in leg
each discipline separately with only short re- muscle recruitment during cycling between
covery periods (i.e. 2–4 hours). Short-term motor triathletes and cyclists only highlights a disparity
learning studies (i.e. 1–7 days of training) provide between groups at a point in time. However, in
strong evidence that interference with acquisition order to provide stronger evidence that ongoing
of a new skill occurs when another task is prac- multidiscipline training interferes with adapta-
ticed in sequence or within short interim peri- tions of muscle recruitment, researchers would
ods.[42-45] Specifically, when multiple tasks are have to use a longitudinal motor learning para-
practiced in sequence or within short interim digm. This would require strict control of train-
periods (i.e. <6 hours), learning of the second ing structure and continued re-assessment over
movement task was biased by the previous task in years of training, and would be especially difficult
the sequence, and with each change of task, to undertake.
training adaptations were overwritten.[42-44,46]
These studies provide evidence of interference 4. Neuromuscular Characteristics and
with motor learning in the initial stages of train- Running Economy
ing. However, the nature of triathlon training
(i.e. athletes who practice multiple disciplines In the late 1980s, Noakes[48] suggested that
with no recovery periods or only short recovery endurance performance may be limited not only
periods) may provide an appropriate model to by aerobic power but also by ‘muscle power’
investigate the ability of the neuromuscular factors related to force and velocity character-
system to adapt (i.e. adaptations of muscle istics of the neuromuscular system. Later investi-
recruitment) to ongoing multidiscipline training. gations used a battery of tests to determine the
Evidence suggests that running and cycling influence of neuromuscular characteristics on
performance of triathletes is less than that for performance. In a homogenous group of. highly
cycling and running athletes who train for the trained endurance runners with similar VO2max
single discipline (i.e. those who only train for values, those athletes with faster 10 km and 5 km
running or who only train for cycling).[47] It could run times displayed shorter stance phase contact
be argued that the decrement in performance is times and higher relative muscle pre-activation
due to less time spent training the single discipline (i.e. prior to touchdown), accompanied with
despite similar total training times. However, lower relative electromyographic (iEMG) activity
Chapman et al.[40] have shown that patterns of leg during the propulsion phase than those athletes
muscle activity in highly trained triathletes with slower run times.[49,50] Furthermore, there
are less developed than in cyclists matched for was a significant correlation between running
cycling training loads. Specifically, triathletes economy and mean stance phase contact times
show greater variation between pedal strokes, during constant velocity running.[49] The authors
more extensive and variable muscle co-activity, speculated that in addition to aerobic power and
less modulation of muscle activity (i.e. greater running economy, the ability of the neuro-
amplitude of muscle activity in periods between muscular system to repeatedly produce rapid
primary bursts), and display patterns of muscle force during maximal and submaximal running

ª 2009 Adis Data Information BV. All rights reserved. Sports Med 2009; 39 (11)
908 Bonacci et al.

plays an important role in determining distance 900 Gluteus maximus

running performance in highly trained athletes. It


has been suggested that shorter stance phase 500
contact times and greater muscle pre-activation
may represent enhanced leg muscle stiffness,
leading to a faster transition from the braking to 100
propulsive phase of ground contact.[50,51]
Dalleau et al.[52] highlighted the importance of
neuromuscular factors by demonstrating that 900 Biceps femoris
running economy was related to the stiffness of
the propulsive leg, with greater stiffness eliciting
500
the best running economy.[52] Leg stiffness is
modulated by neuromuscular activation, and
changes in stiffness have been shown to occur as a 100
result of neuromuscular adaptation to training
(i.e. learning of more efficient or more skilled
patterns of motor recruitment).[53] In support of 900 Vastus lateralis
the association between motor recruitment and
leg stiffness, a reduction in EMG pre-activation
EMG (µV)

was shown to be significantly related to a de- 500

crease in post-landing leg stiffness following


fatiguing exercise.[54] Greater duration of muscle
100
co-activation of bi-articular leg muscles during
stance has also been significantly associated with
better running economy.[55] Muscle co-activation 700 Gastrocnemius
modulates leg stiffness during running and may
alter running economy through utilization of 500
stored elastic energy, which has no additional
metabolic cost. 300
Kyrolainen et al.[56] found that as running
100
speed increased so did EMG preactivation and
ground reaction forces, along with their rate of
force production (figure 2). Preparatory muscle
600 Tibialis anterior
function is an important function of the stretch
shortening cycle (SSC). The SSC is a combination
400
of a high velocity eccentric muscle contraction
followed immediately with a concentric contrac-
200
tion. SSC muscle function enhances performance
during the final phase (concentric action),[57] and
the increase in preparatory muscle activity with
higher running speeds was suggested to be a 200 ms
mechanism to tolerate higher impact loads, reg- Fig. 2. Muscle activity patterns of five muscles from the slowest
ulate landing stiffness[58] and improve running speed of 3.25 m/s (thin line; mean of 170 contacts) up to the maximal
economy.[56] However, in that study, the increase speed (thick line; mean of 34 contacts). Data are the mean rectified
electromyogram (EMG) measurements from a representative
in EMG activity may also be explained by the subject. The dashed lines indicate the respective EMG curves at
associated change in running kinematics with the three medium running speeds and the vertical lines indicate the
beginning of the contact phase. Note the greater EMG activity prior to
higher running speeds. A more recent study contact (i.e. preactivation) with higher running speeds (reproduced
showed that a greater ratio of eccentric to from Kyrolainen et al.,[56] with permission).

ª 2009 Adis Data Information BV. All rights reserved. Sports Med 2009; 39 (11)
Neuromuscular Adaptations and Running Economy 909

concentric vastus lateralis muscle activity was have recommended that alterations in running
associated with a lower metabolic demand during economy in highly trained distance runners must
running (i.e. better running economy).[59] exceed 2.4% to be confident a practically worth-
Taken together, the findings from these studies while change has occurred.
suggest that neuromuscular characteristics may
play an important role in running economy, 5.1 Resistance Training
especially in athletes with similar physiological
attributes. The timing and amplitude of muscle It is well documented that initial performance
activity has shown the most consistent asso- gains following resistance training are a result of
ciation with running economy. Greater muscle neuromuscular adaptations rather than within-
activity prior to and in the initial phase of ground muscle adaptations (i.e. hypertrophy).[72,73]
contact may enhance running economy by These adaptations include increased motor unit
increasing leg stiffness and maximizing exploita- recruitment and motor unit synchronization.[72-74]
tion of stored elastic energy. Resistance training may improve running econ-
omy through improved leg muscle coordi-
5. Training, Shoes, In-Shoe Orthoses, nation and co-activation and decreasing stance
Musculoskeletal Injury and Running phase contact times, thereby allowing a faster
Economy transition from the braking to the propulsive
phase through elastic recoil.[26,50,56,72] For resis-
Trained runners have a superior running tance training to improve running economy, a
economy to lesser trained or untrained run- positive ‘transfer of learning’ would need to oc-
ners,[22,23,60] indicating positive adaptations in cur. Transfer occurs when the training for one
response to training programmes. Training pro- task affects the performance or learning of a
grammes can potentially improve running eco- subsequent task. As a general principle, a positive
nomy through physiological, biomechanical and transfer would require that a specific pattern of
neuromuscular adaptations. Interventions such muscle recruitment associated with optimal per-
as altitude training and training in the heat are formance of a resistance training task enhances
aimed at improving cardiorespiratory function, running economy if it was expressed during run-
and have previously been reviewed in this jour- ning.[75] EMG analysis may allow for the identi-
nal.[3] Resistance training, plyometrics, stretching fication of the transfer of learning from resistance
and multidiscipline training are training inter- or plyometric training to running.
ventions that feasibly have the potential to alter In a group of . moderately trained female dis-
running economy through neuromuscular adap- tance runners (VO2max = 51 mL/kg/min), 10 weeks
tations. Passive physical interventions such as of traditional weight training combined with en-
use of shoes and in-shoe orthoses may also have durance training significantly improved . running
the potential to elicit similar effects on neuro- economy (4%) without any changes in VO2max.[24]
muscular control and running economy. Muscu- In further support of this training modality,
loskeletal pain and injury can result in a loss two further studies have reported a 7%[76] and
of training time and impaired neuromuscular 5%[77] improvement in running economy with
control,[61-64] with potential consequential altera- heavy resistance training (table I). Improvements
tions in running economy. In order to evaluate in maximal strength were reported in all experi-
the effect of injury and training interventions on mental groups, indicating positive neuromus-
running economy it is first useful to understand cular adaptations occurred. However, resistance
the typical intraindividual variation in this mea- training was performed in addition to normal
sure. Well controlled studies using moderate to endurance training volumes, therefore the im-
highly trained subjects report intraindividual provements in running economy may be related
variations in running economy of between 1.5% to the increased volume of training rather
and 5%.[65-71] Further to this, Saunders et al.[70] than the resistance training itself. Støren et al.[77]

ª 2009 Adis Data Information BV. All rights reserved. Sports Med 2009; 39 (11)
910 Bonacci et al.

Table I. Comparison of the effect of resistance and plyometric training programmes on running economy
Study (year) Subjects Volume Frequency Control Results
and duration strength/force RE
(%) (%)
Johnston et al.[24] (1997) 12 moderately 2–3 sets of 6–20 3 d/wk for Endurance › 24.4–33.8 › 4
trained runners RM in addition to 10 wk running
endurance training
Millet et al.[76] (2002) 15 highly trained 3–5 sets of 3–5 RM 2 d/wk for Endurance › 17–25 › 5.6–7
triathletes in addition to 14 wk training
endurance training (swim, cycle,
run)
Støren et al.[77] (2008) 17 moderately 4 sets of 4 RM in 8 wk Endurance › 33.2 › 5
trained runners addition to running
endurance training
Paavolainen et al.[26] (1999) 22 moderately 15–90 min/session 9 wk Endurance › 24.4–33.8 › 8.1
trained cross- running and
country runners circuit training
Turner et al.[78] (2003) 18 recreational 1 set of 5–25 reps 3 d/wk for Endurance 2 › 2–3
distance runners in addition to 6 wk running
endurance training
Spurrs et al.[79] (2003) 17 moderately 2–3 sets of 8–15 2–3 d/wk for Endurance › 11.4–13.6 › 4.1–6.7
trained runners reps in addition to 6 wk running
endurance training
Saunders et al.[80] (2006) 15 highly trained 30 min/session in 3 d/wk for Endurance 2 › 4
runners addition to 9 wk running
endurance training
highly trained = national/international level and maximal oxygen consumption >65 mL/min/kg; moderately trained = weekly running volume
>30 km/wk; RE = run economy; recreational = weekly running volume <30 km/wk; reps = repetitions; RM = repetition maximum; › indicates
increase; 2 indicates no change.

suggested the main training response from the et al.[26] examined the effects of substituting 32%
heavy resistance training was a change in muscle of endurance training hours with explosive
recruitment patterns, yet no direct measurement strength training over 9 weeks on selected neuro-
of muscle recruitment (i.e. EMG) was provided muscular characteristics and performance mea-
to support this notion. sures in moderately trained runners. Velocity of a
maximal 20 m sprint, distance of a series of five
5.2 Plyometric Training continual forward jumps and stance phase con-
tact times during constant velocity running were
Explosive resistance training or plyometrics is used as indirect measures of neuromuscular
a specific form of strength training that aims to characteristics. These variables are thought to
enhance the ability of muscles to generate power represent the ability of the neuromuscular system
through the SSC by use of explosive activities to repeatedly produce rapid force during intense
such as jumping, hopping and bounding.[78] exercise, and the capability to store and utilize
The SSC utilizes the ability of soft tissues to store elastic energy.[26,49,50] A significant improvement
and return elastic energy, thus reducing energy in 5 km run performance (3.1%), running econo-
expenditure.[81-83] It has been speculated that my (8.1%), five-jump distance (4.6%), and velo-
stiffness of the musculotendinous system may city over a 20 m sprint (3.4%) was found, along
determine the body’s ability to use such energy,[84] with a concurrent decrease in stance phase con-
and that plyometric training has the potential to in- tact times.[26] The authors suggested that the
crease musculotendinous stiffness.[79] Paavolainen improved performance was a result of enhanced

ª 2009 Adis Data Information BV. All rights reserved. Sports Med 2009; 39 (11)
Neuromuscular Adaptations and Running Economy 911

neuromuscular characteristics that were trans- economy following resistance training, these
ferred into improved muscle power and running findings add some weight to the model of en-
economy. durance performance described by Paavolainen
Three further studies have provided support et al.[49,50] whereby endurance performance is in-
that simultaneous plyometric and endurance fluenced by neuromuscular characteristics along
training improves running economy in moder- with aerobic power, and that endurance perfor-
ately and highly trained athletes[78-80] (table I). mance may be improved through enhanced
Proposed explanations for the improvement in- neuromuscular function. However, this premise
clude increased lower body musculotendinous is based on indirect measures of neuromuscular
stiffness, and enhanced muscle power develop- function and elastic energy return such as contact
ment and elastic energy return. Turner et al.,[78] times and vertical jump height. Enhancements in
however, reported no change in four indirect strength and power development during isolated
measures of the ability of the muscles to store and tasks may reflect neuromuscular adaptations but
return elastic energy following plyometric train- this has not been confirmed by more direct mea-
ing, despite an improved running economy. surements of muscle recruitment, such as EMG.
Countermovement jumps and static jumps on an Thus, it is not possible to infer that these adap-
inclined sled were used as measures of elastic tations translate into more efficient muscle
energy return as opposed to the running-specific recruitment patterns during running, or that they
measures described by Paavolainen et al.[26] The are responsible for the enhanced running economy
mechanics of jumping on a sled are different to following resistance and plyometric training.
the mechanics of running at speed and it is likely
that the measures used were insufficient to detect 5.3 Stretching
any change in elastic energy return during run-
ning. A direct method to quantify elastic energy There are two diametrically opposed hypo-
utilization has yet to be developed, yet there is a theses for the effect of stretching on energy
consensus that this phenomenon contributes to requirements. It has been suggested that if
economy of movement.[27,82,83,85] stretching decreases the visco-elastic properties of
It has been proposed that more efficient motor muscle and tendon,[89,90] then less energy may be
recruitment patterns as a result of training, whe- required to move the limb. Alternatively, the
ther at the neural or muscular level, may decrease decreased compliance may reduce the storage of
the oxygen cost at a given running velocity.[24] If elastic energy, increasing energy require-
the rate of force development and peak force ments.[91,92] Stretching has indeed been shown
is enhanced, a longer recovery period between to alter the compliance of human tendons
muscle contractions is possible, leading to in vivo.[93,94] There is also evidence to suggest that
improved muscle blood perfusion and thereby stretching induces acute neuromuscular effects.
improving economy.[86,87] In support of this, a Numerous studies have demonstrated a decrease
recent investigation found 8 weeks of concurrent in a muscle’s ability to produce force immediately
endurance and explosive strength training signif- after passive stretching,[95-99] along with de-
icantly improved leg extensor rapid force pro- creases in EMG amplitude during iso-
duction and activation, along with a significant metric[95,98,99] and concentric[97] muscle actions.
improvement in work economy (7% – 6%) during In contrast, an acute bout of assisted and un-
a constant velocity double-poling action in mod- assisted static quadriceps stretches did not alter
erately trained cross-county skiing athletes.[88] peak torque or EMG amplitude of the quadriceps
Despite the different mode of testing, the weight- muscle group during an eccentric muscle ac-
bearing nature of the double-poling test could tion.[100] A further study found that four sets of
indicate these results are applicable to running three different dynamic stretches did not alter
economy. While it is difficult to determine the peak torque, but increased EMG amplitude
exact mechanisms responsible for the improved of the biceps femoris muscle during maximal

ª 2009 Adis Data Information BV. All rights reserved. Sports Med 2009; 39 (11)
912 Bonacci et al.

isometric contractions at 81 and 101 knee flex- sures were not performed. In their subsequent
ion.[101] Methodological differences in the mode investigation with a larger population over a
(i.e. static vs dynamic) and duration of stretching 3-week period, Godges et al.[104] found no effect
may explain the inconsistent findings between the of stretching on running economy. Furthermore,
various studies. It is likely the observed neuro- the technique employed in their original study
muscular effects are specific to the mode of involved passive stretching at end of range with
stretching and the subsequent muscle activity restraints and suspended weights, a technique
(i.e. isometric vs isokinetic). Further research is that neither recreational nor elite athletes are
required to understand the differential effects of likely to employ. A recent systematic review
various modes of stretching on acute neuro- concluded that an acute bout of stretching pre-
muscular control during exercise. exercise may improve running economy, but
Early studies examined the relationship be- regular stretching over time has no effect on
tween flexibility and running economy. Gleim economy.[91] These findings do not suggest
et al.[102] found that untrained subjects with the stretching should be discounted as a training
least flexibility on a number of active and passive modality, because stretching exercises are
measures about the trunk and lower extremity commonly prescribed to running athletes for the
were more economical during walking and run- maintenance and promotion of range of mo-
ning. Similarly, Craib et al.[103] reported reduced tion,[107] especially after injury.
active hip external rotation and passive ankle
dorsiflexion range of motion was associated with 5.4 Multidiscipline Sports and Training
better running economy in moderately trained
distance runners. Both investigators attributed Impairments in overground[108,109] and tread-
the superior economy to increased storage and mill[110-113] running economy have frequently
return of elastic energy and a reduction in energy- been observed in moderately trained athletes
expensive stabilizing muscle activity, though they following cycling (i.e. when running ‘off-
did not provide evidence for these assumptions. the-bike’) compared with an isolated control
Most importantly, both these investigations were run. Further investigation in the same area found
correlative studies and neither study provides that running economy after maximal cycling is
evidence that altering flexibility through various not increased compared with a control run in
interventions will result in an enhanced running elite level triathletes.[114] The increase in oxygen
economy. consumption during running after cycling varies
To date, three studies have examined the ef- from 1.6% to 11.6% and is thought to be a reflec-
fects of stretching programmes on running eco- tion of ability level, with more experienced ath-
nomy in recreationally active athletes. Two letes displaying less impairment in running
of these found stretching over a period of economy.[115]
3 weeks[104] or 10 weeks[105] had no impact on Proposed explanations for the increased oxy-
running economy despite significantly improving gen consumption during running after cycling
flexibility. Conversely, Godges et al.[106] found include glycogen depletion,[108,109,113,115] ventila-
that an acute bout of end-range stretching re- tory muscle fatigue,[113] dehydration[108,109,112]
sulted in an immediate, significant reduction and leg muscle fatigue.[111,112] Hausswirth
(4–7%) in oxygen consumption at. workloads et al.[112] attributed the increased metabolic cost
equivalent to 40%, 60% and 80% VO2max. The of running at the end of a triathlon to bio-
discrepancies reported may relate to different mechanical variables such as stride length and
methodological procedures. The study by trunk gradient. In contrast, several others have
Godges et al.[106] was limited to seven subjects reported no change in running kinematics fol-
with tight hip flexor or extensor muscles. In lowing cycling.[109,113,116,117] A recent review
addition, running economy was only measured suggested that if the consequence of previous ex-
immediately post-stretching and follow-up mea- ercise is to reduce subsequent running economy,

ª 2009 Adis Data Information BV. All rights reserved. Sports Med 2009; 39 (11)
Neuromuscular Adaptations and Running Economy 913

then it is more likely to be through physiological cycling.[3] However, it is probable that alterations
rather than biomechanical factors.[3] While this in patterns of muscle recruitment after cycling
seems the most logical rationale, it fails to con- may also be a contributing factor to the increased
sider the influence of the neuromuscular system, metabolic cost of running in some athletes.[120]
and the possibility that movement patterns may Two recent studies have indeed shown that
be preserved but muscle activity altered.[116] The alterations in run performance after variable
transition from bike to run involves a switch cycling compared with steady-state cycling may
from a predominantly concentric type of muscle occur in the absence of physiological changes.
activity to a combined eccentric-concentric Run time to exhaustion was found to be signi-
action.[114,115] This requires rapid neuromuscular ficantly greater following a variable cycling
adjustments to be made in order to effectively intensity (–20% of 90% lactate threshold) com-
utilize stored elastic energy. The quantity of pared with a constant intensity (90% of lactate
elastic energy stored and re-used is influenced by threshold).[121] Conversely, a 5 km run time trial
leg stiffness, and lower limb stiffness has been was significantly better (4.4%) following a 20 km
shown to be correlated to running economy.[52] constant intensity cycle compared with a variable
Only neuromuscular activation is able to mod- intensity cycle.[122] Although these are conflicting
ulate leg stiffness.[52] findings, both protocols that reported improve-
Initial EMG studies of the cycle-run transition ments in run performance completed the final
report small and sometimes only transient chan- stages of the cycle leg as a low intensity segment.
ges in muscle activation that may be attributed to Hence it appears that completing the final
alterations in kinematics, running speed or fati- stages of the cycling phase at a high intensity is
gue.[118,119] More recently, Chapman et al.[116] detrimental to subsequent run performance.
used a new paradigm to discriminate the influ- Interestingly, despite considerable within-subject
ence of fatigue and altered running speed on leg changes .in run performance, no differences in
kinematics and muscle activation. They found average VO2, ventilation, heart rate or rating of
that a select proportion of highly trained triath- perceived exertion were detected between the
letes (30%) exhibited muscle activity in the post- controlled or variable conditions during both the
cycling run leg that more closely resembled cycle and the subsequent run leg. While cycling at
that used during cycling rather than the muscle a lower intensity in the final portion of the
activity used during the control pre-bike run. The cycle leg may allow for a greater metabolic re-
altered muscle activity was evident as soon as covery,[121] it is also possible that alterations in
running commenced and persisted for the dura- neuromuscular control may be responsible for
tion of the 30-minute run off-the-bike. Moreover, the difference in run performance.
despite the altered muscle activity, no changes in A recent study with a small sample size of
running kinematics were observed. As only the triathletes demonstrated a similar magnitude of
tibialis anterior muscle was investigated, further neuromuscular fatigue following constant-versus
work is required to determine if similar altera- variable-intensity cycling.[123] The authors con-
tions in activation exist in the other leg and thigh cluded that in the field of triathlon, variations
muscles. in run performance cannot be attributed to dif-
Interference with execution of optimal pat- ferent levels of neuromuscular fatigue following
terns of muscle recruitment when switching from constant-versus-variable cycling. Perhaps then it
cycling to running may alter muscle stiffness is the change in lower limb muscle coordination
regulation and hinder the athlete’s ability to during running after cycling,[116] independent of
effectively utilize elastic energy during run- neuromuscular fatigue, that contributes to the
ning.[120] Recovery of elastic energy is known difference in run performance. Further work ex-
to reduce energy expenditure.[81-83] Certainly, amining lower limb muscle coordination during
physiological stress appears to be the primary running after cycling is required to explore this
reason for the increased cost of running after supposition.

ª 2009 Adis Data Information BV. All rights reserved. Sports Med 2009; 39 (11)
914 Bonacci et al.

5.5 Shoes and In-Shoe Orthoses economy. Oxygen consumption and EMG acti-
vity during running were compared between a
With every ground contact during running, medium hardness elastic shoe and a softer viscous
energy is transferred between the athlete and shoe. They found that running economy re-
supporting surface. The interaction between the sponses to the shoes were highly individual, i.e.
athlete and surface is coupled by the shoe and some athletes consumed less oxygen for the
insert or orthoses. Theoretically, performance elastic shoe condition while others consumed less
can be influenced by the shoe and shoe insert or for the viscous shoe condition. The EMG data
orthosis through its mass, its potential to change also showed muscle- and subject-specific re-
movement patterns and alter muscle activity, and sponses to the shoes. An interesting finding was
by minimizing the energy that is lost by the ath- that all runners who consumed more oxygen
lete.[124,125] In a landmark review paper, Nigg in the viscous shoe showed higher vastus medialis
et al.[126] proposed a new concept for use of shoes, pre-activation in that shoe; similarly, the runners
inserts and orthoses in sport: (i) the skeleton has a who consumed more oxygen in the elastic
preferred path for a given movement task; (ii) if shoe demonstrated higher vastus medialis pre-
an intervention (shoe, insert, orthoses) supports activation in that shoe. This seems counter-
the preferred path, muscle activity can be re- intuitive, given that EMG pre-activation is
duced; (iii) an optimal shoe, insert or orthosis thought to modulate leg stiffness and enhance
feels comfortable because it reduces muscle acti- elastic energy return, which has been shown to be
vity and the resulting fatigue; and (iv) perfor- metabolically more efficient.[52,54,58] However, all
mance should increase with an optimal shoe, changes in running economy were £2.0% and the
insert or orthosis since muscle activity is minimized running economy and EMG measurements were
and thus energy expenditure is reduced. Early not made simultaneously, so it is difficult to draw
work has indeed shown that orthoses elicit short- any solid conclusions from this study other than
term effects on lower limb muscle activity during that changes in running economy and muscle
walking and running.[14-16,127] The demonstrated activity with different shoes are subject specific.
changes in muscle activity have shown high Surprisingly, the effect of orthoses on running
intersubject variability,[14-16,127] indicating the economy has received very little attention, despite
individual nature of neuromuscular responses to being commonly prescribed to running athletes.
orthoses. Furthermore, no studies have simultaneously
Shoe mass is an example of how manipulation measured running economy and EMG activity of
of footwear can affect energy requirements. the leg muscles. The studies that have investi-
When different types of footwear were compared gated the effect of orthoses on muscle activity
it was found that wearing heavier models signi- have shown high intersubject variability in the
ficantly elevated oxygen consumption in trained EMG responses to orthoses.[14-16,127] Whether the
runners without concomitant changes in stride changes in muscle activity associated with ortho-
length.[128] When identical shoe types are mod- sis prescription correspond to an alteration in
ified only with respect to their mass, oxygen running economy has yet to be determined.
consumption is significantly greater with the Three studies have investigated the direct effect
heavier shoes during walking and running.[129,130] of orthoses on running economy. Two of the stu-
Modifying shoe material properties can also dies found that running economy was not altered
influence economy of locomotion. The use of air- with orthosis use in recreational[132] and moder-
soled shoes elicited a superior running economy ately trained runners.[133] In contrast, the other
compared with regular ethylene vinyl acetate study found that both flexible and semi-rigid
(EVA), midsoles in trained distance runners.[131] orthoses significantly increased oxygen consump-
Nigg et al.[17] attempted to verify their concept of tion in runners who had a history of running-
an optimal shoe by examining the effect of shoe related injuries.[134] This is the only investigation
materials on lower limb EMG and running that included a symptomatic population, to whom

ª 2009 Adis Data Information BV. All rights reserved. Sports Med 2009; 39 (11)
Neuromuscular Adaptations and Running Economy 915

orthoses are commonly prescribed as a tool for targeted interventions, the specific neuromuscular
symptomatic relief. However, no detail was given impairments that occur following injury[61-64,139]
as to the type or site of injury, the mechanism of may persist well after the athlete has returned to
injury or current state of symptoms. Further- training and competition.
more, analysis of data reveals the increase in The literature to date fails to provide any in-
oxygen consumption when running in rigid sight into the possible effect that any injury in an
and flexible orthoses was only 2.0% and 1.7%, endurance athlete may have on running econo-
respectively, which is within intraindividual my. Therefore, to explore this area we present
variation[66,68,70,71] and may not be a practically some available evidence from a wider model.
worthwhile change.[70] There is some evidence that walking gait econo-
Taken collectively, it is likely that orthoses my is decreased in those with knee joint osteo-
elicit subject-specific short-term effects on neuro- arthritis – a progressive form of musculoskeletal
muscular control during running, but there is in- injury and pain.[143-146] Anterior cruciate-
sufficient evidence to date to support the concept deficient patients have also demonstrated an 8%
proposed by Nigg et al.[126] that an optimal ortho- decrement in running economy compared with
sis reduces muscle activity, minimizes energy healthy controls,[147] and anterior cruciate liga-
expenditure and improves run performance. ment deficiency has been associated with in-
creased hamstring muscle activity during running
5.6 Musculoskeletal Injury and cutting manoeuvres.[141,142] Whilst these in-
juries and the activities used to test economy
Musculoskeletal overuse injury is arguably the (e.g. walking economy) only partially resemble
most significant adverse effect of participation in the routine laboratory test intensity, and injuries
endurance exercise and constitutes a major im- sustained by endurance athletes, they provide
pediment to participation in physical activity. a snapshot of how musculoskeletal injury may
The knee and shin are the most common sites affect running economy in endurance athletes.
of injury in endurance athletes,[135-137] and the Exercise-induced muscle damage (EIMD) is a
majority (50–75%) of all running injuries are further paradigm with which to investigate the
reported to be overuse in nature.[135,137,138] effect of musculoskeletal pain and injury on
Alterations in neuromuscular control – in- performance. EIMD occurs after performing
cluding muscle imbalances, altered muscle unaccustomed exercise or exercise of increased
timing, muscle fatigue and muscle weakness – intensity or duration; it results in muscle stiffness,
have been associated with musculoskeletal swelling, impairment of muscle function and
injury and pain in numerous independent delayed-onset muscle soreness.[148] For a compre-
reports.[61-64,139,140] Unfortunately, much of the hensive review of the alterations in neuromus-
research has been retrospective, and our under- cular function that follow EIMD the reader is
standing of overuse injury causation is limited. directed to a recent review in this journal.[148] In
Moreover, knowledge of the direct effect of short, documented outcomes of EIMD include
musculoskeletal injury and neuromuscular im- reflex inhibition of muscle activity, decreased
pairments on running economy is limited. While strength and power-generating ability, and a de-
it is presumed that injury and subsequent pain crease in the force to electromyographic (iEMG)
and functional impairments hinder performance activity ratio.[148] In relation to performance,
through loss of training hours and competition, EIMD from a bout of isokinetic resistance
many athletes may continue to participate with exercises[149,150] and downhill running[151] did not
sequelae of injury (e.g. pain, swelling, proprio- alter running economy in recreationally active
ceptive deficits). Furthermore, alterations in subjects.[149-151] In contrast, a 3.2% reduction in
muscle recruitment that occur with injury and running economy and stride length was found
ensuing pain have been exhibited up to 66 months 48 hours after performing a single bout of
post-injury.[141,142] It is possible that without downhill running (resulting in considerable

ª 2009 Adis Data Information BV. All rights reserved. Sports Med 2009; 39 (11)
916 Bonacci et al.

muscle soreness) in moderately trained triathletes leg muscle recruitment during running remains
and distance runners.[152] Perhaps changes in unknown.
running economy and kinematics due to EIMD The adverse effect of cycling on subsequent
are less sensitive in untrained subjects because of running economy in triathletes is most likely due
their less refined movement and muscle activity to physiological stress, although alterations in
patterns. A similar protocol using trained and muscle recruitment patterns should not be dis-
untrained subjects may provide further support counted as a potential contributor. There is in-
for this idea. sufficient evidence for the alteration of running
economy through stretching, shoe material
6. Conclusions modifications, in-shoe orthoses and musculoske-
letal injury in endurance athletes. Exercise-
The purposes of this review were to: (i) examine induced muscle damage reduces running economy
the adaptations of lower limb muscle recruitment in moderately trained athletes through altera-
(i.e. neuromuscular adaptations) to different tions in kinematics, which may be associated with
modes of training (i.e. running, cycling, multi- changes in neuromuscular control.
discipline); (ii) examine what aspects of neuro-
muscular control are associated with running 7. Future Directions
economy; and (iii) examine whether neuromuscular
adaptations induced by training, passive inter- Future sport performance research needs to
ventions and injury can be coupled with changes consider the role of the neuromuscular system in
in running economy. It had previously been endurance activities. The available evidence sug-
assumed that superior cycling and running gests that adaptations of leg muscle recruitment
performance was evidence for greater neuro- do occur in response to ongoing endurance
muscular adaptation in trained athletes. Recent training. Research is yet to establish the optimal
scientific knowledge supports this belief, with duration and intensity of training to promote
evidence that ongoing single-discipline training these adaptations and whether further improve-
leads to more refined patterning of leg muscle ments can be achieved through training inter-
recruitment. This is thought to be a positive ventions once at the elite level. These questions
neuromuscular adaptation to endurance training, warrant future investigation. Further knowledge
which may reduce metabolic demand and en- of the relationship between leg muscle recruit-
hance performance. A difference in leg muscle ment and running economy may divulge
recruitment during cycling has been demon- information about optimal patterns of muscle re-
strated between multi- and single-discipline cruitment for economical running. Measurement
athletes. This highlights a difference in neuromus- of leg muscle recruitment pre- and post-training
cular adaptation to single- and multidiscipline interventions would help explain whether run-
training. However, it is uncertain whether these ning economy is altered through adaptations in
specific neuromuscular adaptations are beneficial leg muscle recruitment.
or detrimental to sport-specific endurance per- In recent times, investigators have directed
formance. their attention to the neuromuscular effects of
Available evidence suggests that in athletes shoes and in-shoe orthoses. The available evi-
with similar physiological attributes, neuromus- dence suggests that changes in leg muscle activity
cular characteristics play an important role in with various shoe materials and orthoses may be
endurance running performance. The consistent specific to an individual, and thus an optimal
finding from studies of improvements in running shoe or orthosis for performance would also re-
economy following strength and plyometric quire individual consideration. However, the
training appears related to neuromuscular adap- relationship between shoes, in-shoe orthoses,
tations (e.g. improvements in strength, force muscle activity and performance remains unclear
production). Whether these adaptations alter and requires further investigation.

ª 2009 Adis Data Information BV. All rights reserved. Sports Med 2009; 39 (11)
Neuromuscular Adaptations and Running Economy 917

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