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[ clinical commentary ]

DUSTIN GROOMS, MEd, ATC, CSCS1 • GREGORY APPELBAUM, PhD2


JAMES ONATE, PhD, ATC, FNATA1

Neuroplasticity Following Anterior


Cruciate Ligament Injury:
A Framework for Visual-Motor
Training Approaches in Rehabilitation
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A
nterior cruciate ligament (ACL) rupture is a common chanical factors, such as muscle strength,
activity-related knee injury that usually requires surgical balance, and plyometric function, and
give less consideration to cognitive or
reconstruction to restore knee stability and function.140 The
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

neurological components.60,107,109,156 While


lifetime burden of ACL injury ranges from $7.6 to $17.7 rectifying the biomechanical profile and
billion per year in the United States.96 Despite surgical reconstruction restoring muscle strength are vital compo-
and physical rehabilitation, injury of the ACL dramatically increases nents of the rehabilitation process, there
the risk for costly and long-term disabling osteoarthritis, associated may be more potential to improve func-
tion and decrease reinjury risk.58,99 Recent
decreased lifelong physical activity, and rate is further compounded by the inabil- reports have found unresolved neuroplas-
decreased work productivity.4,14,93,96 Im- ity of a majority of individuals to return to tic alterations after injury, reconstruction,
portantly, reconstruction and rehabili- preinjury levels of activity.10 and rehabilitation that may limit function
Journal of Orthopaedic & Sports Physical Therapy®

tation that rely primarily on traditional Although evidence supports neuro- and return to sports participation.9,17,87,94
neuromuscular interventions have a fail- muscular training for effective injury By targeting these neurologic factors and
ure rate of up to 30% for rerupture after prevention and rehabilitation, many of integrating neurocognition during neuro-
return to sport.74,120,121,154 This high failure these approaches primarily target biome- muscular rehabilitation progressions, it
may be possible to improve the transfer of
sensorimotor adaptations from the clinic
TTSYNOPSIS: The neuroplastic effects of anterior neurocognitive and visual-motor approaches with
to activity, and ultimately to improve pa-
cruciate ligament injury have recently become traditional neuromuscular interventions during
more evident, demonstrating underlying nervous tient outcomes.16,61
anterior cruciate ligament injury rehabilitation.
system changes in addition to the expected me- Physical therapists, athletic trainers, strength The training, and even restoration, of
chanical alterations associated with injury. Inter- coaches, and other health care and performance primarily biomechanical factors relative
ventions to mitigate these detrimental neuroplastic to ACL-injury risk67,132 may not address
professionals can capitalize on this integration
effects, along with the established biomechanical all the physiologic consequences of in-
of sciences to utilize visual-training technologies
changes, need to be considered in the rehabilita-
tion process and return-to-play progressions. This and techniques to improve on already-established jury, as patient-reported dysfunction and
commentary establishes a link between dynamic neuromuscular training methods. poor movement control may persist for
movement mechanics, neurocognition, and visual TTLEVEL OF EVIDENCE: Therapy, level 5. J Or- years.8,108,119,129,131,158 The impaired physi-
processing regarding anterior cruciate ligament thop Sports Phys Ther 2015;45(5):381-393. Epub cal performance and patient-reported
injury adaptations and injury risk. The proposed dysfunction might, in part, have a neu-
10 Jan 2015. doi:10.2519/jospt.2015.5549
framework incorporates evidence from the
TTKEY WORDS: ACL, motor control, neuroscience,
rologic origin.79,84,123 The capacity for
disciplines of neuroscience, biomechanics, motor
control, and psychology to support integrating return to sports neuroplasticity after injury and during
therapy may present an opportunity to

School of Health and Rehabilitation Sciences, College of Medicine, The Ohio State University, Columbus, OH. 2Department of Psychiatry and Behavioral Sciences, Duke University,
1

Durham, NC. The authors certify that they have no affiliations with or financial involvement in any organization or entity with a direct financial interest in the subject matter or
materials discussed in the article. Address correspondence to Dustin Grooms, The Ohio State University, School of Health and Rehabilitation Sciences, 453 West 10th Avenue,
228C Atwell Hall, Columbus, OH 43210. E-mail: Dustin.Grooms@osumc.edu t Copyright ©2015 Journal of Orthopaedic & Sports Physical Therapy®

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[ clinical commentary ]
close the gap between rehabilitation and place high demand on cognitive and ACL Injury–Induced Sensory and
activity by targeting a broader spectrum sensorimotor processes and, in turn, Visual-Motor Processing Compensations
of sensorimotor function during neuro- increase ACL reinjury risk.26,68,82,88 In To better understand the rationale for
muscular training.58,64,108,109 Alternative a constantly changing environment, how visual-motor training may enhance
approaches and adjunct therapies may the sensory system’s 3 primary afferent ACL-injury rehabilitation, a thorough
help to address the neurological sys- pathways (vestibular, visual, and so- understanding of the current evidence
tem functions associated with the faulty matosensory) provide the complex and on neuroplastic changes associated with
movement patterns underlying ACL rein- integrated information necessary for ACL injury is required. The overarching
jury risk.18,87,94,121 the efferent neuromuscular control sys- concept is that the CNS afferent input is
As an example, typical rehabilitative tem to maintain adequate stability and disrupted due to the lost somatosensory
exercises are completed with an internal control.95,153 One area of sensorimotor signals from the ruptured ligament and
focus of control, meaning that full atten- function that may uniquely be affected increased nociceptor activity associated
tion is directed to the internal aspects by ACL injury is motor control requir- with pain, swelling, and inflammation.
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of the movement only (eg, avoidance of ing visual feedback.95 The visual system The disrupted sensory input and inju-
excessive knee valgus or increasing knee provides a fundamental mechanism for ry-associated joint instability, muscle
flexion).20,155,156 Internal focus can offer coordination, regulation, and control of atrophy, and movement compensations
positive benefits early in rehabilitation, movement while managing environmen- combine to facilitate motor control adap-
when the need to develop or restore a tal interactions (external focus).122,139,150 tations. The reconstruction process leads
motor pattern or muscle contraction Visual feedback is especially needed in to further deafferentation of the joint,
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

ability is vital. But, function in the ath- executing movement sequences5,111 and causing continued neuroplastic modifica-
letic environment, or even in activities increasing task complexity and variabil- tions that result in maladapted efferent
of daily living, requires constant interac- ity.40,89,128,150 The interplay between vision neuromuscular output (FIGURE 1).
tions with the dynamic and constantly and somatosensation is particularly vital
changing visual environment. Sport and to provide sufficient afferent input to the CNS Adaptations
activities of daily living therefore require central nervous system (CNS) to regu- In animal models, the ACL mechanore-
an external focus of control, where at- late motor control and to maintain neu- ceptor and afferent connections can be
tention is directed to the environment romuscular integrity during action and traced within the nervous system to the
and the body relies on automatic mo- environmental interaction.133,134,143,149,153 spinal cord, brain stem, and cerebral
Journal of Orthopaedic & Sports Physical Therapy®

tor control to maintain joint-to-joint In this sensory-to-motor feedback loop, regions, contributing to proprioceptive,
integrity.11,41,128 changes to visual or sensory feedback nociceptive, and reflex function.59,118 The
The need to challenge a broad spec- lead to subsequent alterations in neu- initial sensorimotor neuroplasticity after
trum of sensorimotor control is demon- romuscular control during movement ACL injury is likely caused by the abrupt
strated by the noncontact ACL-injury (closed-loop processing).23,95,133,143,150,153 loss of this connection, which once pro-
scenario: a failure to maintain knee neu- Trauma to the ACL has been shown to vided the nervous system with continu-
romuscular control while attending to modify how the nervous system pro- ous feedback. In human studies, the
an external focus of attention, involving cesses these interactions between vision afferent loss is demonstrated by altered or
highly complex dynamic visual stimuli, and somatosensation.2,3,55,79,115 Targeting absent somatosensory-evoked potentials
variable surfaces, movement planning, injury-induced sensory-motor plastic- with stimulation of the common peroneal
rapid decision making, variable player ity presents a unique opportunity to im- nerve37,39,147,148 or the ACL directly.125 The
positions and environment interactions, prove the translation of neuromuscular loss of primary afferent information com-
and unanticipated perturbations.26,68,82,88 system enhancements from the reha- bined with the pain and inflammatory
The need to bridge the intense neuro- bilitation environment to the return- response contribute to fundamentally
cognitive and motor control demands to-sport environment.29,76,100 Thus, our alter the somatosensory feedback.32,75,79,91
of sport during rehabilitation may purpose in this commentary is to high- The disrupted input, combined with me-
therefore benefit from specific interven- light the contributions of nervous sys- chanical changes and compensations110,131
tions that target these neurocognitive tem function and reorganization in the (contralateral loading,15,119 hip or ankle
factors in addition to the biomechani- ACL-injury rehabilitation process, and strategies48,56), facilitates the adaptations
cal techniques that are already widely specifically how adding visual-motor ap- for motor control.68,128,129 On a founda-
addressed. proaches during neuromuscular training tional level, altered motor output mani-
The transition from rehabilitation may mitigate potentially limiting factors fests in disrupted gamma motor neuron
to sport activity is challenged by com- during return to high-demand physical function83,85,86 and perturbation reflex-
plex environmental interactions that activities. es,38,44 which play a key role in the abil-

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This partial deafferentation is further il-
• Afferent input disrupted lustrated by investigations utilizing tran-
Sensory
neuroplasticity • Somatosensory processing altered scranial magnetic stimulation to assess
the CNS efferent pathway between the
quadriceps and the brain.65,90,113,123 Her-
oux and Tremblay65 reported enhanced
• Inhibited joint position and motion detection resting corticomotor excitability in those
Proprioception
• Depressed somatosensory contribution to motor control with ACL injury. A potential mechanism
for increased resting motor cortex excit-
ability may be due to the affected sen-
sory feedback, as the brain attempts to
Motor • Efferent output altered
maintain motor output with attenuated
neuroplasticity • Motor processing requires more planning
sensory input. This increase in excitabil-
and visual feedback
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ity may increase potential feedforward


mechanisms by decreasing the thresh-
old for connections with motor plan-
Postural control • Decreased stability without
ning areas, or allow for increased input
visual feedback
from other sensory sources (vision, ves-
tibular).62,116,144,159 A recent neuroimaging
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

investigation by Kapreli et al79 provides


• Visual feedback further evidence of the neuroplastic ef-
Movement
reliance to maintain
control fects of ACL injury. They performed func-
neuromuscular control
tional magnetic resonance imaging of
the brain during knee flexion and exten-
FIGURE 1. The conceptual framework for neurologic and visual-motor adaptations after ACL injury, a cascade of sion, and found that those with an ACL
neuroplasticity following ACL injury that contributes to visual feedback dependence to maintain neuromuscular injury had increased activation of the
control. Abbreviation: ACL, anterior cruciate ligament.
presupplementary motor area, posterior
secondary somatosensory area, and pos-
Journal of Orthopaedic & Sports Physical Therapy®

ity to maintain neuromuscular integrity roplasticity and altered mechanical and terior inferior temporal gyrus compared
in a changing environment that requires biological function of the joint combine to matched controls.79 The presupple-
rapid and precise muscle stiffness or ac- to reduce proprioception acuity as mea- mentary motor area is highly involved in
tivation strategies.30,81,145 The lost ability sured by joint position sense,27,92 move- complex motor planning,12,111 and, despite
to rely on reflex and gamma motor neu- ment detection,27,54 and force sense.66 To the relative simplicity of the movement
ron drive to prepare alpha motor neuron investigate the neurologic adaptations of task (single-joint movement of 40° of
function requires the CNS to engage in functional sensory loss, Baumeister et knee flexion/extension while lying su-
supplementary mechanisms, such as in- al17,18 used electroencephalography during pine), those with an ACL injury needed to
creased utilization of visual feedback, to force- and joint-sense tasks and found engage higher-level motor control areas
maintain the required sensory input for that those with ACL reconstructions had to a greater degree to execute the move-
motor control. As such, neuromuscular greater brain activation in attentional ment. This increased activation may indi-
control after ACL injury may require and sensory areas. The increased acti- cate that, on a neural control level, simple
enhanced visual feedback, depriving the vation may be attributed to less neural movements are more taxing to those with
CNS of resources once used for managing efficiency or increased neural load to a previous ACL injury.104 The increase in
environmental interaction to maintain complete the same task; interestingly, posterior secondary somatosensory area
knee joint stability. despite increased cortical activation, pro- provides further evidence of sensory-
These deficits in neural function are prioceptive performance was still worse based neuroplasticity after injury, as this
not rectified with ACL reconstruction in those with ACL reconstruction as com- area is involved in regulating painful
and may become even more pronounced pared to controls.17,18 These results indi- stimuli but is highly interconnected with
and/or present bilaterally.24,83,84,87,94,130,148 cate that the loss of the native ACL not the anterior secondary somatosensory
The bilateral motor control, reflex, and only constitutes a mechanical instability area that integrates somatosensory in-
proprioceptive changes are theorized to but also a degree of nervous system deaf- puts.33,49,145 Interestingly, the participants
be due to both spinal59,118 and supraspi- ferentation that is not rectified with re- in the study did not report pain during
nal39,123 mechanisms.124 This ongoing neu- constructive surgery and rehabilitation.78 the movement, conceivably indicating

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[ clinical commentary ]
a sensory processing adaptation from
the initial increase in nociceptive input Injury: structure damage
from the traumatic nature of the injury.
Alternatively, the prolonged nature of
the rehabilitation, chronic pain, or joint
instability may continue to disrupt typi- Neuromuscular control adaptations
cal somatosensory-system afferent inte- • Depressed somatosensory-motor control
gration. The posterior inferior temporal • Increased visual feedback dependence
gyrus plays a role during many cerebral
functions,25,28 but may primarily be in-
volved with visual processing of move-
ment.122 As such, an increase in posterior
inferior temporal gyrus activation during
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movement may indicate that, in response Integrated sensory and visual-


Traditional training
to ACL injury, there is an increased uti- motor training
Compensatory Plasticity

lization of visual processing and motor +

Adaptive Plasticity
+
planning resources for movement con-
current with depression of somatosen- Utilization of vision via motor Utilization of somatosensation via
control compensations modified visual feedback
sory function.37,39,55,79,147,148
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

= =
Biomechanical Adaptations
Compensatory sensorimotor control Adaptive sensorimotor control
These neuroplastic observations follow- strategy strategy
ing ACL injury are further supported by
biomechanical evidence suggesting that
FIGURE 2. Conceptual training model. The top indicates the neuromuscular cascade of events postinjury, the left
with increased task complexity, neu- column is the traditional training model reinforcing the visual feedback overreliance for motor control, and the
romuscular control is deteriorated in right column indicates the proposed integration of modified visual feedback training to decrease visual reliance
individuals with an ACL injury or re- and improve sensory-motor function.
construction to a greater extent than in
Journal of Orthopaedic & Sports Physical Therapy®

controls, possibly due to overload of in healthy athletes with the addition of a and greater reliance on visual feedback.
motor planning resources.73,112 The spe- defender,102 a virtual soccer interface,36 or This ACL injury–induced neuroplasticity
cific neuroplastic visual-motor control a level of unanticipated decision making can have consequences for function and
adaptation is observed during static during the task (selecting direction).101,126 further injury risk, as the visual feedback
balance, as those with ACL injury have The effect of occupying the visual system and motor planning neural mechanisms
significantly diminished postural control with environmental cues during landing become overloaded in the athletic envi-
when vision is obstructed (blindfold or or change of direction is even greater in ronment. Specific additions to current
eyes closed),114,115 but limited to no deg- those with a history of ACL injury.72,73 neuromuscular interventions targeting
radation in postural control with eyes These findings, taken together, sug- these neuroplastic imbalances may play
open, as they are able to use vision to gest that ACL injury may lead to a a significant role to induce sensorimo-
compensate and maintain balance.69,97 A cascade of neuroplastic and neuromus- tor adaptations to decrease dependence
more pronounced effect on neuromuscu- cular alterations that increase reliance on visual feedback when transitioning to
lar control is observed when disrupting on visual feedback and cortical motor more demanding activities.
visual-motor processing during complex planning for the control of knee move-
landing and cutting maneuvers that play ment. The postinjury disrupted sensory Visual-Motor Training
an even greater role in injury risk.102,103,142 feedback, combined with the observed as a Rehabilitation Tool
The simple addition of a target during a motor compensations, contributes to Typically, neuromuscular interven-
jump-landing task increased injury risk fundamentally alter the CNS mecha- tions (eg, plyometrics, balance training,
mechanics52 and altered muscle activa- nisms for motor control.1,17,18,80,94,147,148,160 strengthening exercises) allow full focus
tion, decreasing postural stability.152 The In attempting to regulate neuromuscu- of attention on the movement, whereas
effects of forcing visual focus on the en- lar control in the presence of decreased in sporting situations this is rarely the
vironment during more complex cutting somatosensory input, the nervous system case.88,98 Traumatic injuries (ACL rup-
or direction-change tasks further de- supplements with increased motor plan- tures) tend to occur during complex
grade neuromuscular control capability ning, conscious cortical involvement, game situations when the player must

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ity).2,17,18,20,55,61 Disrupting visual feedback
as an adjunct to traditional rehabilita-
tion may more closely mimic actual ac-
tivity demands via escalated load on the
neurocognitive system36,52,98,102,152 and
smooth the transition back to activity by
providing a closer analog to the inherent
environmental challenges of sport.95,98
Historically, the primary method to dis-
rupt the visual feedback system has been
to use complete visual obstruction (eyes
closed or blindfold). This kind of visual
deprivation presents a motor control
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challenge in a healthy population133 and


has a more pronounced effect in indi-
viduals with an ACL injury.55,115 However,
FIGURE 3. Strobe glasses. The top series of pictures provides an example of a first-person perspective with the rehabilitation using eyes-closed or blind-
glasses set at a moderate level of occlusion (approximately level 5 or 6, with a 150- to 233-millisecond opaque folded conditions55 has been restricted to
interval). The 3 pictures demonstrate the 100-millisecond transparent intervals of vision with the opaque condition
removed from the illustration. The bottom series of pictures depicts the opaque condition on the left and the clear
static balance,115 proprioceptive,55 or sim-
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

condition on the right. These conditions continuously alternate and have 8 settings, in which the clear condition plified single-movement34,133 tasks. The
always lasts 100 milliseconds and the opaque conditions may be controlled to last from 25 to 900 milliseconds. influence of modifying the visual input
by any means (ball, defender, blindfold,
manage multiple variables (eg, ball, plexities increase.19,46,76,77 Currently used target, visual signals) during more chal-
players, field position, game strategy) rehabilitative methods may even be fur- lenging dynamic tasks, such as rapid di-
requiring full visual attention to the en- ther contributing to the neuromuscular rection change or jump landing, has an
vironment, theoretically leaving less control compensations and facilitating even greater effect on neuromuscular
cognitive processing resources for neu- possible compensatory neuroplasticity control.34,36,52,133,152
romuscular control.26,68,71,82,88,98 These en- (FIGURE 2).17,18,65,79,83,87,129 Recognizing and
Journal of Orthopaedic & Sports Physical Therapy®

vironmental demands and the increased addressing the specific postinjury neuro- Direct Visual Disruption
need for visual feedback for knee con- plasticity during neuromuscular training Ideally, inhibiting visual input during
trol in individuals after ACL injury55,79,115 may provide an avenue for the clinician to these dynamic, more athletic maneu-
combine to create a higher-risk state for address both the physical and neurocog- vers would provide a means to directly
the athlete. This framework indicates a nitive demands of return to sport.13,121,157 address the compensatory neuroplastic
CNS alteration of afferent processing, to This framework highlights 3 related sequelae after ACL injury and train the
compensate for the lost somatosensory sensorimotor adaptations occurring in the neuromuscular system in a functional
contribution by increasing utilization athlete with an ACL injury: (1) depressed manner. A recent technological innova-
of visual resources for neuromuscular or disrupted somatosensory input and tion has made this possible by decreas-
control, which may be an adaptation of altered sensorimotor processing, which ing visual input without fully removing
the disrupted proprioceptive afferent in- induce (2) increased visual processing to it.21,22 This tool, stroboscopic eyewear
put from the damaged ACL and associ- plan movement and maintain neuromus- (eg, PLATO Visual Occlusion Spectacles
ated noxious stimuli.1,17,18,50,117 It is possible cular control and (3) increased cortical [Translucent Technologies Inc, Toronto,
that after extensive time and/or training, top-down motor control strategies. Canada], Nike SPARQ Vapor Strobes
a measure of motor function may be re- [Nike Inc, Beaverton, OR], PRIMARY
stored, but at the expense of compensa- Modifying Visual Feedback Strobe Glasses [Appreciate Co, Ltd, Kyo-
tions that allow the sensory deficits to The need to transfer neuromuscular to, Japan]) (FIGURE 3), has the ability to
remain.2,53,57 Motor function may normal- control strategies from the stable train- partially obstruct vision by intermittently
ize with basic tasks in the clinic, such as ing environment to the chaotic athletic switching from clear to opaque, allowing
hop or strength tests, but may not trans- field requires that interventions integrate highly complex, dynamic athletic maneu-
fer to the demanding athletic environ- complex sensory inputs (environmen- vers to be performed under degraded vi-
ment, where the proprioceptive sensory tal stimulus, visual and proprioceptive sual input (FIGURE 4).6,21,22,106 Practice with
loss may result in impaired motor func- acuity) in conjunction with the mo- a stroboscopic vision system has already
tion as the task and environmental com- tor outputs (strength, movement qual- been shown to enhance aspects of basic

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[ clinical commentary ]
Exercise

Single-leg hop with air target, unstable


landing and reaction ball
Stand on 1 leg, jump forward, contact air
target in flight with opposite hand of
jump-landing leg; on landing, catch ball.
Shown with Vertec target at 50% of
maximum jump height

Broad jump with reaction ball and


unanticipated cut
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Stand on both feet, jump out, land on both


feet, and track the ball to determine cut
direction. Progress to decrease
anticipation time from landing to ball
release and cut direction
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

Single leg, air target, and reaction ball


Stand on both feet with knees slightly bent,
then jump and rotate 180° while in the air.
The opposite hand of the landing foot
reaches out to contact a target. When
landing, catch the ball. Shown with Vertec
target at 50% of maximum jump height
Journal of Orthopaedic & Sports Physical Therapy®

FIGURE 4. Examples of higher-level, dynamic neuromuscular training exercises incorporating visual target acquisition, environmental interaction, anticipatory ability, unstable
surfaces, and stroboscopic visual interference, using stroboscopic glasses.

visual cognition, such as transient at- transparent status). This adjustability is After injury, the CNS experiences a
tention,7 anticipatory trajectory estima- an important feature because postinjury, compensatory overutilization of visual
tion,138 and short-term memory.6 These visual interference could increase rein- feedback to maintain neuromuscular
abilities may play a role in mitigating or jury risk during rehabilitation, particu- control. The suggested intermittent visu-
avoiding injurious collisions or situations larly if the athlete has not yet adapted to al training can decrease the available vi-
via improved anticipation and processing the depressed visual feedback. The abil- sual feedback to the CNS. This may force
speed,63 which in turn may modify ACL- ity to scale the level of interference up or the CNS to engage in an adaptive strategy
injury risk.141 Training with intermittent down provides a means for the clinician by increased weighting of the remaining
visual input also offers a simple, easy-to- to progress the patient, based on clinical proprioceptive inputs, as opposed to con-
implement, and novel stress to the neu- judgment. Also, a warm-up period is rec- tinuing to compensate with visual feed-
ral control system that is compatible with ommended to allow patients to familiar- back (FIGURE 2). The neural mechanisms
current neuromuscular training exercis- ize themselves with the visual effect by underlying this sensory visual-motor in-
es. The disrupted visual feedback may doing less aggressive movements, such teraction are theoretical at this point, but
more closely simulate the neurocognitive as single-leg balance or upper extremity may include increased utilization or effi-
demands of activity in the safety of a con- exercises (ball toss), before advancing to ciency of the remaining proprioceptive or
trolled clinic or field environment under jump-landing or direction-change tasks. vestibular inputs, and/or improved visu-
the supervision of a qualified profession- The eyewear is also wireless and portable, al-motor processing efficiency to make up
al. Such stroboscopic visual training can making for flexible implementation in a for the increased demand. Alternatively,
also be tailored to fit a desired difficulty wide assortment of clinics or on-field intermittent visual training could lead
level by altering the rate of stroboscop- progressions of already-established neu- to increased attentional focus70 and/or
ic interruption (ratio of opaque versus romuscular training exercises.107 changes in the rate of memory consoli-

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dation6 that, in turn, improve the use of Visual-Motor Training (Nike, Inc), to web-based applications, to
afferent information for guiding motor Stroboscopic training, dual tasking us- simple paper or object manipulation.35,47
control. Regardless of the mechanism, ing environmental interaction or adding Software or full electronic station setups
this training may improve the transition visual obstruction, and facilitating motor are ideal and the literature supports their
to athletic activity by decreasing depen- learning are methods to decrease visual ability to increase performance metrics in
dence on vision to maintain dynamic feedback during established exercises to athletes, but the clinician may not have
motor control, allowing its use for envi- make vision a less salient form of infor- access to this type of technology. Alter-
ronmental interaction on return to the mation for motor programming. These native mechanisms to train the visual
complex athletic environment. strategies may stimulate the CNS to re- system with minimal equipment include
weight information from the somatosen- the use of a tachistoscope (flash cards of
Indirect Visual Distraction sory and vestibular inputs to decrease objects/numbers/letters of increasing
Other techniques to modify visual feed- excessive reliance on visual feedback. An value that must be attended to and re-
back outside of stroboscopic eyewear alternative to reducing visual feedback called) to improve object recognition in
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may be more accessible and still provide dependence is to make the visual pro- the visual field, a Brock string (string of
a means to encourage adaptive neuro- cessing system more efficient and able colored balls at different distances held
plasticity. Progressively increasing the to handle the increased demand. The to the face; the participant must focus on
difficulty of the sensorimotor challenge injury may only allow so much sensory each one in sequence) to improve occulo-
can not only facilitate neuroplasticity adaptation, and a degree of increased vi- motor muscle capacity to focus on targets
for motor control, but also improve sen- sual feedback may have to be regulated rapidly, and saccades (charts of random
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

sory integration and address the visual to maintain neuromuscular integrity letters on a wall; the player must focus on
processing bias. The key considerations during action, regardless of how much each one and call out letters in sequence)
to completing the latter are the focus of we attempt to force proprioceptor or ves- to improve rapid visual processing.
attention, task complexity, visual input, tibular upregulation. In this case, visual
and cognitive load during rehabilita- training in isolation or in combination Motor Learning Applications
tion.29,126 Many mechanisms, such as in- with neuromuscular training methods The increased level of cortical drive dur-
corporating reaction-time components,126 may provide a means to further address ing movement, seen in individuals with
ball tracking, engaging other players,102 the compensatory neuroplasticity fol- an ACL injury, provides a neurological
adding decision-making29 or anticipa- lowing injury. Visual training has been mechanism18,65,79 to explain the greater
Journal of Orthopaedic & Sports Physical Therapy®

tory aspects,126 and having the patient shown to enhance sport performance35,106 amount of cocontraction and muscle-
dual task112 by engaging the upper ex- and improve reaction time and visual guarding strategies seen after injury.146
tremity while performing lower extrem- processing ability.6,7,138 Simply increasing Such a neuromuscular control strategy is
ity exercises or occupying the mind with these fundamental neurocognitive at- consistent with an increase in internal fo-
memory or related tasks, can increase the tributes may allow the athlete to handle cus of control, likely due to the increased
neural demand of neuromuscular train- the dual task of maintaining knee control conscious awareness of the injured joint
ing strategies. Recently, Negahban et while interacting with the environment and its movement as opposed to atten-
al112 used a classic dual-task paradigm by and responding to potentially injurious tion to the external environment.58,155
having individuals post–ACL reconstruc- situations. Rehabilitation guidelines that focus on
tion maintain single-leg postural control Many methods for training the visual explicit feedback (eg, contract quadri-
while performing a cognitive task (hold- system exist, and each one tends to fo- ceps or keep knees over your toes) might
ing a string of numbers in mind). This cus on a different visual construct. These be further promoting the top-down cor-
additional demand degraded postural constructs include occulomotor control, tical and visual feedback control of the
stability in the ACL cohort but had little multiple-object tracking, visual sensitiv- movement, as opposed to facilitating a
effect in control participants. This builds ity, spatial attention, visual memory, reac- return to a more autonomic somatosen-
on previous work that has established tion time, and processing speed. Several sory feedback control and visual feedback
that adding environmental interactions, commercial tools exist that target 1 or on the environment. As discussed earlier,
such as a target, another player, a ball, or more of these visual processing attributes. the increased activation of the presupple-
decision making, has greater influence These tools range in cost and approach, mentary motor area to perform a simple
in those with ACL injury.42,73,151 Conse- from high-level computer-based systems, knee joint movement79 further demon-
quently, strategies to address these per- such as CogniSens (CogniSens Inc, Mon- strates the increased need for cortical
formance deficits should be incorporated treal, Canada), Dynavision (Dynavision motor planning of movement after ACL
in neuromuscular training targeting the International LLC, West Chester, OH), injury. The implications of these findings
transition from clinic to activity. and the SPARQ Sensory Training Station are concerning for return to sport, as the

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[ clinical commentary ]
demands of complex, more dynamic mo- tion and injury prevention programs. Im- this may decrease the ability to compen-
tion may exceed the capability of the re- plementation can be as basic as adding an sate for environmental stimuli and atten-
gion to program optimal movement and eyes-closed or a cognitive dual task dur- uate unanticipated maneuvers, such as
may contribute to injury risk. ing quadriceps contraction sets as the pa- cutting or landing, that depend on quick
The classic mechanism to rectify in- tient progresses toward the autonomous visual processing.31,72,102 Future studies
creased reliance on cortical mechanisms stage in that exercise during the first few should investigate the potential associa-
for lower extremity control is to advance clinic visits, or including environmen- tion of varying visual processing capabili-
patients to the autonomous stage of mo- tal stimuli (other players, unanticipated ties and sensorimotor neural integration
tor learning.95 In early-stage rehabilita- direction changes, target acquisition, or with musculoskeletal risk. Future studies
tion, explicit focus is needed to restore reaction ball) during functional tasks lat- should also investigate visual feedback
muscle function, and internally focused er in rehabilitation, and can advance to modification or visual-motor additions
feedback such as “contract your quad,” highly complex virtual reality simulations to neuromuscular training in relation to
“knees over the toes,” or “bend your knee” that are increasing in quality and accessi- injury prevention.
Downloaded from www.jospt.org at on September 6, 2022. For personal use only. No other uses without permission.

is commonly used. Advancing rehabilita- bility.43,51 Collectively, these vision-based


tive feedback to an external focus, such as interventions are gaining widespread use CONCLUSION
“land on the markers” or “touch the target in a number of clinical (eg, concussion,

T
as you land,” will facilitate transfer of mo- cognitive disorders) and nonclinical (eg, his review highlights a concep-
tor control to subcortical regions and free entertainment, performance enhance- tual framework for integrating a
cortical resources for programming more ment, military) applications, and future variety of visual-motor constructs
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

complex motor actions.58,127,137 Such motor integration with musculoskeletal injury during neuromuscular rehabilitation as
learning principles applied to neuromus- rehabilitation may create an entirely new a future avenue of research to optimize
cular training may assist in transferring avenue for improving neuromuscular musculoskeletal therapy interventions.
knee control strategies to the athletic field function to prevent and treat orthopae- A strength of these recommendations
when conscious attention is being paid dic injuries. is that they act as adjunct strategies to
to the environment and not knee posi- foundational neuromuscular techniques
tion.127,136 The additions to neuromuscu- Visual-Motor Training in for optimizing strength, multiplanar knee
lar training previously discussed can also Primary ACL Injury Prevention and trunk control, and movement asym-
help speed the process of acquiring the The presented evidence suggests that metries.45 These suggestions provide an
Journal of Orthopaedic & Sports Physical Therapy®

ability to transfer motor skills to the field. ACL injury can alter the nervous system opportunity to supplement more tradi-
utilization of somatosensory input, affer- tional interventions by further targeting
Limitations ent integration, and motor output. These neuroplastic, cognitive, and visual-mo-
The framework described above provides neuroplastic effects induce a neuromus- tor capabilities. The clinician can ap-
an opportunity to develop hypothesis- cular control strategy that increases de- proximate the neurocognitive demands
driven clinical and research constructs pendence on visual feedback to regulate of higher-intensity athletic activity in a
for further exploration. Prior to stead- dynamic stability of the system. However, safe, controlled, and—most important-
fast clinical recommendations, rigorous some of the described postinjury adapta- ly—feedback-rich environment under the
longitudinal and controlled trials should tions may actually be present prior to in- supervision of a well-trained professional
be undertaken; however, exploration jury, potentially playing a role in primary before reintegration into sport. Recogni-
of novel neuromuscular re-education ACL risk. Swanik et al141 reported initial tion of the visual-motor implications of
techniques may provide immediate en- findings of decreased visual processing neuromuscular control and injury recov-
hancement to current rehabilitation and capabilities in individuals prior to ACL ery and prevention, combined with new
prevention methods. We have suggested injury. Using neurocognitive testing, they technologies and approaches, may help
some methods to address the postinjury found that a decrease in visual processing to mitigate postinjury movement dys-
neuroplasticity during the rehabilitation speed and reaction time was predictive function and decrease injury risk when
process, and, undoubtedly, clinicians and of subsequent ACL injury.141 A theorized returning to activity. t
researchers will develop more novel and mechanism for visual function influenc-
applicable methods in the near future. ing injury risk is in the ability to prepare ACKNOWLEDGEMENTS: The primary author
There is insufficient evidence to recom- the neuromuscular system in anticipa- would like to thank Dr Ajit Chaudhari, Dr
mend one method or system over any tion of high-risk situations, maneuvers, Deborah Larsen, Dr Stephen Page, and Dr
other at this time, but we encourage cli- or incoming players.63,105 If visual pro- Alexandra Borstad for their mentorship, train-
nicians to consider visual-motor function cessing resources are taxed to maintain ing, and scholarly discussions related to this
on any level as a part of ACL rehabilita- the afferent input for knee motor control, manuscript.

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2010;207:466-475. http://dx.doi.org/10.1016/j. binocular and monocular viewing. Motor Con-
REFERENCES bbr.2009.10.034 trol. 2003;7:46-56.
12. Ball T, Schreiber A, Feige B, Wagner M, Lucking 23. Berthoz A, Lacour M, Soechting JF, Vidal
1. A  dachi N, Ochi M, Uchio Y, Iwasa J, Ryoke K, CH, Kristeva-Feige R. The role of higher-order PP. The role of vision in the control of pos-
Kuriwaka M. Mechanoreceptors in the anterior motor areas in voluntary movement as revealed ture during linear motion. Prog Brain Res.
cruciate ligament contribute to the joint position by high-resolution EEG and fMRI. Neuroimage. 1979;50:197-209. http://dx.doi.org/10.1016/
sense. Acta Orthop Scand. 2002;73:330-334. 1999;10:682-694. http://dx.doi.org/10.1006/ S0079-6123(08)60820-1
http://dx.doi.org/10.1080/000164702320155356 nimg.1999.0507 24. Biedert RM, Zwick EB. Ligament-muscle reflex
2. Ageberg E, Fridén T. Normalized motor function 13. Baltaci G, Harput G, Haksever B, Ulusoy B, arc after anterior cruciate ligament reconstruc-
but impaired sensory function after unilateral Ozer H. Comparison between Nintendo Wii Fit tion: electromyographic evaluation. Arch Orthop
non-reconstructed ACL injury: patients com- and conventional rehabilitation on functional Trauma Surg. 1998;118:81-84.
pared with uninjured controls. Knee Surg Sports performance outcomes after hamstring anterior 25. Binder JR, Desai RH. The neurobiology of se-
Traumatol Arthrosc. 2008;16:449-456. http:// cruciate ligament reconstruction: prospective, mantic memory. Trends Cogn Sci. 2011;15:527-
dx.doi.org/10.1007/s00167-008-0499-9 randomized, controlled, double-blind clinical 536. http://dx.doi.org/10.1016/j.tics.2011.10.001
3. Ageberg E, Roberts D, Holmström E, Fridén trial. Knee Surg Sports Traumatol Arthrosc. 26. Boden BP, Torg JS, Knowles SB, Hewett TE. Vid-
T. Balance in single-limb stance in patients 2013;21:880-887. http://dx.doi.org/10.1007/ eo analysis of anterior cruciate ligament injury:
Downloaded from www.jospt.org at on September 6, 2022. For personal use only. No other uses without permission.

with anterior cruciate ligament injury: rela- s00167-012-2034-2 abnormalities in hip and ankle kinematics. Am
tion to knee laxity, proprioception, muscle 14. Barenius B, Ponzer S, Shalabi A, Bujak R, Norlén J Sports Med. 2009;37:252-259. http://dx.doi.
strength, and subjective function. Am J Sports L, Eriksson K. Increased risk of osteoarthritis org/10.1177/0363546508328107
Med. 2005;33:1527-1535. http://dx.doi. after ACL reconstruction – a 14-year follow- 27. Bonfim TR, Jansen Paccola CA, Barela JA.
org/10.1177/0363546505274934 up study of a randomized controlled trial. Proprioceptive and behavior impairments in
4. Ajuied A, Wong F, Smith C, et al. Anterior Arthroscopy. 2013;29:e80-e81. http://dx.doi. individuals with anterior cruciate ligament
cruciate ligament injury and radiologic pro- org/10.1016/j.arthro.2013.07.080 reconstructed knees. Arch Phys Med Rehabil.
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

gression of knee osteoarthritis: a system- 15. Bates NA, Ford KR, Myer GD, Hewett TE. Impact 2003;84:1217-1223.
atic review and meta-analysis. Am J Sports differences in ground reaction force and center 28. Bonner MF, Price AR. Where is the anterior
Med. 2014;42:2242-2252. http://dx.doi. of mass between the first and second landing temporal lobe and what does it do? J Neurosci.
org/10.1177/0363546513508376 phases of a drop vertical jump and their impli- 2013;33:4213-4215. http://dx.doi.org/10.1523/
5. Amador N, Fried I. Single-neuron activity in cations for injury risk assessment. J Biomech. JNEUROSCI.0041-13.2013
the human supplementary motor area un- 2013;46:1237-1241. http://dx.doi.org/10.1016/j. 29. Borotikar BS, Newcomer R, Koppes R, McLean
derlying preparation for action. J Neurosurg. jbiomech.2013.02.024 SG. Combined effects of fatigue and decision
2004;100:250-259. http://dx.doi.org/10.3171/ 16. Baumeister J, Reinecke K, Liesen H, Weiss making on female lower limb landing pos-
jns.2004.100.2.0250 M. Cortical activity of skilled performance in tures: central and peripheral contributions to
6. Appelbaum LG, Cain MS, Schroeder JE, a complex sports related motor task. Eur J ACL injury risk. Clin Biomech (Bristol, Avon).
Darling EF, Mitroff SR. Stroboscopic visual Appl Physiol. 2008;104:625-631. http://dx.doi. 2008;23:81-92. http://dx.doi.org/10.1016/j.
org/10.1007/s00421-008-0811-x clinbiomech.2007.08.008
Journal of Orthopaedic & Sports Physical Therapy®

training improves information encoding in


short-term memory. Atten Percept Psychophys. 17. Baumeister J, Reinecke K, Schubert M, Weiss 30. Boudreau SA, Farina D, Falla D. The role of motor
2012;74:1681-1691. http://dx.doi.org/10.3758/ M. Altered electrocortical brain activity after learning and neuroplasticity in designing reha-
s13414-012-0344-6 ACL reconstruction during force control. J bilitation approaches for musculoskeletal pain
7. Appelbaum LG, Schroeder JE, Cain MS, Mitroff Orthop Res. 2011;29:1383-1389. http://dx.doi. disorders. Man Ther. 2010;15:410-414. http://
SR. Improved visual cognition through stro- org/10.1002/jor.21380 dx.doi.org/10.1016/j.math.2010.05.008
boscopic training. Front Psychol. 2011;2:276. 18. Baumeister J, Reinecke K, Weiss M. Changed 31. Brown TN, Palmieri-Smith RM, McLean SG. Sex
http://dx.doi.org/10.3389/fpsyg.2011.00276 cortical activity after anterior cruciate and limb differences in hip and knee kinematics
8. Ardern CL, Taylor NF, Feller JA, Webster KE. ligament reconstruction in a joint position and kinetics during anticipated and unantici-
Return-to-sport outcomes at 2 to 7 years after paradigm: an EEG study. Scand J Med Sci pated jump landings: implications for anterior
anterior cruciate ligament reconstruction sur- Sports. 2008;18:473-484. http://dx.doi. cruciate ligament injury. Br J Sports Med.
gery. Am J Sports Med. 2012;40:41-48. http:// org/10.1111/j.1600-0838.2007.00702.x 2009;43:1049-1056. http://dx.doi.org/10.1136/
dx.doi.org/10.1177/0363546511422999 19. Beck S, Taube W, Gruber M, Amtage F, Gollhofer bjsm.2008.055954
9. Ardern CL, Taylor NF, Feller JA, Whitehead TS, A, Schubert M. Task-specific changes in mo- 32. Brumagne S, Cordo P, Verschueren S. Proprio-
Webster KE. Psychological responses matter in tor evoked potentials of lower limb muscles ceptive weighting changes in persons with low
returning to preinjury level of sport after anterior after different training interventions. Brain Res. back pain and elderly persons during upright
cruciate ligament reconstruction surgery. Am J 2007;1179:51-60. http://dx.doi.org/10.1016/j. standing. Neurosci Lett. 2004;366:63-66. http://
Sports Med. 2013;41:1549-1558. http://dx.doi. brainres.2007.08.048 dx.doi.org/10.1016/j.neulet.2004.05.013
org/10.1177/0363546513489284 20. Benjaminse A, Otten E. ACL injury prevention, 33. Chen TL, Babiloni C, Ferretti A, et al. Hu-
10. Ardern CL, Webster KE, Taylor NF, Feller JA. more effective with a different way of motor man secondary somatosensory cortex is
Return to the preinjury level of competitive learning? Knee Surg Sports Traumatol Arthrosc. involved in the processing of somatosen-
sport after anterior cruciate ligament recon- 2011;19:622-627. http://dx.doi.org/10.1007/ sory rare stimuli: an fMRI study. Neuroimage.
struction surgery: two-thirds of patients have s00167-010-1313-z 2008;40:1765-1771. http://dx.doi.org/10.1016/j.
not returned by 12 months after surgery. Am 21. Bennett S, Ashford D, Rioja N, Elliott D. Inter- neuroimage.2008.01.020
J Sports Med. 2011;39:538-543. http://dx.doi. mittent vision and one-handed catching: the 34. Chu Y, Sell TC, Abt JP, et al. Air assault soldiers
org/10.1177/0363546510384798 effect of general and specific task experience. demonstrate more dangerous landing biome-
11. Babiloni C, Marzano N, Infarinato F, et al. “Neural J Mot Behav. 2004;36:442-449. http://dx.doi. chanics when visual input is removed. Mil Med.
efficiency” of experts’ brain during judgment org/10.3200/JMBR.36.4.442-449 2012;177:41-47.
of actions: a high-resolution EEG study in elite 22. Bennett SJ, Elliott D, Weeks DJ, Keil D. The ef- 35. Clark JF, Ellis JK, Bench J, Khoury J, Graman P.
and amateur karate athletes. Behav Brain Res. fects of intermittent vision on prehension under High-performance vision training improves bat-

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45-05 Grooms.indd 389 4/15/2015 6:49:33 PM


[ clinical commentary ]
ting statistics for University of Cincinnati base- DW. Lower extremity compensations following contextual interference in motor skill learning. J
ball players. PLoS One. 2012;7:e29109. http:// anterior cruciate ligament reconstruction. Phys Mot Behav. 1995;27:299-309. http://dx.doi.org/1
dx.doi.org/10.1371/journal.pone.0029109 Ther. 2000;80:251-260. 0.1080/00222895.1995.9941719
36. Cortes N, Blount E, Ringleb S, Onate JA. 49. Ferretti A, Babiloni C, Gratta CD, et al. Functional 62. Hamzei F, Liepert J, Dettmers C, Weiller C,
Soccer-specific video simulation for improv- topography of the secondary somatosensory Rijntjes M. Two different reorganization pat-
ing movement assessment. Sports Biomech. cortex for nonpainful and painful stimuli: an terns after rehabilitative therapy: an explor-
2011;10:22-34. http://dx.doi.org/10.1080/147631 fMRI study. Neuroimage. 2003;20:1625-1638. atory study with fMRI and TMS. Neuroimage.
41.2010.547591 50. Flor H, Braun C, Elbert T, Birbaumer N. Extensive 2006;31:710-720. http://dx.doi.org/10.1016/j.
37. Courtney C, Rine RM, Kroll P. Central somato- reorganization of primary somatosensory cortex neuroimage.2005.12.035
sensory changes and altered muscle synergies in chronic back pain patients. Neurosci Lett. 63. Harpham JA, Mihalik JP, Littleton AC, Frank
in subjects with anterior cruciate ligament 1997;224:5-8. BS, Guskiewicz KM. The effect of visual and
deficiency. Gait Posture. 2005;22:69-74. http:// 51. Fluet GG, Deutsch JE. Virtual reality for sensory performance on head impact biome-
dx.doi.org/10.1016/j.gaitpost.2004.07.002 sensorimotor rehabilitation post-stroke: the chanics in college football players. Ann Biomed
38. Courtney CA, Durr RK, Emerson-Kavchak AJ, promise and current state of the field. Curr Phys Eng. 2014;42:1-10. http://dx.doi.org/10.1007/
Witte EO, Santos MJ. Heightened flexor with- Med Rehabil Rep. 2013;1:9-20. http://dx.doi. s10439-013-0881-8
drawal responses following ACL rupture are org/10.1007/s40141-013-0005-2 64. Herman DC, Weinhold PS, Guskiewicz KM, Gar-
Downloaded from www.jospt.org at on September 6, 2022. For personal use only. No other uses without permission.

enhanced by passive tibial translation. Clin 52. Ford KR, Myer GD, Smith RL, Byrnes RN, Dopirak rett WE, Yu B, Padua DA. The effects of strength
Neurophysiol. 2011;122:1005-1010. http://dx.doi. SE, Hewett TE. Use of an overhead goal alters training on the lower extremity biomechanics
org/10.1016/j.clinph.2010.07.029 vertical jump performance and biomechanics. of female recreational athletes during a stop-
39. Courtney CA, Rine RM. Central somato- J Strength Cond Res. 2005;19:394-399. http:// jump task. Am J Sports Med. 2008;36:733-740.
sensory changes associated with improved dx.doi.org/10.1519/15834.1 http://dx.doi.org/10.1177/0363546507311602
dynamic balance in subjects with anterior 53. Fremerey RW, Lobenhoffer P, Zeichen J, Skutek 65. Heroux ME, Tremblay F. Corticomotor excit-
cruciate ligament deficiency. Gait Posture. M, Bosch U, Tscherne H. Proprioception after ability associated with unilateral knee dysfunc-
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

2006;24:190-195. http://dx.doi.org/10.1016/j. rehabilitation and reconstruction in knees with tion secondary to anterior cruciate ligament
gaitpost.2005.08.006 deficiency of the anterior cruciate ligament: a injury. Knee Surg Sports Traumatol Arthrosc.
40. Dault MC, Frank JS, Allard F. Influence of a prospective, longitudinal study. J Bone Joint 2006;14:823-833. http://dx.doi.org/10.1007/
visuo-spatial, verbal and central executive Surg Br. 2000;82:801-806. s00167-006-0063-4
working memory task on postural control. Gait 54. Fridén T, Roberts D, Ageberg E, Waldén M, Zät- 66. Heroux ME, Tremblay F. Weight discrimina-
Posture. 2001;14:110-116. terström R. Review of knee proprioception and tion after anterior cruciate ligament in-
41. Del Percio C, Babiloni C, Marzano N, et al. the relation to extremity function after an ante- jury: a pilot study. Arch Phys Med Rehabil.
“Neural efficiency” of athletes’ brain for upright rior cruciate ligament rupture. J Orthop Sports 2005;86:1362-1368.
standing: a high-resolution EEG study. Brain Phys Ther. 2001;31:567-576. http://dx.doi. 67. Hewett TE, Myer GD, Ford KR, et al. Bio-
Res Bull. 2009;79:193-200. http://dx.doi. org/10.2519/jospt.2001.31.10.567 mechanical measures of neuromuscular
org/10.1016/j.brainresbull.2009.02.001 55. Fridén T, Roberts D, Movin T, Wredmark T. Func- control and valgus loading of the knee pre-
42. Demont RG, Lephart SM, Giraldo JL, Swanik
Journal of Orthopaedic & Sports Physical Therapy®

tion after anterior cruciate ligament injuries. dict anterior cruciate ligament injury risk in
CB, Fu FH. Muscle preactivity of anterior cruci- Influence of visual control and proprioception. female athletes: a prospective study. Am J
ate ligament-deficient and -reconstructed Acta Orthop Scand. 1998;69:590-594. Sports Med. 2005;33:492-501. http://dx.doi.
females during functional activities. J Athl Train. 56. Goerger BM, Marshall SW, Beutler AI, Blackburn org/10.1177/0363546504269591
1999;34:115-120. JT, Wilckens JH, Padua DA. ACL injury alters 68. Hewett TE, Torg JS, Boden BP. Video analysis of
43. Deutsch JE. Virtual reality and gaming systems pre-injury coordination of the hip and knee: the trunk and knee motion during non-contact ante-
to improve walking and mobility for people with JUMP-ACL study [abstract]. Med Sci Sports rior cruciate ligament injury in female athletes:
musculoskeletal and neuromuscular conditions. Exerc. 2013;45:221. lateral trunk and knee abduction motion are
Stud Health Technol Inform. 2009;145:84-93. 57. Gokeler A, Benjaminse A, Hewett TE, et al. combined components of the injury mechanism.
44. Di Fabio RP, Graf B, Badke MB, Breunig A, Proprioceptive deficits after ACL injury: are Br J Sports Med. 2009;43:417-422. http://
Jensen K. Effect of knee joint laxity on long- they clinically relevant? Br J Sports Med. dx.doi.org/10.1136/bjsm.2009.059162
loop postural reflexes: evidence for a human 2012;46:180-192. http://dx.doi.org/10.1136/ 69. Hoffman M, Schrader J, Koceja D. An investiga-
capsular-hamstring reflex. Exp Brain Res. bjsm.2010.082578 tion of postural control in postoperative anterior
1992;90:189-200. 58. Gokeler A, Benjaminse A, Hewett TE, et al. cruciate ligament reconstruction patients. J Athl
45. Di Stasi S, Myer GD, Hewett TE. Neuromuscular Feedback techniques to target functional Train. 1999;34:130-136.
training to target deficits associated with sec- deficits following anterior cruciate ligament 70. Holliday J. Effect of Stroboscopic Vision Training
ond anterior cruciate ligament injury. J Orthop reconstruction: implications for motor control on Dynamic Visual Acuity Scores: Nike Vapor
Sports Phys Ther. 2013;43:777-792. http:// and reduction of second injury risk. Sports Med. Strobe® Eyewear. Logan, UT: Utah State Univer-
dx.doi.org/10.2519/jospt.2013.4693 2013;43:1065-1074. http://dx.doi.org/10.1007/ sity; 2013.
46. Emanuel M, Jarus T, Bart O. Effect of focus of s40279-013-0095-0 71. Hootman JM, Dick R, Agel J. Epidemiology of
attention and age on motor acquisition, reten- 59. Gómez-Barrena E, Martinez-Moreno E, Munuera collegiate injuries for 15 sports: summary and
tion, and transfer: a randomized trial. Phys Ther. L. Segmental sensory innervation of the anterior recommendations for injury prevention initia-
2008;88:251-260. http://dx.doi.org/10.2522/ cruciate ligament and the patellar tendon of the tives. J Athl Train. 2007;42:311-319.
ptj.20060174 cat’s knee. Acta Orthop Scand. 1996;67:545-552. 72. Houck JR, De Haven KE, Maloney M. Influence of
47. Erickson GB, Citek K, Cove M, et al. Reliabil- 60. Grindstaff TL, Hammill RR, Tuzson AE, Hertel J. anticipation on movement patterns in subjects
ity of a computer-based system for measur- Neuromuscular control training programs and with ACL deficiency classified as noncopers. J
ing visual performance skills. Optometry. noncontact anterior cruciate ligament injury Orthop Sports Phys Ther. 2007;37:56-64. http://
2011;82:528-542. http://dx.doi.org/10.1016/j. rates in female athletes: a numbers-needed-to- dx.doi.org/10.2519/jospt.2007.2292
optm.2011.01.012 treat analysis. J Athl Train. 2006;41:450-456. 73. Houck JR, Wilding GE, Gupta R, De Haven KE,
48. Ernst GP, Saliba E, Diduch DR, Hurwitz SR, Ball 61. Hall KG, Magill RA. Variability of practice and Maloney M. Analysis of EMG patterns of control

390 | may 2015 | volume 45 | number 5 | journal of orthopaedic & sports physical therapy

45-05 Grooms.indd 390 4/15/2015 6:49:33 PM


subjects and subjects with ACL deficiency 86. K onishi Y, Konishi H, Fukubayashi T. Gamma loop org/10.4085/1062-6050-43.5.538
during an unanticipated walking cut task. dysfunction in quadriceps on the contralateral 100. M  cLean SG, Borotikar B, Lucey SM. Lower
Gait Posture. 2007;25:628-638. http://dx.doi. side in patients with ruptured ACL. Med Sci limb muscle pre-motor time measures dur-
org/10.1016/j.gaitpost.2006.07.001 Sports Exerc. 2003;35:897-900. http://dx.doi. ing a choice reaction task associate with
74. Hui C, Salmon LJ, Kok A, Maeno S, Linklater org/10.1249/01.MSS.0000069754.07541.D2 knee abduction loads during dynamic single
J, Pinczewski LA. Fifteen-year outcome of 87. Konishi YU. ACL repair might induce fur- leg landings. Clin Biomech (Bristol, Avon).
endoscopic anterior cruciate ligament recon- ther abnormality of gamma loop in the 2010;25:563-569. http://dx.doi.org/10.1016/j.
struction with patellar tendon autograft for intact side of the quadriceps femoris. Int J clinbiomech.2010.02.013
“isolated” anterior cruciate ligament tear. Am Sports Med. 2011;32:292-296. http://dx.doi. 101. McLean SG, Huang X, van den Bogert AJ.
J Sports Med. 2011;39:89-98. http://dx.doi. org/10.1055/s-0030-1270488 Association between lower extremity pos-
org/10.1177/0363546510379975 88. Krosshaug T, Nakamae A, Boden BP, et al. ture at contact and peak knee valgus mo-
75. Im HJ, Kim JS, Li X, et al. Alteration of sensory Mechanisms of anterior cruciate ligament injury ment during sidestepping: implications for
neurons and spinal response to an experimental in basketball: video analysis of 39 cases. Am ACL injury. Clin Biomech (Bristol, Avon).
osteoarthritis pain model. Arthritis Rheum. J Sports Med. 2007;35:359-367. http://dx.doi. 2005;20:863-870. http://dx.doi.org/10.1016/j.
2010;62:2995-3005. http://dx.doi.org/10.1002/ org/10.1177/0363546506293899 clinbiomech.2005.05.007
art.27608 89. Lajoie Y, Teasdale N, Bard C, Fleury M. Attention- 102. McLean SG, Lipfert SW, van den Bogert AJ.
Downloaded from www.jospt.org at on September 6, 2022. For personal use only. No other uses without permission.

76. Jarus T, Gutman T. Effects of cognitive processes al demands for static and dynamic equilibrium. Effect of gender and defensive opponent on
and task complexity on acquisition, retention, Exp Brain Res. 1993;97:139-144. the biomechanics of sidestep cutting. Med Sci
and transfer of motor skills. Can J Occup Ther. 90. Lepley AS, Bahhur NO, Murray AM, Pietro- Sports Exerc. 2004;36:1008-1016.
2001;68:280-289. simone BG. Quadriceps corticomotor excit- 103. McLean SG, Neal RJ, Myers PT, Walters MR.
77. Jensen JL, Marstrand PC, Nielsen JB. Motor ability following an experimental knee joint Knee joint kinematics during the sidestep cut-
skill training and strength training are as- effusion. Knee Surg Sports Traumatol Arthrosc. ting maneuver: potential for injury in women.
sociated with different plastic changes in the 2015;23:1010-1017. http://dx.doi.org/10.1007/ Med Sci Sports Exerc. 1999;31:959-968.
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

central nervous system. J Appl Physiol (1985). s00167-013-2816-1 104. Meister I, Krings T, Foltys H, et al. Effects of
2005;99:1558-1568. http://dx.doi.org/10.1152/ 91. Levine JD, Dardick SJ, Basbaum AI, Scipio E. long-term practice and task complexity in musi-
japplphysiol.01408.2004 Reflex neurogenic inflammation. I. Contribution cians and nonmusicians performing simple
78. Kapreli E, Athanasopoulos S. The anterior cruci- of the peripheral nervous system to spatially re- and complex motor tasks: implications for
ate ligament deficiency as a model of brain mote inflammatory responses that follow injury. cortical motor organization. Hum Brain Mapp.
plasticity. Med Hypotheses. 2006;67:645-650. J Neurosci. 1985;5:1380-1386. 2005;25:345-352. http://dx.doi.org/10.1002/
http://dx.doi.org/10.1016/j.mehy.2006.01.063 92. Littmann AE, Iguchi M, Madhavan S, Kolarik JL, hbm.20112
79. Kapreli E, Athanasopoulos S, Gliatis J, et al. Shields RK. Dynamic-position-sense impair- 105. Mihalik JP, Blackburn JT, Greenwald RM, Cantu
Anterior cruciate ligament deficiency causes ment’s independence of perceived knee function RC, Marshall SW, Guskiewicz KM. Collision
brain plasticity: a functional MRI study. Am J in women with ACL reconstruction. J Sport type and player anticipation affect head impact
Sports Med. 2009;37:2419-2426. http://dx.doi. Rehabil. 2012;21:44-53. severity among youth ice hockey players. Pe-
org/10.1177/0363546509343201 93. Lohmander LS, Englund PM, Dahl LL, Roos EM. diatrics. 2010;125:e1394-e1401. http://dx.doi.
Journal of Orthopaedic & Sports Physical Therapy®

80. Kennedy JC, Alexander IJ, Hayes KC. Nerve The long-term consequence of anterior cruciate org/10.1542/peds.2009-2849
supply of the human knee and its functional ligament and meniscus injuries: osteoarthritis. 106. Mitroff SR, Friesen P, Bennett D, Yoo H, Reichow
importance. Am J Sports Med. 1982;10:329-335. Am J Sports Med. 2007;35:1756-1769. http:// AW. Enhancing ice hockey skills through strobo-
81. Knecht S, Henningsen H, Elbert T, et al. Cortical dx.doi.org/10.1177/0363546507307396 scopic visual training: a pilot study. Athl Train
reorganization in human amputees and mislo- 94. Madhavan S, Shields RK. Neuromuscular Sports Health Care. 2013;5:261-264. http://
calization of painful stimuli to the phantom limb. responses in individuals with anterior cru- dx.doi.org/10.3928/19425864-20131030-02
Neurosci Lett. 1995;201:262-264. ciate ligament repair. Clin Neurophysiol. 107. Myer GD, Ford KR, Brent JL, Hewett TE. An
82. Koga H, Nakamae A, Shima Y, et al. Mechanisms 2011;122:997-1004. http://dx.doi.org/10.1016/j. integrated approach to change the outcome part
for noncontact anterior cruciate ligament inju- clinph.2010.09.002 II: targeted neuromuscular training techniques
ries: knee joint kinematics in 10 injury situations 95. Magill R. Motor Learning and Control: Concepts to reduce identified ACL injury risk factors. J
from female team handball and basketball. Am and Applications. 8th ed. Boston, MA: WCB/ Strength Cond Res. 2012;26:2272-2292. http://
J Sports Med. 2010;38:2218-2225. http://dx.doi. McGraw-Hill; 2007. dx.doi.org/10.1519/JSC.0b013e31825c2c7d
org/10.1177/0363546510373570 96. Mather RC, 3rd, Koenig L, Kocher MS, et al. 108. Myer GD, Martin L, Jr., Ford KR, et al. No
83. Konishi Y, Aihara Y, Sakai M, Ogawa G, Fu- Societal and economic impact of anterior association of time from surgery with
kubayashi T. Gamma loop dysfunction in cruciate ligament tears. J Bone Joint Surg Am. functional deficits in athletes after anterior
the quadriceps femoris of patients who 2013;95:1751-1759. http://dx.doi.org/10.2106/ cruciate ligament reconstruction: evidence
underwent anterior cruciate ligament recon- JBJS.L.01705 for objective return-to-sport criteria. Am J
struction remains bilaterally. Scand J Med 97. Mattacola CG, Perrin DH, Gansneder BM, Sports Med. 2012;40:2256-2263. http://dx.doi.
Sci Sports. 2007;17:393-399. http://dx.doi. Gieck JH, Saliba EN, McCue FC, 3rd. Strength, org/10.1177/0363546512454656
org/10.1111/j.1600-0838.2006.00573.x functional outcome, and postural stability after 109. Myer GD, Paterno MV, Ford KR, Hewett TE. Neu-
84. Konishi Y, Fukubayashi T, Takeshita D. Mecha- anterior cruciate ligament reconstruction. J Athl romuscular training techniques to target deficits
nism of quadriceps femoris muscle weakness Train. 2002;37:262-268. before return to sport after anterior cruciate
in patients with anterior cruciate ligament 98. McCormick BT. Task complexity and jump land- ligament reconstruction. J Strength Cond Res.
reconstruction. Scand J Med Sci Sports. ings in injury prevention for basketball players. 2008;22:987-1014. http://dx.doi.org/10.1519/
2002;12:371-375. Strength Cond J. 2012;34:89-92. http://dx.doi. JSC.0b013e31816a86cd
85. Konishi Y, Fukubayashi T, Takeshita D. Possible org/10.1519/SSC.0b013e31823ee08e 110. Myer GD, Schmitt LC, Brent JL, et al. Utilization
mechanism of quadriceps femoris weakness 99. McLean SG. The ACL injury enigma: we of modified NFL combine testing to identify
in patients with ruptured anterior cruciate liga- can’t prevent what we don’t understand. J functional deficits in athletes following ACL
ment. Med Sci Sports Exerc. 2002;34:1414-1418. Athl Train. 2008;43:538-540. http://dx.doi. reconstruction. J Orthop Sports Phys Ther.

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45-05 Grooms.indd 391 4/15/2015 6:49:34 PM


[ clinical commentary ]
2011;41:377-387. http://dx.doi.org/10.2519/ 122. P  euskens H, Vanrie J, Verfaillie K, Orban GA. movements. J Neurophysiol. 2005;93:3200-
jospt.2011.3547 Specificity of regions processing biological mo- 3213. http://dx.doi.org/10.1152/jn.00947.2004
111. Nachev P, Wydell H, O’Neill K, Husain M, Ken- tion. Eur J Neurosci. 2005;21:2864-2875. http:// 135. Schutte MJ, Dabezies EJ, Zimny ML, Happel
nard C. The role of the pre-supplementary dx.doi.org/10.1111/j.1460-9568.2005.04106.x LT. Neural anatomy of the human anterior
motor area in the control of action. Neuroim- 123. Pietrosimone BG, Lepley AS, Ericksen HM, Grib- cruciate ligament. J Bone Joint Surg Am.
age. 2007;36 suppl 2:T155-T163. http://dx.doi. ble PA, Levine J. Quadriceps strength and cor- 1987;69:243-247.
org/10.1016/j.neuroimage.2007.03.034 ticospinal excitability as predictors of disability 136. Seidler RD. Neural correlates of motor learn-
112. Negahban H, Ahmadi P, Salehi R, Mehravar M, after anterior cruciate ligament reconstruction. ing, transfer of learning, and learning to learn.
Goharpey S. Attentional demands of postural J Sport Rehabil. 2013;22:1-6. Exerc Sport Sci Rev. 2010;38:3-9. http://dx.doi.
control during single leg stance in patients 124. Pietrosimone BG, McLeod MM, Lepley AS. A org/10.1097/JES.0b013e3181c5cce7
with anterior cruciate ligament reconstruction. theoretical framework for understanding neuro- 137. Seidler RD, Noll DC. Neuroanatomical correlates
Neurosci Lett. 2013;556:118-123. http://dx.doi. muscular response to lower extremity joint in- of motor acquisition and motor transfer. J Neu-
org/10.1016/j.neulet.2013.10.022 jury. Sports Health. 2012;4:31-35. http://dx.doi. rophysiol. 2008;99:1836-1845. http://dx.doi.
113. Norte GE, Pietrosimone BG, Hart JM, Hertel J, org/10.1177/1941738111428251 org/10.1152/jn.01187.2007
Ingersoll CD. Relationship between transcranial 125. Pitman MI, Nainzadeh N, Menche D, Gasalberti 138. Smith TQ, Mitroff SR. Stroboscopic training
magnetic stimulation and percutaneous electri- R, Song EK. The intraoperative evaluation of enhances anticipatory timing. Int J Exerc Sci.
Downloaded from www.jospt.org at on September 6, 2022. For personal use only. No other uses without permission.

cal stimulation in determining the quadriceps the neurosensory function of the anterior cruci- 2012;5:344-353.
central activation ratio. Am J Phys Med Rehabil. ate ligament in humans using somatosensory 139. Smith WM, Bowen KF. The effects of delayed and
2010;89:986-996. http://dx.doi.org/10.1097/ evoked potentials. Arthroscopy. 1992;8:442-447. displaced visual feedback on motor control. J
PHM.0b013e3181f1c00e 126. Pollard CD, Heiderscheit BC, van Emmerik Mot Behav. 1980;12:91-101.
114. O’Connell M, George K, Stock D. Postural sway RE, Hamill J. Gender differences in lower ex- 140. Spindler KP, Wright RW. Clinical practice.
and balance testing: a comparison of normal tremity coupling variability during an unan- Anterior cruciate ligament tear. N Engl J
and anterior cruciate ligament deficient knees. ticipated cutting maneuver. J Appl Biomech. Med. 2008;359:2135-2142. http://dx.doi.
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.

Gait Posture. 1998;8:136-142. 2005;21:143-152. org/10.1056/NEJMcp0804745


115. Okuda K, Abe N, Katayama Y, Senda M, Kuroda 127. Powers CM, Fisher B. Mechanisms underlying 141. Swanik CB, Covassin T, Stearne DJ, Schatz P.
T, Inoue H. Effect of vision on postural sway ACL injury-prevention training: the brain-behav- The relationship between neurocognitive func-
in anterior cruciate ligament injured knees. J ior relationship. J Athl Train. 2010;45:513-515. tion and noncontact anterior cruciate ligament
Orthop Sci. 2005;10:277-283. http://dx.doi. http://dx.doi.org/10.4085/1062-6050-45.5.513 injuries. Am J Sports Med. 2007;35:943-948.
org/10.1007/s00776-005-0893-9 128. Remaud A, Boyas S, Lajoie Y, Bilodeau M. At- http://dx.doi.org/10.1177/0363546507299532
116. On AY, Uludağ B, Taskiran E, Ertekin C. Dif- tentional focus influences postural control and 142. Swanik CB, Lephart SM, Giraldo JL, Demont RG,
ferential corticomotor control of a muscle reaction time performances only during chal- Fu FH. Reactive muscle firing of anterior cruci-
adjacent to a painful joint. Neurorehabil lenging dual-task conditions in healthy young ate ligament-injured females during functional
Neural Repair. 2004;18:127-133. http://dx.doi. adults. Exp Brain Res. 2013;231:219-229. http:// activities. J Athl Train. 1999;34:121-129.
org/10.1177/0888439004269030 dx.doi.org/10.1007/s00221-013-3684-0 143. Thompson HW, McKinley PA. Landing from
117. Palmieri-Smith RM, Villwock M, Downie 129. Roberts D, Ageberg E, Andersson G, Fridén
Journal of Orthopaedic & Sports Physical Therapy®

a jump: the role of vision when landing from


B, Hecht G, Zernicke R. Pain and effusion T. Clinical measurements of proprioception, known and unknown heights. Neuroreport.
and quadriceps activation and strength. J muscle strength and laxity in relation to func- 1995;6:581-584.
Athl Train. 2013;48:186-191. http://dx.doi. tion in the ACL-injured knee. Knee Surg Sports 144. Tinazzi M, Rosso T, Zanette G, Fiaschi A, Aglioti
org/10.4085/1062-6050-48.2.10 Traumatol Arthrosc. 2007;15:9-16. http://dx.doi. SM. Rapid modulation of cortical propriocep-
118. Park HB, Koh M, Cho SH, Hutchinson B, Lee org/10.1007/s00167-006-0128-4 tive activity induced by transient cutaneous
B. Mapping the rat somatosensory pathway 130. Roberts D, Fridén T, Stomberg A, Lindstrand deafferentation: neurophysiological evidence of
from the anterior cruciate ligament nerve A, Moritz U. Bilateral proprioceptive defects short-term plasticity across different somato-
endings to the cerebrum. J Orthop Res. in patients with a unilateral anterior cruciate sensory modalities in humans. Eur J Neurosci.
2005;23:1419-1424. http://dx.doi.org/10.1016/j. ligament reconstruction: a comparison between 2003;18:3053-3060.
orthres.2005.03.017.1100230626 patients and healthy individuals. J Orthop Res. 145. Torquati K, Pizzella V, Babiloni C, et al. Nocicep-
119. Paterno MV, Ford KR, Myer GD, Heyl R, 2000;18:565-571. http://dx.doi.org/10.1002/ tive and non-nociceptive sub-regions in the
Hewett TE. Limb asymmetries in landing and jor.1100180408 human secondary somatosensory cortex: an
jumping 2 years following anterior cruciate 131. Roewer BD, Di Stasi SL, Snyder-Mackler L. MEG study using fMRI constraints. Neuroimage.
ligament reconstruction. Clin J Sport Med. Quadriceps strength and weight acceptance 2005;26:48-56. http://dx.doi.org/10.1016/j.
2007;17:258-262. http://dx.doi.org/10.1097/ strategies continue to improve two years after neuroimage.2005.01.012
JSM.0b013e31804c77ea anterior cruciate ligament reconstruction. J 146. Vairo GL, Myers JB, Sell TC, Fu FH, Harner CD,
120. Paterno MV, Rauh MJ, Schmitt LC, Ford KR, Biomech. 2011;44:1948-1953. http://dx.doi. Lephart SM. Neuromuscular and biomechanical
Hewett TE. Incidence of contralateral and ipsi- org/10.1016/j.jbiomech.2011.04.037 landing performance subsequent to ipsilateral
lateral anterior cruciate ligament (ACL) injury 132. Sadoghi P, von Keudell A, Vavken P. Effective- semitendinosus and gracilis autograft anterior
after primary ACL reconstruction and return to ness of anterior cruciate ligament injury preven- cruciate ligament reconstruction. Knee Surg
sport. Clin J Sport Med. 2012;22:116-121. http:// tion training programs. J Bone Joint Surg Am. Sports Traumatol Arthrosc. 2008;16:2-14.
dx.doi.org/10.1097/JSM.0b013e318246ef9e 2012;94:769-776. http://dx.doi.org/10.2106/ http://dx.doi.org/10.1007/s00167-007-0427-4
121. Paterno MV, Schmitt LC, Ford KR, et al. Biome- JBJS.K.00467 147. Valeriani M, Restuccia D, Di Lazzaro V, France-
chanical measures during landing and postural 133. Santello M, McDonagh MJ, Challis JH. Visual schi F, Fabbriciani C, Tonali P. Central nervous
stability predict second anterior cruciate liga- and non-visual control of landing movements in system modifications in patients with lesion of
ment injury after anterior cruciate ligament humans. J Physiol. 2001;537:313-327. the anterior cruciate ligament of the knee. Brain.
reconstruction and return to sport. Am J 134. Scheidt RA, Conditt MA, Secco EL, Mussa-Ivaldi 1996;119 pt 5:1751-1762.
Sports Med. 2010;38:1968-1978. http://dx.doi. FA. Interaction of visual and proprioceptive 148. Valeriani M, Restuccia D, Di Lazzaro V, Fran-
org/10.1177/0363546510376053 feedback during adaptation of human reaching ceschi F, Fabbriciani C, Tonali P. Clinical and

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45-05 Grooms.indd 392 4/15/2015 6:49:34 PM


neurophysiological abnormalities before and Human Movement. 4th ed. Hoboken, NJ: Wiley; construction. J Sport Rehabil. 2011;20:207-218.
after reconstruction of the anterior cruciate 2009. 158. Z abala ME, Favre J, Scanlan SF, Donahue J, An-
ligament of the knee. Acta Neurol Scand. 154. Wright RW, Dunn WR, Amendola A, et al. Risk driacchi TP. Three-dimensional knee moments
1999;99:303-307. of tearing the intact anterior cruciate ligament of ACL reconstructed and control subjects
149. Wade MG, Jones G. The role of vision and spa- in the contralateral knee and rupturing the
during gait, stair ascent, and stair descent.
tial orientation in the maintenance of posture. anterior cruciate ligament graft during the first
Phys Ther. 1997;77:619-628. 2 years after anterior cruciate ligament recon- J Biomech. 2013;46:515-520. http://dx.doi.
150. Warren WH, Jr., Kay BA, Zosh WD, Duchon AP, struction: a prospective MOON cohort study. org/10.1016/j.jbiomech.2012.10.010
Sahuc S. Optic flow is used to control human Am J Sports Med. 2007;35:1131-1134. http:// 159. Zanette G, Manganotti P, Fiaschi A, Tamburin
walking. Nat Neurosci. 2001;4:213-216. http:// dx.doi.org/10.1177/0363546507301318 S. Modulation of motor cortex excitability after
dx.doi.org/10.1038/84054 155. Wulf G. Attentional focus and motor learning: a upper limb immobilization. Clin Neurophysiol.
151. Webster KA, Gribble PA. Time to stabilization review of 15 years. Int Rev Sport Exerc Psychol. 2004;115:1264-1275. http://dx.doi.org/10.1016/j.
of anterior cruciate ligament-reconstructed 2013;6:77-104. http://dx.doi.org/10.1080/17509
clinph.2003.12.033
versus healthy knees in National Collegiate 84X.2012.723728
160. Zimny ML, Schutte M, Dabezies E. Mecha-
Athletic Association Division I female athletes. 156. Yoo JH, Lim BO, Ha M, et al. A meta-analysis of
J Athl Train. 2010;45:580-585. http://dx.doi. the effect of neuromuscular training on the pre- noreceptors in the human anterior cruciate
Downloaded from www.jospt.org at on September 6, 2022. For personal use only. No other uses without permission.

org/10.4085/1062-6050-45.6.580 vention of the anterior cruciate ligament injury ligament. Anat Rec. 1986;214:204-209. http://
152. Wikstrom EA, Tillman MD, Schenker S, in female athletes. Knee Surg Sports Traumatol dx.doi.org/10.1002/ar.1092140216
Borsa PA. Failed jump landing trials: deficits Arthrosc. 2010;18:824-830. http://dx.doi.
in neuromuscular control. Scand J Med org/10.1007/s00167-009-0901-2

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Sci Sports. 2008;18:55-61. http://dx.doi. 157. Yosmaoglu HB, Baltaci G, Kaya D, Ozer H. Track-
org/10.1111/j.1600-0838.2006.00629.x ing ability, motor coordination, and functional
153. Winter DA. Biomechanics and Motor Control of determinants after anterior cruciate ligament re- WWW.JOSPT.ORG
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